Psychophysical and neuroimaging responses to
moving stimuli in a patient with the Riddoch
phenomenon due to bilateral visual cortex lesions
Citation for published version (APA):
Arcaro, M. J., Thaler, L., Quinlan, D. J., Monaco, S., Khan, S., Valyear, K. F., Goebel, R., Dutton, G. N.,
Goodale, M. A., Kastner, S., & Culham, J. C. (2019). Psychophysical and neuroimaging responses to
moving stimuli in a patient with the Riddoch phenomenon due to bilateral visual cortex lesions.
Neuropsychologia, 128, 150-165. https://doi.org/10.1016/j.neuropsychologia.2018.05.008

Document status and date:
Published: 01/05/2019
DOI:
10.1016/j.neuropsychologia.2018.05.008
Document Version:
Publisher's PDF, also known as Version of record
Document license:
Taverne
Please check the document version of this publication:
• A submitted manuscript is the version of the article upon submission and before peer-review. There can
be important differences between the submitted version and the official published version of record.
People interested in the research are advised to contact the author for the final version of the publication,
or visit the DOI to the publisher's website.
• The final author version and the galley proof are versions of the publication after peer review.
• The final published version features the final layout of the paper including the volume, issue and page
numbers.
Link to publication

General rights
Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright
owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these
rights.
• Users may download and print one copy of any publication from the public portal for the purpose of private study or research.
• You may not further distribute the material or use it for any profit-making activity or commercial gain
• You may freely distribute the URL identifying the publication in the public portal.
If the publication is distributed under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license above,
please follow below link for the End User Agreement:
www.umlib.nl/taverne-license
Take down policy
If you believe that this document breaches copyright please contact us at:
repository@maastrichtuniversity.nl
providing details and we will investigate your claim.

Download date: 18 Apr. 2024

Neuropsychologia 128 (2019) 150–165

Contents lists available at ScienceDirect

Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia

Psychophysical and neuroimaging responses to moving stimuli in a patient
with the Riddoch phenomenon due to bilateral visual cortex lesions

T

Michael J. Arcaroa,b,c, Lore Thalerd, Derek J. Quinlane, Simona Monacof, Sarah Khang,
Kenneth F. Valyearh, Rainer Goebeli, Gordon N. Duttonj, Melvyn A. Goodalee,g, Sabine Kastnerb,c,
⁎
Jody C. Culhame,g,
a

Department of Neurobiology, Harvard Medical School, Boston, MA, USA
Department of Psychology, Princeton University, Princeton, NJ, USA
c
Princeton Neuroscience Institute, Princeton, NJ, USA
d
Department of Psychology, Durham University, Durham, UK
e
Brain and Mind Institute, University of Western Ontario, London, Ontario, Canada
f
Center for Mind and Brain Sciences, University of Trento, Trento, Italy
g
Department of Psychology, University of Western Ontario, London, Ontario, Canada
h
School of Psychology, University of Bangor, Bangor, Wales
i
Department of Cognitive Neuroscience, Maastricht University, Maastricht, The Netherlands
j
Department of Visual Science, Glasgow Caledonian University, Glasgow, UK
b

A R T I C LE I N FO

A B S T R A C T

Keywords:
Riddoch phenomenon
Blindsight
Vision
Motion perception
FMRI
Middle temporal area (MT+)

Patients with injury to early visual cortex or its inputs can display the Riddoch phenomenon: preserved
awareness for moving but not stationary stimuli. We provide a detailed case report of a patient with the Riddoch
phenomenon, MC. MC has extensive bilateral lesions to occipitotemporal cortex that include most early visual
cortex and complete blindness in visual field perimetry testing with static targets. Nevertheless, she shows a
remarkably robust preserved ability to perceive motion, enabling her to navigate through cluttered environments and perform actions like catching moving balls. Comparisons of MC's structural magnetic resonance
imaging (MRI) data to a probabilistic atlas based on controls reveals that MC's lesions encompass the posterior,
lateral, and ventral early visual cortex bilaterally (V1, V2, V3A/B, LO1/2, TO1/2, hV4 and VO1 in both
hemispheres) as well as more extensive damage to right parietal (inferior parietal lobule) and left ventral occipitotemporal cortex (VO1, PHC1/2). She shows some sparing of anterior occipital cortex, which may account
for her ability to see moving targets beyond ~15 degrees eccentricity during perimetry. Most strikingly, functional and structural MRI revealed robust and reliable spared functionality of the middle temporal motion
complex (MT+) bilaterally. Moreover, consistent with her preserved ability to discriminate motion direction in
psychophysical testing, MC also shows direction-selective adaptation in MT+. A variety of tests did not enable
us to discern whether input to MT+ was driven by her spared anterior occipital cortex or subcortical inputs.
Nevertheless, MC shows rich motion perception despite profoundly impaired static and form vision, combined
with clear preservation of activation in MT+, thus supporting the role of MT+ in the Riddoch phenomenon.

1. Introduction
In 1917, a Scottish neurologist, George Riddoch, described a phenomenon whereby five patients with occipital lobe injury, reported
seeing moving targets in the affected parts of the visual field even
though they could not see stationary targets. Although such patients
could perceive “something” moving, the items lacked form and were
often described as “vague and shadowy” (Riddoch, 1917). More generally, detection of moving but not static targets, sometimes called
⁎

statokinetic dissociation (SKD), has even been reported in neurologically intact individuals (Hudson and Wild, 1992; Safran and Glaser,
1980) but may be eliminated with careful methodology (Phu et al.,
2016); as such, the term Riddoch phenomenon is typically applied to
patients, while SKD can include typical individuals. Historically, a related phenomenon of “blindsight” described patients with damage to
visual cortex or its inputs, who could respond correctly to stimuli in
their blind fields of which they were unaware (Weiskrantz et al., 1974).
However, more recent accounts and taxonomies of blindsight

Corresponding author at: Brain and Mind Institute, University of Western Ontario, London, Ontario, Canada.
E-mail address: jculham@uwo.ca (J.C. Culham).

https://doi.org/10.1016/j.neuropsychologia.2018.05.008
Received 4 September 2017; Received in revised form 7 May 2018; Accepted 7 May 2018

Available online 09 May 2018
0028-3932/ © 2018 Elsevier Ltd. All rights reserved.

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

function can arise from spared “islands” of occipital tissue (Fendrich
et al., 1992); however, at least in some patients, this account is untenable (Kentridge et al., 1997).
Neuroimaging investigations of specific patients with blindsight
have provided support for the proposal of alternate subcortical pathways to MT+ and beyond. One patient, GY, who demonstrates the
Riddoch phenomenon (and blindsight), has been extensively studied
with psychophysical testing and neuroimaging. Functional magnetic
resonance imaging (fMRI) has shown that two patients, FS (Stoerig
et al., 1998) and GY (Zeki and Ffytche, 1998) show spared activation in
MT+ despite an absence of activation in V1 (ruling out spared islands
of processing). In GY, this activation was enhanced for fast motion and
trials during which he was aware of the movement (Zeki and Ffytche,
1998). Another patient studied with magnetoencepahalography (MEG)
showed responses in MT+ that preceded other extrastriate responses
(Schoenfeld et al., 2002), consistent with rapid subcortical inputs. The
signature of MT+ activation had been suggested as a possible means to
distinguish genuine blindsight from its absence (including cases arising
from confounds; Danckert and Culham, 2010); however, results have
been mixed. Some reports show activation in MT+ and intact LGNMT+ connections (Ajina et al., 2015b) or collicular-extrastriate connections (Leh et al., 2006) in patients with visual-field loss who demonstrate blindsight (including GY; Bridge et al., 2008) but not those
who do not. In contrast, another report shows multiple patients with
unilateral occipital damage and spared processing within and inputs to
ipsilesional MT+ , but without behavioral signatures of blindsight or
the Riddoch phenomenon (Barleben et al., 2015).
Some have argued that although patients with the Riddoch phenomenon can detect stimulus motion, under some circumstances, they
cannot discriminate motion direction (Azzopardi and Cowey, 2001;
Barton and Sharpe, 1997). Specifically, three patients with visual field
scotomata arising from occipital damage were able to detect a variety of
moving stimuli. However, they were able to discriminate direction for

acknowledge subtypes that may include awareness (Kentridge and
Heywood, 1999). Since Riddoch's seminal report, additional patients
have been reported showing the Riddoch phenomenon and have been
studied in terms of their perceptual reports (Schoenfeld et al., 2002;
Zappia et al., 1971) and in some cases, brain function (Stoerig et al.,
1998; Zeki and Ffytche, 1998). In addition, later research has also revealed a syndrome with the inverse dissociation to the Riddoch phenomenon, akinetopsia, in which a patient was able to see static images
but not perceive their movement (Zihl et al., 1983; Zihl et al., 1991).
Multiple accounts have been given for the Riddoch phenomenon
(and blindsight more generally). Most interestingly, the phenomenon
can be explained by the combination of damage to the primary visual
pathway (from retina to lateral geniculate nucleus, LGN, of the thalamus, to primary (striate) visual cortex, V1) and a sparing of alternate
pathways from subcortical structures (including the LGN, pulvinar, and
superior colliculus) to extrastriate cortex (reviewed in Ajina and Bridge,
2016). One extrastriate area that appears critical is the middle temporal
motion complex, MT+ (defined in humans based on the homology with
macaque area MT and its satellites; also called V5(+); Tootell et al.,
1995; Zeki et al., 1991), which provides output to areas within the
dorsal visual stream to guide actions (Milner and Goodale, 1995).
Subcortically, the LGN appears to be necessary for the preservation of
visual responses in adult extrastriate cortex. Visually evoked responses
are detectable in extrastriate cortex of adult monkeys with a lesioned
V1 (Collins et al., 2005; Schmid et al., 2013), but are extinguished by
inactivation of the LGN (Schmid et al., 2010). Additional subcorticalcortical pathways may also be sufficient for the preservation of cortical
visual function in the absence of V1 (Ajina and Bridge, 2018;
Mikellidou et al., 2017a) A retina-pulvino-MT pathway can also support
residual visual function in cortex following lesions to V1 early in life
(Warner et al., 2015). Collicular input to MT via the pulvinar may also
support visual function that bypasses V1 (Berman and Wurtz, 2010;
Rodman et al., 1990). An alternate account suggests that spared visual

Fig. 1. Extent of lesion. (A) Sagittal slices from MC's T1-weighted anatomical scans. MC's lesion included most of occipital cortex bilaterally as well as posterior
temporal cortex bilaterally and right parietal cortex. (B) MC's lesion (grey shading) projected onto an MNI surface with probabilistic estimates of 21 retinotopic areas
defined in neurologically intact participants (solid white lines). MC's lesion was classified into regions with that were completely lesioned and lacked any identifiable
tissue (darker transparent grey with black outline) and regions with abnormal tissue or atrophy (lighter transparent grey with black outline). MC's lesion encompassed early visual areas V1-V3 as well as extrastriate areas hV4, V3A, V3B, LO1–2, and VO1.
151

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

simple stimuli (single dots or bars), seemingly based on first-order
motion processing rather than feature tracking (Azzopardi and Hock,
2011), but not for more complicated patterns (gratings, plaids or
random dot kinematograms, RDKs). Patients were also unable to distinguish between incoherent (random) and fully (100%) coherent motion of RDKs. Moreover, the relationship between RDK coherence and
MT+ activation to RDKs in the blind fields of patients is abnormal
compared to their sighted fields or to controls, suggesting that in the
intact brain, V1 input shapes the response to coherence (Ajina et al.,
2015a).
In sum, although there are several well-described cases of the
Riddoch phenomenon and neuroimaging evidence supports the sparing
of motion processing via subcortical inputs to MT+ and beyond, many
uncertainties remain. The number of cases in the literature is small and,
in the most well-studied case of GY, the acquisition of his occipital lesion in childhood has led to concerns that the possibility of extensive
plasticity during development makes his case atypical. Moreover, while
psychophysical (e.g., Azzopardi and Cowey, 2001) and neuroimaging
(e.g., Zeki and Ffytche, 1998) studies of GY have shown detection and
neural responses to moving stimuli, our understanding would benefit
from further study and additional cases.
Here we provide the first detailed report of a new patient who shows
a clear case of the Riddoch phenomenon despite extensive bilateral
occipitotemporal lesions resulting from strokes. MC's verbal descriptions of her perceptual experience are striking. For example, she describes seeing rain moving down a window pane but cannot see the
stationary objects that would normally be visible through the window.
Her case is also striking in terms of the size of her lesions, which extend
well beyond the V1 lesions reported in most previous cases of the
Riddoch phenomenon (but see de Gelder et al., 2008 for a similar case
with comparably extensive lesions). Despite the absence of almost all
occipital cortex, MC's visual experiences are surprisingly rich, enabling
her not just to perceive moving stimuli, but to use her sense of motion
for everyday actions such as navigation and grasping.
Our goals here are twofold. First, we begin by providing a comprehensive case history of MC and detailed description of her structural
anatomy, including comparisons with probabilistic databases of visual
areas based on data from typical participants. The case details serve as a
foundation for our second but more central goal, to use fMRI and
psychophysics to investigate MC's preserved motion perception and its
neural substrates. The comprehensive case details can also provide a
foundation for ongoing and future studies of her abilities and interesting dissociations such as spared grasping of objects despite impaired
object perception (Goodale et al., 2008).
We expected that MC, like other patients with Riddoch phenomenon, would show preserved functionality of motion-selective extrastriate cortex, particularly MT+, and indeed she did. As such, additional tests were done to determine the nature of her residual motion
processing, particularly whether it included direction discrimination
neurally and behaviorally.

collapse and severe hypotension as a result of a lung infection. She
remained in a coma for 52 days, during which time she suffered a bilateral occipital infarction as initially revealed by a computerized tomography (CT) scan.
Upon her initial arousal from the coma, she reported no sense of
vision. Approximately six months later, she began to experience visual
phenomena (such as her first phenomenological report of perceiving the
reflections off a metallic gift bag) and described vivid sensations of
color, “like fireworks going off.” When she visited an ophthalmologist,
Dr. Gordon Dutton (co-author), two years after the initial incident, she
reported that she had no useful vision. Nevertheless, and much to her
own surprise, she was able to mirror arm movements made by the examiner and to walk around obstacles (Dutton, 2003).
MC's everyday phenomenology is fascinating. For example, Dutton
(2003, pp. 5–6) reported, “She can see rainwater running down a
window but cannot see through it. When her daughter is walking away
from her, she can see her daughter's pony tail moving from side to side
but cannot see her daughter. She can see the movement of the water
going down the plug hole but she cannot see her child in the bath.” She
described her visual experiences as “like being underwater,” as if
“you’re standing at the top of a bridge and look down at a stream - the
way water flows around with the current”. She remarked that she can
see outlines or blobs moving. Although she had noted such “weird” (in
her words) phenomenology, she discounted its validity because of
having been told that she was blind by a number of physicians. In fact,
since meeting Dr. Dutton and in participating in these experiments, she
frequently expressed a sense of vindication that her “strange” percepts
were legitimized.
Dr. Dutton encouraged her to develop strategies to use motion and
self-motion to improve her visual abilities and her confidence to trust
them. Specifically, at his encouragement, she learned to make side-toside head movements and acquired a rocking chair. Moreover, she
followed his advice to learn horseback riding at a school for the blind
and became quite proficient at it, becoming able to guide the horse at a
canter through a slalom course defined by traffic cones (See
Supplementary Video, Part A). She no longer requires self-motion
strategies to take advantage of her residual vision but reports that they
were very helpful initially. She easily navigates through obstacles (See
Supplementary Video, Part B) as could another patient with similar
bilateral occipital lesions (de Gelder et al., 2008) and an experimental
macaque named Helen with striate cortex lesions (Humphrey, 1974).
MC can also catch balls that are rolled or thrown towards her, moving
her arm to reach to the correct location and preshaping her hand appropriately, even when she is surprised by a different size than expected
(See Supplementary Video, Part C). Although she can reliably describe
the motion of stimuli, her descriptions of form are less reliable. As one
example, she may clearly report the experimenter's hand moving toward her, but not be able to tell reliably whether the thumb is pointing
up vs. down (See Supplementary Video, Part D). As another example,
she reported that when she first became visually aware, occasionally
she would reach down to the floor attempting to pick up a sunbeam or
pattern on the carpet, unaware that it was not an actual object.
Supplementary material related to this article can be found online at
http://dx.doi.org/10.1016/j.neuropsychologia.2018.05.008.
Over the past decade, MC's self-reports recorded in the clinical notes
describe continuing improvements in her residual vision abilities.
Clinical reports described abilities such as “reading” large letters by
tracing their forms by hand (with an acuity of approximately 1/60,
improving to 1/12 two years later when she no longer needed to trace
the letters but could imagine or pantomime doing so). During early
(2002) and later (2008) interviews, she reported palinopsia, the persistence of images such as colors, glare, and flash photographs for
seconds to hours. She reports vivid sensations of color, especially red
and yellow, though in case reports (2000) and in our own testing, her
reported percepts often do not match the actual color.
Prior to her incident, MC worked as a secretary at a hospital eye

2. Case history
MC is a right-handed female, born in 1969, with acquired bilateral
occipitotemporal lesions (Fig. 1A). Note that our patient MC is different
from another patient MC who demonstrates blindsight (Radoeva et al.,
2008). Several previous reports have provided brief descriptions of our
patient MC's case (Dutton, 2003) and have examined aspects of her
condition including spared haptic object recognition despite impaired
visual recognition (Snow et al., 2015), impairments in peripheral but
not central auditory motion perception (Thaler et al., 2016), activation
for sounds conveying material properties (Arnott et al., 2008), and
spared affective processing of faces (Striemer et al., 2017). Nevertheless, this is the first comprehensive report of her history and fullest
description of the lesioned and spared functional regions.
In February 1999, at age 30, MC experienced severe respiratory
152

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

comparable mask from the MNI template, then used a 12-parameter
linear registration (FSL's FLIRT) on these masks to align the shape of
MC's intact brain with the MNI template. This transformation was applied to MC's T1-weighted structural image, then a nonlinear registration (AFNI's 3dQwarp) was performed between a masked version of
MC's anatomy that only included intact tissue and a comparably masked
version of the MNI template. This nonlinear transformation was applied
to MC's unmasked T1 anatomical image, to the lesion mask, and all
functional datasets for mapping to the MNI template.

clinic for ten years. She is intelligent, high-functioning, highly motivated, and very personable, upbeat, and cooperative. She displays no
memory or cognitive deficits. She wears a prosthetic lower leg because
of an amputation related to the respiratory collapse. In everyday life,
she walks outdoors and on stairs with a cane and/or with assistance
from family members; however, she said she mostly uses the cane to
ensure that others realize she is blind and move out of the way.
Nonetheless, she can detect the presence of stairs and obstacles and
adjust her steps accordingly. She navigates inside her house without a
cane or assistance. She learned Grade 1 Braille but found it too challenging to progress further (perhaps due to the absence of visual cortex;
e.g., Cohen et al., 1997).
Goldmann perimetry (April 2011, carefully conducted by neuroophthalmologist Alex Fraser at Western's University Hospital in the
presence of the senior author and reported in Thaler et al., 2016) revealed no detection of static visual targets but spared perception of
moving targets presented in the upper left and lower right visual
quadrants. Earlier perimetry results were mixed, with one report of
spared motion processing across the visual field, particularly the lower
right visual field (2001, according to case reports), one report failing to
find any residual vision (2004, according to case reports), and one report indicating spared motion perception in the upper left visual field
(June 2007, at Western's University Hospital). These may indicate either simple variability in quality of the perimetry testing or in MC's
strategies and confidence. Alternatively, given that MC regularly reports verbally that her residual motion “keeps getting better”, there
may have been some functional recovery over the years; however, this
possibility is speculative.
MC has difficulty sustaining visual fixation. She has strabismus, with
concomitant left exotropia and hypertropia (i.e., her left eye deviates
outward and upward). Though Goldmann perimetry in 2011 was conducted only when MC was looking straight ahead, in general her ability
to maintain fixation is poor (as is typical of patients lacking foveal
cortex). As such, calibration of an eye tracker is non-trivial, making it
difficult to conduct eye tracking with any certainty.

3.3. Probabilistic atlases
Two probabilistic atlases were registered to the MNI template: (1) A
probabilistic atlas of 25 retinotopic areas (Wang et al., 2015) spanning
occipital cortex (V1, V2, V3, hV4), ventral temporal cortex (VO1, VO2,
PHC1, and PHC2), lateral occipital cortex (LO1, LO2, TO1 / hMT, TO2 /
MST), dorsal extrastriate (V3A, V3B), posterior parietal (IPS0, IPS1,
IPS2, IPS3, IPS4, IPS5, SPL1), and frontal cortex (FEF, IFS). (2) A
probabilistic atlas of anatomically defined MT based on cytoarchitecture (hOC5; Malikovic et al., 2007). A map of brain regions most
likely to show motion-selective activity was generated through a Neurosynth meta-analysis of 383 studies for regions active in experiments
that involved “motion” as a reverse inference (neurosynth.org; Yarkoni
et al., 2011). A surface model of the MNI template was used to visualize
correspondence between these probabilistic atlases and MC's lesion map
and to ensure reasonable co-registration.
3.4. Characterization of lesioned regions
MC's lesion comprises most of occipital cortex bilaterally and extends into posterior temporal cortex bilaterally and right parietal cortex
(Fig. 1B, Supplemental Figure 1). Some spared tissue is present in the
anterior calcarine sulcus bilaterally, parts of the collateral sulcus bilaterally, lateral occipital cortex including anterior parts of the lateral
occipital sulcus bilaterally, and the intraparietal sulcus in the right
hemisphere. To assess the relationship between MC's lesions and visual
areas, a map of her lesion was projected onto the MNI template and
compared with a probabilistic atlas of retinotopic areas (Wang et al.,
2015). Lesioned tissue comprised visual areas V1, V2, V3, hV4, V3A,
V3B, VO1, VO2, and approximately the posterior half of TO1 bilaterally. The lesion also covered VO2, PHC1, and PHC2 in the left
hemisphere. Tissue covering most of IPS0–4 and PHC1–2 in the right
hemisphere was abnormal with relatively thin grey matter and dark
surrounding white matter (as compared to the MNI volume template).
Abnormal tissue was also identified within anterior parts of V1 and V2
as well as parts of the fusiform and collateral sulcus in the right
hemisphere.
MC's lesion spared at least part of the cortex where the motion-selective MT+ complex would be expected. Human fMRI studies have
distinguished some of the subdivisions of the MT+ complex (Dukelow
et al., 2001; Huk et al., 2002). However, the correspondence between
functionally defined, retinotopy-defined and cytoarchitectonically defined cortical fields in this vicinity remains tentative (Amano et al.,
2009; Bridge, Clare, & Krug, 2014), making it difficult to determine
which specific portions are intact vs. damaged in MC. MC's lesion appeared to largely spare tissue in the expected location of a human occipital region, hOc5, proposed as equivalent to MT+ (Malikovic et al.,
2007; See Supplemental Figure 2). However, as shown in Fig. 1B (and
Supplemental Figure 2), the lesion overlapped with the posterior end of
the expected locus of one motion-sensitive retinotopic area in temporaloccipital cortex, TO1, suggested as the human homologue of MTproper, but largely spared adjacent motion-sensitive area TO2, suggested as the human homologue of MSTl (Amano et al., 2009). Tissue
within TO2 and the non-lesioned parts of lateral occipital cortex appeared abnormal with thinned grey matter. Comparisons with the
Neurosynth meta-analytic database suggested that MC's lesions largely

3. Structural magnetic resonance imaging
MC's structural anatomy has been previously described in brief
(Arnott et al., 2008; Snow et al., 2015; Thaler et al., 2016). Using
structural data collected in 2011, we conducted an extensive characterization of her anatomy by mapping her lesion, co-registering her
brain with the MNI template to enable comparisons with probabilistic
atlases.
3.1. Lesion mapping
As shown in Fig. 1B and Supplemental Figure 1, a mask of MC's
lesion extent was identified based on the T1-weighted structural image.
The mask contained two grades. The first comprised voxels that did not
have any clear remaining tissue. The second comprised voxels that
contained tissue that was clearly abnormal. This included regions of
grey matter where the cortical thickness was visibly thinner than
comparable regions of the MNI template and white matter regions
where the T1-weighted intensities were at least 20% less than that of
white matter in non-damaged regions of MC's brain. These regions typically surrounded the first grade of the mask. The complete volume of
MC's anatomical and lesion mask have been made publicly available
(Arcaro, 2017).
3.2. Anatomical registration with MNI template
Given the extent of MC's lesion, standard anatomical registration
methods yielded poor alignment with MNI template brain. To circumvent this issue, we first manually identified a brain mask of non-lesioned tissue from MC's T1-weighted structural volume and a
153

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

outward (run duration = 5 min, 4 s × 4 runs in two sessions). Data
were collected on a Siemens 3-Tesla Allegra scanner at the University of
Maastricht with a single-channel head coil. Functional data were collected at a 3.5-mm isotropic resolution [TR = 2 s; TE = 30 ms; flip
angle 90 deg.; 32 slices. Anatomical scans (ADNI MPRAGE) were collected at 1-mm isotropic resolution.

spared the regions most commonly activated by studies involving
“motion” (Supplemental Figure 2). In sum, comparisons of MC's brain
with three atlases from typical participants (based on cytoarchitectonic,
retinotopic and functional criteria) suggest that the tissue in MC's MT+
is at least partially spared, if not entirely normal. As such, fMRI will
provide a valuable means to assess the functionality of this region.
Thalamic visual structures appeared at least partially spared. The
LGN appeared atrophied in both hemispheres. There was also a small
lesion within the left posterior thalamus anterior to the visual pulvinar
(Supplemental Figure 1B; Arcaro et al., 2015), and overlapped with
subregions of somatosensory VP (Krauth et al., 2010; Morel et al.,
1997). The medial pulvinar was located just posterior to the lesion, but
did not overlap. Given some imprecision in the registration and individual variability, it is possible that the lesion includes anterior-most
parts of the medial pulvinar.

4.1.2. Visual responsiveness: Flickering checkerboards
To evaluate general visual responsiveness in MC's visual system, in
2011 we examined whether cortical and subcortical structures showed
increases in activity during viewing of checkerboard stimuli counterphase flickering at 4 Hz. We also examined whether contrast response
functions would be similar to those found in typical participants, with
strong gains in activation as a function of contrast for early visual areas
V1, V2, and V3, but not MT+ (Kastner et al., 2004; Tootell et al., 1995).
Three levels of root-mean-square contrast were used: 5%, 40%, and
100%. Full-field (30° diameter) checkerboard stimuli were presented in
blocks of 17.5 s and alternated with equally long presentations of black
screens as a baseline condition. During a given run, each contrast
condition was presented three times in pseudorandom order with the
constraint that all conditions were presented prior to the next repetition
(run duration = 5 mins, 37.5 s × 3 runs). A total of 15 blocks were
collected for each contrast level. Data were collected on a 3-Tesla Siemens TIM Trio scanner at the University of Western Ontario with a 12channel head coil. Functional data were collected at a 2-mm isotropic
resolution [TR = 2.5 s; TE = 40; flip angle = 70; 37 slices]. Anatomical
(T1-weighted) scans were collected at 1-mm isotropic resolution.

4. Methods
In brief, due to geographic constraints, MC was tested across multiple sessions over several years. Results are presented chronologically.
We began with initial psychophysical and fMRI tests in 2007
(University of Western Ontario), which suggested the foundations for
her Riddoch phenomenon – spared motion perception and spared
processing in MT+. fMRI tests were replicated and extended in later
sessions (2009, Maastricht University; 2011, University of Western
Ontario). Extensive psychophysical testing was conducted June and
September 2013, in Glasgow and at Durham University, respectively
with some stimuli using similar parameters as in the fMRI scans.
Psychophysical tests from 2007 showed similar effects as those from
2013 (motion detection abilities, highest sensitivity to low spatial and
high temporal frequencies, especially 4 Hz). Although results from 2007
provided some guidance for fMRI studies, they have not been included
here for conciseness and because they used criterion-dependent
methods (“Did you see motion? Yes/no”); whereas, the 2013 methods
used criterion-free methods (“Did you see motion in the first or second
interval?”) and included much more testing.

4.1.3. Direction-selective adaptation for random dots
In 2011, we used an fMRI adaptation paradigm (Grill-Spector et al.,
1999) to determine whether activation in MT+ (and other regions)
would show direction-selective adaptation for RDKs, as shown previously in neurologically intact participants (Konen and Kastner, 2008).
That is, we tested whether motion responses would be reduced when
motion direction was repeated vs. variable, a population-level signature
of direction-selective neurons.
Pilot psychophysical tests (2007) suggested that MC had high sensitivity to low spatial frequencies and high temporal frequencies (replicated with more rigor in 2013, see Sections 4.2.2.1 and 5.2.2.1). As
such, in fMRI pilot testing, we first showed MC a variety of dot patterns
to see which patterns evoked the strongest sense of motion. In fact, MC
was unable to perceive any motion in the conventional displays. Based
on this, rather than the fine RDK displays previously used for typical
participants (e.g., 1000 dots with 0.15° diameter; Konen and Kastner,
2008), we used a display with fewer (50) and larger (2.85°) dots within
a 30° circular aperture at a velocity of 22°/s.
Moving dot stimuli were presented in 16-s blocks in which random
dots moved continuously in one direction (adapted blocks) or changed
direction every second (non-adapted blocks). We investigated two
conditions of optic flow: planar and radial motion. In planar motion,
dots moved leftward or downward. In radial motion, random dots
moved away from the central point of the screen. Within a non-adapted
block, motion directions were presented in pseudorandom order with
the constraint that all conditions were presented prior to the next repetition. Each run consisted of six blocks (three adapted and three nonadapted) of moving dots and alternated with equally long presentations
of stationary dots. Each run started and ended with a blank (no visual
stimulation) period that lasted for 20 s. The order of specific motion
directions was randomized across scans (run duration = 3 mins, 52 s ×
5 runs). A total of 15 adapted and 15 non-adapted blocks (5 × motion
direction) were collected. Data were collected on a 3-Tesla Siemens TIM
Trio scanned at the University of Western Ontario with a 12-channel
head coil. Functional data were collected at a 3-mm isotropic resolution
[TR = 2 s; TE = 30; flip angle = 70; 37 slices]. Anatomical (T1weighted) scans were collected at 1-mm isotropic resolution.

4.1. Functional magnetic resonance imaging
4.1.1. Motion-selectivity: Moving vs. stationary checkerboards
Given MC's spared motion perception, we initially examined whether her brain, particularly the middle temporal motion complex, MT+,
showed preferential activation to moving vs. stationary stimuli. Data
was collected on two occasions to compare activation for a moving
checkerboard to a stationary checkerboard (in 2007), sometimes also in
comparison to a blank screen (in 2008). The checkerboard loomed and
receded (changing direction every 2 s), with radial motion chosen to
minimize the likelihood of eye movements. MC was instructed to try to
gaze at a red fixation point in the centre of the display; however, given
her problems maintaining fixation, it is unlikely that she was able to do
so. Nevertheless, given that our interest is in whether she shows responses to motion or not, it is not critical whether the visual motion
arose from stimulus motion and/or retinal motion.
In 2007, the display cycled through 16-s blocks of stationary and
moving checkerboards of 30° diameter (run duration = 3 min, 24 s × 5
runs). Data were collected on a 4-Tesla Varian-Siemens UNITY INOVA
whole-body imaging system at the University of Western Ontario using
a single-channel occipital surface coil. Functional data (T2 * -weighted,
gradient-echo echoplanar imaging) were collected at a resolution of
3 mm x 3 mm in-plane × 4 mm slice thickness (× 25 slices) with a
volume acquisition time of 2 s (based on 2 segments/plane at a time to
repeat, TR, = 1000 ms; time to echo, TE = 15 ms; flip angle = 60 deg.,
navigator-echo-corrected). Anatomical (T1-weighted) scans were collected at a 1-mm isotropic resolution.
In 2008, the display cycled through 16-s blocks of a blank screen, a
static checkerboard, and a checkerboard that oscillated inward and
154

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

4.2. Psychophysical testing

4.1.4. Resting-state functional connectivity
In 2011, we collected a single, 8-minute rest scan for functional
connectivity analyses. The lights were turned off in the scanner and no
visual stimuli were presented. MC was instructed to remain still for the
duration of the scan and to keep her eyes shut. Functional data were
collected at a 3-mm isotropic resolution [TR = 2 s; TE = 30; flip angle
= 70; 37 slices].

Psychophysical tests were run for a variety of stimuli: checkerboards, RDKs, gratings and dots to address behavioral performance
useful for interpreting fMRI data. Stimuli were run using VPixx software
(v. 2.8.4; VPixx Technologies Inc.) on a calibrated MacBook Pro laptop
and its internal screen or a Mac Mini with a Samsung SyncMaster 2333
monitor (60-Hz refresh rate). MC was tested across four days (in June &
Sept. 2013). Viewing distance was 57 cm. Testing relied on forcedchoice procedures that are criterion-free.

4.1.5. fMRI preprocessing and data analysis
Functional scan data were analyzed using Analysis of Functional
NeuroImages (AFNI), SUMA, Freesurfer, BrainVoyager, and MATLAB.
For each scan session, all images were aligned to a single time point for
that session, detrended and motion corrected. The experiment on
moving vs. stationary checkerboards (Section 4.1.1) and ROI analyses
for other experiments (sections 4.12, 4.13) used spatially unsmoothed
data; all analyses that involved mapping to the MNI surface (Sections
4.1.2, 4.1.3, 4.1.4) used data that were spatially filtered using a
Gaussian filter of 4 mm full-width at half maximum. This smoothing
kernel was chosen to increase signal to noise ratio while maintaining
spatial specificity. The spatial filtering also improved volume-to-surface
mapping by compensating for small imprecisions in the registration
between MC's brain and the MNI template. Each scan was normalized to
its mean. A multiple-regression analysis in the framework of a general
linear model was performed on the localizer experiments. Each stimulus
condition was modeled with a canonical hemodynamic response function. For later data (excluding moving vs. flickering checkerboards),
additional regressors that accounted for variance due to baseline shifts
between scans, linear drifts, and head motion parameter estimates were
also included in the regression model. Due to the time course normalization, beta coefficients were scaled to reflect percentage signal
change. Data for the moving vs. stationary checkerboards was aligned
Talairach space and resampled at a 3-mm isotropic resolution.

4.2.1. Random dot kinematograms
We examined MC's ability to detect motion and discriminate motion
direction using RDKs with parameters comparable to those used for
fMRI testing. The display subtended 30° of visual angle. Given possible
differences between linear and complex motion, we examined three
categories of movement: translation (left/right and, in some cases, up/
down), flow (expansion/contraction) and rotation (clockwise/counterclockwise). Fifty dots diameter 2.85° moved at a speed of 22° (visual
angle)/s (for translation and expansion/contraction and 90° (rotational
angle)/s (for rotation)) with an unlimited lifetime. Dots were white on a
black background for a contrast near 100% (Macbook Pro screen: white
= 127.1 cd/m2; black = 1.4 cd/m2; maximum Michelson contrast =
97.8%; Mac Mini with SyncMaster: white: 202.8 cd/m2; black =
0.2 cd/m2; maximum Michelson contrast = 99.8%).
4.2.1.1. Motion detection. On each trial, an RDK was shown that was
either stationary or moving at 100% coherence for 6 s. MC had to make
a 2-alternative forced-choice decision about whether the stimulus was
moving or stationary. In total, MC completed 120 trials for translation
(80 left-right; 40 up-down), 160 trials for rotation, and 80 trials for
flow. Trials were grouped by motion category in blocks of 40.
4.2.1.2. Motion category discrimination. On each trial, an RDK with
100% coherence was shown for 6 s, reversing direction every 2 s within
one of the three categories of motion (translation, flow or rotation). MC
had to make a 3-alternative forced-choice decision about which
category of motion was shown. In total, MC completed 120 trials (in
blocks of 30).

4.1.5.1. Analysis of motion direction and alternating contrast checkerboard
experiments. To estimate the response magnitude for each stimulus
block within an ROI, the mean signal was extracted and block responses
were normalized (to motion onset for the moving vs. stationary
checkerboards and to the mean activity during 4 s preceding stimulus
onset for other data). The time window corresponding to the peak
activity for each block (8–18 s for motion adaptation and 7.5–17.5 s for
checkerboard contrast) was averaged to derive estimates of the
response for each stimulus condition. For the contrast experiment, an
analysis of variance (ANOVA) was run for each ROI to evaluate whether
activity across blocks varied as a function of contrast. Post-hoc t-tests
were conducted when appropriate. For the motion adaptation
experiment, an unpaired t-test was run for each ROI to evaluate
whether activity across blocks significantly differed between adapted
and non-adapted conditions. An analysis of variance was also run to
assess whether activity varied across the three motion adaptation types.

4.2.1.3. Opposite motion direction discrimination. On each trial, a RDK
was shown that moved in one of two opposite directions with 100%
coherence for 6 s. MC had to make a 2-alternative forced-choice
decision about which of the two directions was shown. In total, MC
completed 240 trials (60 left-right translation, 20 up-down translation,
60 rotation, 100 flow) in blocks of 20 grouped by motion category.
4.2.1.4. Opposite motion direction discrimination as a function of
coherence. On each trial, an RDK was shown for 6 s in which a
certain percentage of the dots (3.125–100%) moved coherently while
the others moved randomly. MC had to make a 2-alternative forcedchoice decision about which of the two motion directions was shown. In
total, MC completed 1008 trials (432 left-right; 192 up-down; 192
rotation; 192 flow) in blocks of 48.

4.1.5.2. Analysis of functional connectivity data. For correlation and ICA
analyses, several additional steps were performed on the data: (1)
removal of signal deviation > 2.5 SDs from the mean (AFNI's
3dDespike); temporal filtering retaining frequencies in the
0.01–0.1 Hz band; (3) linear and quadratic detrending; and (4)
removal by linear regression of several sources of variance: (i) six
motion parameter estimates (three translation and thee rotation) and
their temporal derivatives, (ii) the signal from a ventricular regions,
(iii) the signal from a white matter region, (iv) the signal from the
lesion region. Global mean signal removal was not included in the
analysis. To minimize the effect of any evoked response due to the
scanner onset, the initial 10 (20 s) TRs were removed from the rest scan.
Seed-based Pearson correlation and independent component analyses
(ICA) were conducted on rest data. Regions of interest for correlation
analyses were defined based on the motion localizer in 2011.

4.2.2. Gratings and bars
4.2.2.1. Gratings: Spatiotemporal sensitivity. To characterize MC's
spatiotemporal sensitivity profile, MC was presented with trials
containing two sequential stimuli, one of which had a vertically
oriented sine-wave grating that could move right or left and that
filled the rectangular display. MC had to make a 2-alternative forcedchoice decision about which interval contained the moving grating.
Gratings were presented at four spatial frequencies (0.5, 1, 2, or 4
cycles/°) and four temporal frequencies (0, 2, 4, or 8 Hz). MC performed
six blocks of testing (12 trials/spatiotemporal combination) for a 100%
contrast grating presented for 500 ms or 2000 ms (which didn’t affect
155

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

showed a checkerboard flickering at 4 Hz and the other a blank screen.
MC had to make a 2-alternative forced-choice decision about which
interval contained the flickering checkerboard. The monitor was calibrated to ensure accurate contrast levels. The checkerboard included 24
radial cycles x 6 concentric cycles on a grey screen. MC completed 40
trials per contrast level (10 blocks of 32 trials/block over two testing
days).

performance, so data were collapsed).
4.2.2.2. Grating and bar motion. To test whether MC's direction
discrimination was poorer for complex than simple stimuli, as
suggested by other patients with blindsight (Azzopardi and Cowey,
2001), we showed her either a square-wave grating or a single bar that
moved in one of four directions orthogonal to its orientation (vertical
stimuli moved left or right; horizontal stimuli moved up or down) for a
duration of 2 s. MC had to make a 4-alternative forced-choice decision
about which of the four motion directions was shown. In total, MC
completed 120 trials for the grating stimulus and 80 trials for the bar
stimulus in blocks of 40. Both the grating and bar had 100% contrast
(black bars on white background in a square-wave profile). The
stimulus subtended 16° (grating and bar) x 16° (grating) or 1° (bar).
Because the grating had a spatial frequency of 0.5 cycles/°, there were 8
black bars and 8 white bars, each 1° wide, equivalent to the width of the
single bar. Both the grating and the bar drifted at 8°/s (corresponding to
a temporal frequency of 4 Hz for the grating) as smoothly as possible
given the maximum refresh rate of the monitor (60 Hz). In sum, the size
and velocity of the single bar equated to those for one bar of the grating.

5. Results
5.1. Functional magnetic resonance imaging
5.1.1. Motion-selectivity: Moving vs. stationary checkerboards
To assess which regions could support MC's preserved motion perception, motion responses were measured throughout visual cortex
with fMRI. MC had dramatic nonverbal and verbal responses when she
first saw moving checkerboards. We were unable to use an eye tracker
in the scanner; nevertheless, we aimed an MR-compatible bore camera
(MRC Systems) toward her eyes to approximately monitor her gaze,
which did shift, particularly up and down. At the onset of the first block
of a moving checkerboard, MC's eyes began watering and her cheek
moved, as seen through the bore camera. At the end of that scan, when
asked if she saw motion, said, “That was amazing. I could see thousands
of things. I’ve never seen so much motion. I can’t believe it! I was crying
and laughing.”
fMRI scanning in 2007 and 2008 revealed that MC showed motion-

4.2.3. Checkerboards: Contrast response functions
We examined MC's contrast response functions across a range of
Michelson contrast levels (100%, 40%, 20%, 10%, 5%, 2.5%, 1%, 0.5%)
that included those tested with fMRI (100%, 40% and 5%). On each
trial, MC was presented with two sequential stimuli, one of which

Fig. 2. Motion responses in MT+ for looming/receding vs. static checkerboards. (A) MC was scanned while viewing 16-s blocks of a static checkerboard, a
looming/receding checkerboard and a blank screen. A contrast of moving > stationary revealed strong activation in dorsal and ventral subregions of MT+ in both
hemispheres. Slice planes are specified in Talairach coordinates and indicated by dashed lines in orthogonal slices. (B) Time courses of activation extracted from
subregions in A show the expected rise in activation with the onset of motion and decline with the offset, consistent with the hemodynamic response function.
Activation was particularly robust in left dorsal MT+.
156

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

Fig. 3. Visual responses in anterior calcarine cortex for visual checkerboards vs. a blank screen. (A) A contrast of moving and stationary checkerboards vs. a
blank screen revealed activation in anterior calcarine cortex, just posterior to the intersection of the calcarine sulcus with the parieto-occipital sulcus. This region
showed no statistically significant difference between moving and static checkerboards. Slice planes are specified in Talairach coordinates and indicated by thin black
dashed lines in orthogonal slices. The parieto-occipital is indicated by solid white line. The calcarine sulcus is indicated by dashed white line. (B) The time course of
activation extracted from the region in A shows the expected rise in activation with the onset of checkerboard stimuli and decline with the offset, consistent with the
hemodynamic response function.

selective activation within MT+ (Fig. 2 and Supplemental Figure 3,
which shows considerable intersession consistency even across years
and scanners). Based on previous studies in neurologically intact participants, MT+ activation would be expected near the junction of the

inferior temporal and lateral occipital sulci (Watson et al., 1993), often
in the ascending limb of the inferior temporal sulcus (Dumoulin et al.,
2000). Motion-selective activation in MC's brain lay at the posterior
edge of MC's spared tissue and included two clusters in each hemisphere

Fig. 4. MC's perimetry and visual field responsiveness. We combined probabilistic retinotopic maps (polar angle on the left and eccentricity on the right) from an
atlas based on neurologically intact participants (A) with MC's visually evoked activity for flickering checkerboard stimuli (shown in orange in (B)). The comparison
suggested that MC may have spared vision in the upper left visual field beyond ~12°(C) consistent with her perimetry data (D, modified from data in Thaler et al.,
2016), which indicated sparing of sensitivity for moving (but not static) targets within the upper left visual field beyond ~10°.
157

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

far peripheral vision (Mikellidou et al., 2017b). Because we were unable to obtain retinotopic maps in MC (due to her inability to maintain
fixation), we cannot definitively determine whether her anterior calcarine activation focus corresponds to prostriata or anterior visual
cortex, both of which represent the visual periphery. Based on the
neuroanatomical locus (posterior to the parieto-occipital sulcus) and
Talairach coordinates, MC's anterior calcarine focus appears more
medial, posterior and superior than the expected prostriata focus
(x = 0, y = −78, z = 16; compared to x = −20, y = −61, z = 1 in
Mikellidou et al., 2017a).

consistent with the sulcal location of MT+: (1) dorsally, within the
ascending limb of the inferior temporal sulcus and (2) ventrally within
the inferior temporal sulcus. Though it is tempting to suggest that the
enhanced activation in 2008 compared to 2007 may indicate some
recovery of MT+, consistent with MC's self-reports that her motion
perception improved, substantive differences between scanners and
protocols may account for the differences.
In addition to the activation in MT+, MC also showed activation in
the anterior calcarine sulcus, just posterior to its intersection with the
parieto-occipital sulcus, POS, as shown in Fig. 3. This region was activated comparably by both moving and static checkerboards compared
to a blank screen but showed no significant motion selectivity. Activation was also observed in the expected location of left human V6/
V6A (also known as superior parieto-occiptial cortex) at the anterior
POS (Pitzalis et al., 2006, 2013).
A recent human fMRI study (Mikellidou et al., 2017b) suggests the
POS-calcarine intersection is the site of a scarcely studied but intriguing
motion-selective visual area, prostriata, previously only reported in
other primates (reviewed in Rockland, 2012; e.g., Yu et al., 2012). The
boundary between human prostriata and adjacent V1 has a mirror reversal of eccentricity maps and prostriata disproportionately represents

5.1.2. Visual responsiveness: Flickering checkerboards
To assess whether any of MC's other remaining visual cortex was
functional, visual responses were measured throughout visual cortex
with fMRI. Visual responsiveness was assessed by contrasting blocks of
full-field, full-contrast checkerboard stimulation flickering at 4 Hz interleaved with blank periods (Supplemental Figure 4). Increased activity to checkerboard stimulation was observed in parts of anterior
calcarine cortex in the right hemisphere (corresponding to peripheral
V1 representing the left hemifield), ventral temporal cortex within and
around the collateral sulcus in the right hemisphere, lateral temporal
Fig. 5. Motion direction selectivity. (A) MC viewed
blocks in which coarse RDKs moved in the same direction
on every trial (adapted condition) or changed from trial to
trial (non-adapted condition) in 16-s blocks. (B)
Significantly greater activity to moving vs. static dots was
observed within right dorsal and ventral MT+ (as well as
right ventral MT+, not shown) (p < 0.01, uncorrected).
(C) In right ventral MT+, activation was significantly
higher for non-adapted vs. adapted motion blocks, a signature of direction selectivity. Vertical dashed line marks
stimulus onset. Shaded region illustrates SEM across
blocks. (D) Sensitivity to motion direction observed in
dorsal subdivision of MT+ bilaterally as well as motionsensitive regions of the intraparietal sulcus. Motion direction sensitivity (or motion sensitivity in general) was
not observed in occipital or ventral temporal cortex.

158

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

to maintain fixation during fMRI scanning (during which no eye monitoring occurred). Thus, the correspondence between the spatial representation of MC's perimetry and fMRI activation should be interpreted with some caution.
To further test the functionality of this remaining tissue in occipital
cortex, responses to the checkerboard stimulus were assessed at three
different contrasts (5%, 40%, and 100%; Supplemental Figure 4C-D).
Previous examinations of contrast response functions in typical participants found that while the fMRI signal increased as a function of
contrast in most visual areas (V1-V4A) and LGN, the MT+ response
showed little or no gain (Kastner et al., 2004; Tootell et al., 1995).
Within the spared part of anterior calcarine cortex, activity across
blocks varied as a function of contrast (ANOVA, main effect of contrast;
F(2,42) = 5.23; p = 0.009). Anterior calcarine cortex activity increased
monotonically from 5% to 40–100% contrast. Post-hoc unpaired t-tests,
revealed a significant difference between 5% and 100% contrasts (t
(28) = 3.34; p = 0.002) and a between 5% and 100% (t(28) = 2.01;
p = 0.05). The mean responses across contrasts also varied for ventral
temporal cortex and the LGN in the right hemisphere, but these differences were not significant (F(2,42) < 0.93; p > 0.41). The signal
within the LGN was particularly noisy, likely due in part to the small
number of voxels. Results from MT+ were uncertain: although activity
appeared to increase with contrast for both dorsal and ventral subdivisions, statistically the effects did not reach significance. Taken together, these results suggest that the remaining tissue in MC's occipital
cortex has at least some preserved visual function and could potentially
support her preserved visual sensitivity.

cortex within and around the inferior temporal sulcus bilaterally, and
anterior parietal cortex in the left hemisphere (Supplemental Figure 4A,
p < 0.0001). Subcortical activity within the LGN and superior colliculus (SC) was observed at a lower threshold (Supplemental Figure 4B;
p < 0.01).
Visual responses within MC's anterior calcarine cortex were consistent with the visual field locations in which she can perceive moving
(but not static) targets. MC's visually evoked responses were compared
with a probabilistic map of V1's visual field coverage in typical participants (Fig. 4A; Wang et al., 2015). Note that because we did not
measure retinotopy in MC herself (due to her inability to maintain
fixation), any comparison with maps from typical participants is necessarily speculative. Also note that probabilistic maps in controls
predated the discovery of human prostriata (Mikellidou et al., 2017b)
and mapping only extended to 15° eccentricity; as such, this data does
not enable us to distinguish V1 from prostriata.
Visual activity to checkerboards in MC was only detected within
zones that represent eccentricities greater than 13° (Fig. 4B + C). The
strongest visual responses were localized to the upper left periphery,
consistent with MC's spared visual sensitivity from perimetry as described in an earlier report (Fig. 4D; Thaler et al., 2016). Though the
fMRI mapping in typical participants only extended to 15° eccentricity
(vs. 90° eccentricity in perimetry testing in MC), MC has intact tissue
anterior to the V1 activity, corresponding to further peripheral parts of
V1 and/or area prostriata, suggesting that this tissue would have been
visually responsive if stimulated. Though MC maintained fixation
during perimetry testing (verified by eye monitoring), she was unable

Fig. 6. MT+ resting-state connectivity. When the time course from each subdivision of MT+ was used as a seed for resting-state correlations, functional connectivity with other subdivisions, including the opposite hemisphere and relatively consistent network of other regions was revealed (r > 0.4). In both hemispheres,
ventral, but not dorsal, MT+ was correlated with the small portion of residual V1 in occipital cortex. Correlations with IPS were observed for both dorsal and ventral
MT+ seeds though were stronger in the left hemisphere. Dashed, semi-transparent white circles denote seed region. Solid white circular outlines illustrate MT+ in
the hemisphere opposite that of the seed.
159

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

together, these data suggest that MC's MT+ and motion-sensitive IPS is
capable of discriminating motion direction and could support her residual direction discrimination abilities.

5.1.3. Direction-selective adaptation for random dots
To assess the degree to which MC's MT+ was functional, responses
to particular motion directions were assessed using an fMRI adaptation
paradigm. fMRI scanning in 2011 confirmed the presence of motionselective activity within MC's MT+ bilaterally as well as within the
intraparietal sulcus (IPS). Two clusters of activity were again identified
within the region of MT+. Activity within both MT+ and IPS was
modulated by the direction of motion (Fig. 5). An fMRI adaptation
paradigm was used to probe the sensitivity of MC's motion-selective
areas to particular direction of motion, as had been previously investigated in typical participants (Konen and Kastner, 2008). MC was
scanned while viewing blocks of uniform translational (left and down)
and flow (outward) and blocks of alternating motion directions
(Fig. 5A). In all motion-selective areas, responses to blocks of alternating (i.e. non-adapted) motion were significantly larger than blocks
of repeated (adapted) motion (Fig. 5C-D; unpaired t-test; t(28) > 2.77;
p < 0.01). In contrast, sensitivity to motion stimulation was not detected within occipital or ventral temporal cortex. The remaining tissue
in both occipital and ventral temporal cortex in the right hemisphere
was visually responsive to full field flickering checkerboard stimuli
(Supplementary Figure 4), but neither region showed motion- (vs.
static) selective activity nor differential activity between mixed and
repeated motion blocks (t(28) < 0.92; p > 0.37). The profile of motion responses across MC's remaining visual cortex resembles typical
activity patterns in healthy individuals where responses to different
motion directions, as assessed by motion adaptation, are strongest
within MT+, FEF, and parietal cortex and weakest within early visual
cortex (Konen and Kastner, 2008; but see Lee and Lee, 2012). Taken

5.1.4. Resting-state functional connectivity
The functional organization of MT+ and MC's remaining visual
cortex was further evaluated using functional connectivity analyses on
data collected during a long rest scan in the absence of visual stimulation. The activity of MC's motion-sensitive areas was correlated at rest
(Fig. 6). When seeding the dorsal and ventral MT+ clusters, spatially
focal correlations (r > 0.4; t(227) > 6.58; p < 0.00001) were observed with the dorsal MT+ ROI in the opposite hemisphere as well as
motion-sensitive regions of posterior parietal cortex, including right
V3A (Tootell et al., 1997) and IPS0–4 (Konen and Kastner, 2008). Both
dorsal and ventral MT+ were correlated with anterior occipital cortex.
Using a complementary data-driven ICA (Supplemental Figure 5),
other activity networks were identified within and around MT+. One
IC map was identified comprising posterior parietal cortex and parts of
lateral temporal cortex within and around MT+. The IC map most
closely resembled the dorsal attention network (Fox et al., 2005). Another IC map was identified within anterior parietal cortex, anterior
lateral temporal cortex, and frontal cortex, and likely overlaps with
tool-selective and grasping regions (Culham and Valyear, 2006; Konen
et al., 2013). A third IC map was identified within the inferior parietal
lobule and the posterior cingulate / precuneus, and most closely resembled the default mode network (Fox et al., 2005). Taken together,
these data provide additional support that MC's motion sensitive regions are functionally similar and are distinct from surrounding cortex.

Fig. 7. Motion psychophysics results. For high-contrast (98%+ contrast) random dot kinematograms (RDKs) with larger-than-typical dot sizes (2.85°), MC showed
above-chance performance for (A) motion detection, (B) discrimination of motion translation, rotation and flow and (C) discrimination opposite directions of motion
for translation and rotation (with mixed results for flow). (D) Moreover, for all categories of motion, her direction discrimination scaled with motion coherence
(though results for flow were noisier). (E) MC was best able to detect gratings at low spatial and high temporal frequencies. MC showed a poorer ability to
discriminate motion direction for (F) square-wave gratings than (G) single bar of the grating.
160

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

5.2. Motion psychophysical testing
Because MC's lesion mapping and fMRI revealed partial sparing of
MT+, the degree of MC's preserved behavioral sensitivity for moving
stimuli was tested in a series of psychophysical experiments.
5.2.1. Random dot kinematograms
5.2.1.1. Motion detection. As shown in Fig. 7A, for all conditions, MC
could discriminate moving from stationary dots with at least 90%
accuracy (94.7% across all trials; chance = 50%). Errors were mostly
reports of perceived motion when stationary dots were presented
(8.3%) rather than a failure to perceive motion when moving dots
were presented (2.2%).
5.2.1.2. Motion category discrimination. As shown in Fig. 7B, when MC
was shown three categories of motion (translation, rotation or flow),
she could discriminate the category with 95.8% accuracy (where
chance was 33%).

Fig. 8. Psychophysical contrast response functions. In a 2-alternative
forced-choice decision, MC's ability to detect a flickering checkerboard increased logarithmically within contrast.

5.2.1.3. Opposite motion direction discrimination. As shown in Fig. 7C,
MC could discriminate between opposite motion directions with 100%
accuracy for translation and rotation. Her performance for flow was
more mixed. For the first two blocks of the first session, she performed
worse than chance, 15%, even when the experimenter asked her to
speak her answers, indicating that she could discern the two directions
but not label them correctly. For the last two blocks of the first session
and one block in the second session she got 100% correct.

been made publicly available as NIFTI images (Arcaro, 2017).
6. Discussion
Our psychophysical and neuroimaging studies of Patient MC provide a detailed characterization of a new case of the scarcely studied
Riddoch phenomenon. Most notably, the results show that MC has a
rich perceptual experience of motion that is accompanied by robust and
reliable activation in visual area MT+ even though it abuts her extensive occipitotemporal lesions. Moreover, both her perception of
motion and fMRI activation in MT+ go beyond a simple response to
motion. Behaviorally, she cannot only detect motion but also shows an
ability to discriminate motion direction; neurally, she shows a response
not just to the presence of motion but also direction-selective adaptation. These results reinforce those highlighting the central role of MT+
in motion perception in Riddoch patients (Schoenfeld et al., 2002; Zeki
and Ffytche, 1998).
In addition, the careful characterization of MC's case and neuroanatomy provides a foundation for understanding her case in ongoing
and future studies. Though Riddoch phenomenon is a striking aspect of
MC's case, she also displays other phenomena akin to blindsight and
perception-action dissociations (Goodale et al., 2008). These may be
related to the particular details of her case, including lesions in the
ventral visual stream (which include LO) and a partially spared dorsal
visual stream (particularly in the left hemisphere). As with other rare
patients such as a DF, a patient with visual form agnosia who shows
perception-action dissociations (Goodale and Milner, 1992), the combination of behavioral testing along with structural and functional
neuroimaging (Bridge et al., 2013; James et al., 2003) has enabled more
sophisticated understanding of behavioral/neural dissociations.

5.2.1.4. Opposite motion direction discrimination as a function of
coherence. As shown in Fig. 7D, for all three motion categories, as
motion coherence increased, so did MC's ability to discriminate
between opposite directions of motion. Her performance scaled
linearly on a log scale. For all categories, her performance was
excellent at full coherence (consistent with Fig. 7A). However, at
lower levels of coherence, her performance differed across category,
with the best performance for rotational and translational motion (with
similar performance for left-right and up-down) and poorer and more
variable performance for flow. Her performance in flow at low
coherence was lower than chance, indicating that as with the 100%
coherence condition in Fig. 7D, her response mapping for flow direction
is unreliable.
5.2.2. Gratings and bars
5.2.2.1. Gratings: Spatiotemporal sensitivity. Although performance was
somewhat variable, as shown in Fig. 7E, there was a clear trend in
which MC's performance for detecting gratings was best for
combinations of low spatial and high temporal frequencies (e.g.,
100% correct for 0.5 cycles/° at 8 Hz vs. 61% correct for 4 cycles/° at
0 Hz, i.e., stationary).
5.2.2.2. Grating and bar motion. As shown in Fig. 7F and G, MC's ability
to discriminate among four directions of motion was indeed poorer for
square-wave gratings (67%) than for a single bar within the grating
(91%). In particular, MC made many errors for horizontal gratings
moving downward, which she often perceived as upward.

6.1. What does MC's case reveal about motion processing in the Riddoch
phenomenon?
MC's case shows that even with considerable damage to a wide
swath of early visual areas, rich motion perception can be preserved
and utilized for daily functions such as navigation and visually guided
actions like catching a ball. We propose that such spared motion perception is enabled by the sparing of processing in the motion-selective
complex MT+ in humans. MC clearly shows activation at the expected
location of MT+ based on its sulcal location (Dumoulin et al., 2000), as
well as comparisons with probabilistic atlases derived from neurologically intact participants using retinotopic mapping (Wang et al., 2015),
cytoarchitectonic divisions (Malikovic et al., 2007), and functional
meta-analyses (Yarkoni et al., 2011). Moreover, our resting-state connectivity data suggest that the subdivisions of MT+ are interconnected

5.2.3. Checkerboards: Contrast response functions
As in typical observers (Kastner et al., 2004; Schade, 1956; Watson,
2000), MC's contrast response function showed an increase in accuracy
as a function of contrast that increased logarithmically when plotted on
a linear scale (and thus linearly when plotted on a logarithmic scale, R2
= 0.93; Fig. 8).
5.3. Data availability
MC's T1 anatomical volume, lesion mask, and MT localizer have
161

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

6.3. From where does the input to MT+ arise?

with one another and other motion-selective regions. As with other
patients with the Riddoch phenomenon and/or blindsight, even with
damage to the primary pathway, subcortical pathways may provide
input to MT+ (Bridge et al., 2008; Leh et al., 2006).
There may also be cases in which MT+ activation is found in the
absence of the Riddoch phenomenon, that is, without motion awareness
(Barleben et al., 2015). Our experiences suggest one possible account
for MT+ activation in the absence of the Riddoch phenomenon may be
a suboptimal choice of stimuli. MC's behavioral detection and discrimination abilities require an optimal combination of low spatial and
high temporal frequencies, scale approximately linearly with contrast
rather than saturating at low contrasts as expected, and vary widely
across stimuli (e.g., better for translation and rotation than flow, better
for bars than gratings, and present only for coarse but not fine dot
patterns). As such, it seems particularly important for future studies to
ensure that a range of stimuli are behaviorally tested and optimized
prior to imaging. Another possible account for MT+ activation in the
absence of motion awareness is that MT+ may be necessary but not
sufficient for conscious awareness.
MC's data show that residual motion processing in the Riddoch
phenomenon goes beyond mere detection of motion but also extends to
direction selectivity. Behaviorally, MC was able to discern the direction
of dots, bars and gratings substantially better than chance (sometimes
with 100% correct). At the neural level, MT+ showed direction-selective adaptation in MC as in past studies of neurologically intact participants (Konen and Kastner, 2008). This finding contradicts the hypothesis that cortically blind patients are able to discriminate direction
only for simple stimuli like bars and single dots but not for more
complex stimuli like gratings or plaids in their scotomata (Azzopardi
and Cowey, 2001). Although we did find that MC performed better at
direction discrimination with a single bar than a grating as would have
been predicted by Azzopardi & Cowey, nevertheless, she could discriminate direction better than chance for the grating and almost perfectly for coarse RDKs. These results suggest that at least some patients
can discriminate direction when stimuli are optimized for their spatiotemporal sensitivity. The better discrimination for a single bar than a
grating may result from differences in motion mechanisms (e.g., easier
attentive tracking with a single bar than a crowded grating; Cavanagh,
1992).

Our testing thus far has not enabled us to determine the source of
input to MT+ with certainty. Of course, the most common explanation
for residual vision is based on subcortical routes to MT+ (including a
colliculo-pulvinar route and a koniocellular LGN route). We had hoped
to discern the contribution of subcortical inputs from LGN and/or SC
via the pulvinar through a variety of methods, including examining
contrast response functions, resting-state connectivity, and diffusion
tensor imaging (not shown). Though visual responses were observed in
MC's LGN and SC, the results from each of these approaches were inconclusive.
A second possibility is that the inputs may be arising from partially
preserved tissue in the anterior calcarine cortex, which may correspond
to peripheral V1 or perhaps even the prostriata region. MC's spared
anterior calcarine tissue may account for her spared motion perimetry
in the peripheral upper left quadrant. Activation in this spared region
scales with luminance contrast and shows resting-state correlations
with MT+. However, its responses differed from MT+; specifically,
unlike MT+ it showed negligible motion selectivity for checkerboards
and no evidence of direction-selective adaptation for RDKs (however,
even in neurologically intact controls, adaptation is weak in V1, V2 and
V3, according to Konen and Kastner, 2008 and unknown in prostriata).
Some have speculated that prostriata may play a role in blindsight
and related phenomena (Rockland, 2012) but evidence is scarce. In
non-human primates, prostriata is characterized by a strong emphasis
on the visual periphery and very short response latencies (Yu et al.,
2012). Prostriata has direct connections to peripheral MT (Palmer and
Rosa, 2006). Recently, a comparable area has been reported in humans
that also lies anterior to V1, represents the far periphery, and responds
best to very fast motion (Mikellidou et al., 2017b) and luminance flicker
(Dechent and Frahm, 2003). Although MC's prostriata appears anatomically preserved, further testing using functional (Mikellidou et al.,
2017b) and anatomical criteria (Glasser et al., 2016, supplemental
neuroanatomical results) would be needed to distinguish it from anterior visual cortex.
In total, MC's spared anterior calcarine, which represents the visual
periphery and may correspond to anterior V1 or prostriata, may play a
role in her awareness of motion and spared MT+ activation. However,
we must emphasize that it certainly does not enable “normal” processing. Most strikingly, MC's peripheral vision does not enable many other
visual functions such as awareness of static targets or good form recognition.

6.2. Potential implications for clinical practice
Though speculative, MC's case raises the possibility that changes to
clinical practice may facilitate recovery in patients with cortical
blindness. Such patients tend to be told by the medical profession that
visual recovery will not occur, and MC was no exception. However,
during the first two years following her brain injury, progressively
improving movement perception took place, akin to the cases described
by Riddoch (1917), yet her percepts were questioned by clinicians.
When she presented two years after her brain injury, she was only
conscious of movement, but unaware that this might accord the facility
to use vision to guide her movements once more. After being encouraged by her clinician to take advantage of her spared motion perception, MC gained confidence in her newfound abilities and continues
to report ongoing improvements. Of course, we cannot exclude the
possibility that her behavioral recovery would have happened regardless. Nevertheless, studies have demonstrated that perceptual training
for complex movement stimuli can yield improvements in motion
perception that generalize to new retinal locations, stimuli and tasks
(Cavanaugh et al., 2017; Cavanaugh and Huxlin, 2017; Das et al., 2014;
Huxlin et al., 2009; Melnick et al., 2016) MC's case history raises the
possibility that even everyday activities may also have the potential to
yield everyday benefits with low costs, though empirical validation
would be necessary.

6.4. Caveats of MC's case and single case studies
There are numerous caveats to MC's case; however, with careful
consideration these should not detract from the value of her case.
We must emphasize that we are not claiming that MC's perception
or activation fall within the range of normal controls. Any comparisons
with controls are indirect, based on the fact that MT+ is one of the most
robust and reliable visual areas to find in individuals (Tootell et al.,
1995; Watson et al., 1993) and many of the experiments were motivated by previous effects in controls (e.g., Kastner et al., 2004; Konen
and Kastner, 2008). To make any claims of normal functionality, we
would need to test a reasonably sized sample of control participants
(ideally age- and sex-matched) on our task and determine whether MC
fell within or outside the expected norms. However, we are not making
such claims, only emphasizing that MC shows robust motion activation
that was very replicable across stimuli, paradigms, and even scanners
over six years and that on a single-subject level, she shows statistically
significant direction discrimination.
Another caveat to MC's case is that in the absence of foveal cortex
(and the presence of strabismus), eye tracking calibration and testing
was not straightforward. Thus, it is quite possible, even likely, that MC
was moving her eyes during testing. However, we must emphasize that
162

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

Eimeren and Kevin Stubbs for assistance with data collection and
analysis and an anonymous reviewer for drawing our attention to the
possible role of area prostriata in MC's case.

regardless of whether her motion detection and discrimination abilities
are due to stimulus motion, retinal motion from eye movements, or
some combination, she retains those abilities. Without the ability to
assess calibrated fixation, our attempts to examine perception and activation at different retinotopic locations were not successful.
Nevertheless, the assessment of her structural data with respect to a
normative atlas, provides some clues as to the sparing of early retinotopic cortex.

Appendix A. Supplementary material
Supplementary data associated with this article can be found in the
online version at http://dx.doi.org/10.1016/j.neuropsychologia.2018.
05.008.

6.5. MC's case in the bigger picture
References
Given the paucity and idiosyncrasies of patients with the Riddoch
phenomenon, MC's case provides a valuable addition to the literature
that can serve as an example and foundation for ongoing and future
studies.
MC's case bears striking similarities to another patient, TN (de
Gelder et al., 2008). TN, like MC, had multiple strokes that led to extensive bilateral lesions in early visual cortex and many spared abilities,
including locomotion and navigation. The degree to which TN displays
the Riddoch phenomenon is unclear. Perimetry for static and flickering
targets revealed no spared vision (though moving targets do not appear
to have been tested); however, TN “sporadically claims to ‘feel’ the
occurrence of visual movement” and shows spared MT+ activation for
looming dots (compared to receding or rotating motion or static dots)
(Hervais-Adelman et al., 2015). Despite his considerable visual impairment, TN can discriminate positive and negative facial expressions,
and his amygdala exhibits increased activity when viewing faces with
emotional expressions (Burra et al., 2017; Pegna et al., 2005). Interestingly, MC has also been shown to discriminate facial emotions better
than chance even though she could not discriminate facial gender
(Striemer et al., 2017). Patients MC and TN also share functional similarities with another patient, BI, who also has bilateral occipital
damage (which in his case arose in early development), and shows
spared navigational abilities and affective processing (Mundinano et al.,
2017).
The registration and comparison of MC's structural anatomy with an
atlas of visual areas based on control participants will facilitate the
interpretation of behavioral and neuroimaging phenomena. Already,
we have shown that, despite damage to an area putatively important for
both tactile and visual shape processing (LOtv subdivision of the lateral
occipital complex; Amedi et al., 2001), MC shows preserved tactile
shape processing (Snow et al., 2015). The new structural imaging
analyses help clarify exactly which divisions of lateral occipital cortex
are implicated. Preliminary testing and analysis also suggests that MC
shows a dissociation between visual perception and visually guided
actions (Goodale et al., 2008) and her case is likely to provide a valuable additional case of this rare dissociation (Goodale and Milner, 1992;
Karnath et al., 2009).

Ajina, S., Bridge, H., 2016. Blindsight and unconscious vision: what they teach us about
the human visual system. Neuroscientist. http://dx.doi.org/10.1177/
1073858416673817.
Ajina, S., Bridge, H., 2018. Subcortical pathways to extrastriate visual cortex underlie
residual vision following bilateral damage to V1. Neuropsychologia. http://dx.doi.
org/10.1016/j.neuropsychologia.2018.01.007.
Ajina, S., Kennard, C., Rees, G., Bridge, H., 2015a. Motion area V5/MT+ response to
global motion in the absence of V1 resembles early visual cortex. Brain 138 (1),
164–178. http://dx.doi.org/10.1093/brain/awu328.
Ajina, S., Pestilli, F., Rokem, A., Kennard, C., Bridge, H., 2015b. Human blindsight is
mediated by an intact geniculo-extrastriate pathway. ELife 4, 1–23. http://dx.doi.
org/10.7554/eLife.08935.
Amano, K., Wandell, B.A., Dumoulin, S.O., 2009. Visual field maps, population receptive
field sizes, and visual field coverage in the human MT+ complex. J. Neurophysiol.
102 (5), 2704–2718. http://dx.doi.org/10.1152/jn.00102.2009.
Amedi, A., Malach, R., Hendler, T., Peled, S., Zohary, E., 2001. Visuo-haptic object-related activation in the ventral visual pathway. Nat. Neurosci. 4 (3), 324–330. http://
dx.doi.org/10.1038/85201.
Arcaro, M., 2017. MC T1 anatomical. Harv. Dataverse. http://dx.doi.org/10.7910/DVN/
OEFOEI.
Arcaro, M.J., Pinsk, M.A., Kastner, S., 2015. The anatomical and functional organization
of the human visual pulvinar. J. Neurosci. 35 (27), 9848–9871. http://dx.doi.org/10.
1523/JNEUROSCI.1575-14.2015.
Arnott, S.R., Cant, J.S., Dutton, G.N., Goodale, M.A., 2008. Crinkling and crumpling: an
auditory fMRI study of material properties. NeuroImage 43 (2), 368–378. http://dx.
doi.org/10.1016/j.neuroimage.2008.07.033.
Azzopardi, P., Cowey, A., 2001. Motion discrimination in cortically blind patients. Brain
124 (1), 30–46. http://dx.doi.org/10.1093/brain/124.1.30.
Azzopardi, P., Hock, H.S., 2011. Illusory motion perception in blindsight. Proc. Natl.
Acad. Sci. USA 108 (2), 876–881. http://dx.doi.org/10.1073/pnas.1005974108.
Barleben, M., Stoppel, C.M., Kaufmann, J., Merkel, C., Wecke, T., Goertler, M.,
Schoenfeld, M.A., 2015. Neural correlates of visual motion processing without
awareness in patients with striate cortex and pulvinar lesions. Hum. Brain Mapp. 36
(4), 1585–1594. http://dx.doi.org/10.1002/hbm.22725.
Barton, J.J.S., Sharpe, J.A., 1997. Motion direction discrimination in blind hemifields.
Ann. Neurol. 41 (2), 255–264. http://dx.doi.org/10.1002/ana.410410217.
Berman, R.A., Wurtz, R.H., 2010. Functional identification of a pulvinar path from superior colliculus to cortical area MT. J. Neurosci. 30 (18), 6342–6354. http://dx.doi.
org/10.1523/JNEUROSCI.6176-09.2010.
Bridge, H., Thomas, O., Jbabdi, S., Cowey, A., 2008. Changes in connectivity after visual
cortical brain damage underlie altered visual function. Brain 131 (6), 1433–1444.
http://dx.doi.org/10.1093/brain/awn063.
Bridge, H., Thomas, O.M., Minini, L., Cavina-Pratesi, C., Milner, A.D., Parker, A.J., 2013.
Structural and functional changes across the visual cortex of a patient with visual
form agnosia. J. Neurosci. 33 (31), 12779–12791. http://dx.doi.org/10.1523/
JNEUROSCI.4853-12.2013.
Burra, N., Hervais-Adelman, A., Celeghin, A., de Gelder, B., Pegna, A.J., 2017. Affective
blindsight relies on low spatial frequencies. Neuropsychologia. http://dx.doi.org/10.
1016/j.neuropsychologia.2017.10.009.
Cavanagh, P., 1992. Attention-based motion perception. Science 257 (5076), 1563–1565.
(Retrieved from). 〈http://www.ncbi.nlm.nih.gov/pubmed/1523411〉.
Cavanaugh, M.R., Barbot, A., Carrasco, M., Huxlin, K.R., 2017. Feature-based attention
potentiates recovery of fine direction discrimination in cortically blind patients.
Neuropsychologia. http://dx.doi.org/10.1016/j.neuropsychologia.2017.12.010.
Cavanaugh, M.R., Huxlin, K.R., 2017. Visual discrimination training improves Humphrey
perimetry in chronic cortically induced blindness. Neurology 88 (19), 1856–1864.
http://dx.doi.org/10.1212/WNL.0000000000003921.
Cohen, L.G., Celnik, P., Pascual-leone, A., Corwell, B., Faiz, L., Hallett, M., Catala, M.D.,
1997. Functional relevance of cross-modal plasticity in blind humans. Nature
389, 5–8.
Collins, C.E., Lyon, D.C., Kaas, J.H., 2005. Distribution across cortical areas of neurons
projecting to the superior colliculus in new world monkeys. Anat. Rec. Part A Discov.
Mol. Cell. Evolut. Biol. 285 (1), 619–627. http://dx.doi.org/10.1002/ar.a.20207.
Culham, J.C., Valyear, K.F., 2006. Human parietal cortex in action. Curr. Opin. Neurobiol.
16 (2), 205–212. http://dx.doi.org/10.1016/j.conb.2006.03.005.
Danckert, J., Culham, J.C., 2010. Reflections on blindsight: neuroimaging and behavioural explorations clarify a case of reversed localisation in the blind field of a patient with hemianopia. Can. J. Exp. Psychol. 64 (2), 86–101. http://dx.doi.org/10.
1037/a0017426.
Das, A., Tadin, D., Huxlin, K.R., 2014. Beyond blindsight: properties of visual relearning

6.6. Conclusion
Here we described a neuropsychological case characterized by a
combination of psychophysical testing and structural MRI, and taskbased and resting-state functional MRI. With many criteria considered
in combination, MC's case supports a key role for the MT+ motion
complex in the Riddoch phenomenon, including key features such as
direction selectivity, even for complex stimuli such as gratings or plaids.
Acknowledgements
This work was supported by a Discovery Grant from the Natural
Sciences and Engineering Research Council of Canada (RGPIN-201604748) and an Operating Grant from the Canadian Institutes of Health
Research to JCC, and by grants from the National Institutes of Health
(RO1MH064043 and RO1EY017699) and the National Science
Foundation (BCS1025149 and BCS1328270) to SK. We thank Lucia van
163

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.
in cortically blind fields. J. Neurosci. 34 (35), 11652–11664. http://dx.doi.org/10.
1523/JNEUROSCI.1076-14.2014.
de Gelder, B., Tamietto, M., van Boxtel, G., Goebel, R., Sahraie, A., van den Stock, J.,
Pegna, A., 2008. Intact navigation skills after bilateral loss of striate cortex. Curr.
Biol. 18 (24). http://dx.doi.org/10.1016/j.cub.2008.11.002.
Dechent, P., Frahm, J., 2003. Characterization of the human visual V6 complex by
functional magnetic resonance imaging. Eur. J. Neurosci. 17 (10), 2201–2211.
http://dx.doi.org/10.1046/j.1460-9568.2003.02645.x.
Dukelow, S.P., DeSouza, J.F., Culham, J.C., van den Berg, A.V., Menon, R.S., Vilis, T.,
2001. Distinguishing subregions of the human MT+ complex using visual fields and
pursuit eye movements. J. Neurophysiol. 86 (4), 1991–2000. (Retrieved from).
〈http://www.ncbi.nlm.nih.gov/pubmed/11600656〉.
Dumoulin, S.O., Bittar, R.G., Kabani, N.J., Baker, C.L., Le Goualher, G., Pike, G.B., Evans,
A.C., 2000. A new anatomical landmark for reliable identification of human area V5/
MT: a quantitative analysis of sulcal patterning. Cereb. Cortex 10 (5), 454–463.
(Retrieved from). 〈http://www.ncbi.nlm.nih.gov/pubmed/10847595〉.
Dutton, G.N., 2003. Cognitive vision, its disorders and differential diagnosis in adults and
children: knowing where and what things are. Eye 17 (3), 289–304. http://dx.doi.
org/10.1038/sj.eye.6700344/r6700344. (pii).
Fendrich, R., Wessinger, C.M., Gazzaniga, M.S., 1992. Residual vision in a scotoma: implications for blindsight. Science 258 (5087), 1489–1491. (Retrieved from). 〈http://
www.ncbi.nlm.nih.gov/pubmed/1439839〉.
Fox, M.D., Snyder, A.Z., Vincent, J.L., Corbetta, M., Van Essen, D.C., Raichle, M.E., 2005.
The human brain is intrinsically organized into dynamic, anticorrelated functional
networks. Proc. Natl. Acad. Sci. USA 102 (27), 9673–9678. http://dx.doi.org/10.
1073/pnas.0504136102.
Glasser, M.F., Coalson, T.S., Robinson, E.C., Hacker, C.D., Harwell, J., Yacoub, E., Van
Essen, D.C., 2016. A multi-modal parcellation of human cerebral cortex. Nature 536
(7615), 171–178. http://dx.doi.org/10.1038/nature18933.
Goodale, M.A., Milner, A.D., 1992. Separate visual pathways for perception and action.
Trends Neurosci. 15 (1), 20–25. (Retrieved from). 〈http://www.ncbi.nlm.nih.gov/
pubmed/1374953〉.
Goodale, M.A., Wolf, M.E., Whitwell, R.L., Brown, L.E., Cant, J.S., Chapman, C.S., Dutton,
G.N., 2008. Preserved motion processing and visuomotor control in a patient with
large bilateral lesions of occipitotemporal cortex. J. Vision. 8, 371. http://dx.doi.org/
10.1167/8.6.371.
Grill-Spector, K., Kushnir, T., Edelman, S., Avidan, G., Itzchak, Y., Malach, R., 1999.
Differential processing of objects under various viewing conditions in the human
lateral occipital complex. Neuron 24 (1), 187–203. (Retrieved from). 〈http://www.
ncbi.nlm.nih.gov/pubmed/10677037〉.
Hervais-Adelman, A., Legrand, L.B., Zhan, M., Tamietto, M., de Gelder, B., Pegna, A.J.,
2015. Looming sensitive cortical regions without V1 input: evidence from a patient
with bilateral cortical blindness. Front. Integr. Neurosci. 9, 1–12. http://dx.doi.org/
10.3389/fnint.2015.00051.
Hudson, C., Wild, J.M., 1992. Assessment of physiologic statokinetic dissociation by
automated perimetry. Invest. Ophthalmol. Vis. Sci. 33 (11), 3162–3168. (Retrieved
from). 〈http://www.ncbi.nlm.nih.gov/pubmed/1399422〉.
Huk, A.C., Dougherty, R.F., Heeger, D.J., 2002. Retinotopy and functional subdivision of
human areas MT and MST. J. Neurosci. 22 (16), 7195–7205 (https://doi.org/
20026661).
Humphrey, N.K., 1974. Vision in a monkey without striate cortex: a case study.
Perception 3 (3), 241–255.
Huxlin, K.R., Martin, T., Kelly, K., Riley, M., Friedman, D.I., Burgin, W.S., Hayhoe, M.,
2009. Perceptual relearning of complex visual motion after V1 damage in humans. J.
Neurosci. 29 (13), 3981–3991. http://dx.doi.org/10.1523/JNEUROSCI.4882-08.
2009.
James, T.W.T.W., Culham, J.C., Humphrey, G.K.K., Milner, A.D.D., Goodale, M.A.M.A.,
2003. Ventral occipital lesions impair object recognition but not object-directed
grasping: an fMRI study. Brain 126 (Pt 11), 2463–2475. http://dx.doi.org/10.1093/
brain/awg248.
Karnath, H.-O., Ruter, J., Mandler, A., Himmelbach, M., 2009. The anatomy of object
recognition–visual form agnosia caused by medial occipitotemporal stroke. J.
Neurosci. 29 (18), 5854–5862. http://dx.doi.org/10.1523/JNEUROSCI.5192-08.
2009.
Kastner, S., O’Connor, D.H., Fukui, M.M., Fehd, H.M., Herwig, U., Pinsk, M.A., 2004.
Functional imaging of the human lateral geniculate nucleus and pulvinar. J.
Neurophysiol. 91 (1), 438–448. http://dx.doi.org/10.1152/jn.00553.2003.
Kentridge, R.W., Heywood, C.A., 1999. The status of blindsight. J. Conscious. Stud. 6 (5),
3–11.
Kentridge, R.W., Heywood, C.A., Weiskrantz, L., 1997. Residual vision in multiple retinal
locations within a scotoma: implications for blindsight. J. Cogn. Neurosci. 9 (2),
191–202. http://dx.doi.org/10.1162/jocn.1997.9.2.191.
Konen, C.S., Kastner, S., 2008. Representation of eye movements and stimulus motion in
topographically organized areas of human posterior parietal cortex. J. Neurosci. 28
(33), 8361–8375. http://dx.doi.org/10.1523/JNEUROSCI.1930-08.2008.
Konen, C.S., Mruczek, R.E.B., Montora, J.L., Kastner, S., 2013. Functional organization of
human posterior parietal cortex: grasping- and reaching-related activations relative
to topographically organized cortex. J. Neurophysiol. 2897–2908. http://dx.doi.org/
10.1152/jn.00657.2012.
Krauth, A., Blanc, R., Poveda, A., Jeanmonod, D., Morel, A., Székely, G., 2010. A mean
three-dimensional atlas of the human thalamus: generation from multiple histological
data. NeuroImage 49 (3), 2053–2062. http://dx.doi.org/10.1016/j.neuroimage.
2009.10.042.
Lee, H.A., Lee, S.-H., 2012. Hierarchy of direction-tuned motion adaptation in human
visual cortex. J. Neurophysiol. 107 (8), 2163–2184. http://dx.doi.org/10.1152/jn.
00923.2010.

Leh, S.E., Johansen-Berg, H., Ptito, A., 2006. Unconscious vision: new insights into the
neuronal correlate of blindsight using diffusion tractography. Brain 129 (7),
1822–1832. http://dx.doi.org/10.1093/brain/awl111.
Malikovic, A., Amunts, K., Schleicher, A., Mohlberg, H., Eickhoff, S.B., Wilms, M., Zilles,
K., 2007. Cytoarchitectonic analysis of the human extrastriate cortex in the region of
V5/MT+: a probabilistic, stereotaxic map of area hOc5. Cereb. Cortex 17 (3),
562–574. http://dx.doi.org/10.1093/cercor/bhj181.
Melnick, M.D., Tadin, D., Huxlin, K.R., 2016. Relearning to see in cortical blindness.
Neuroscientist 22 (2), 199–212. http://dx.doi.org/10.1177/1073858415621035.
Mikellidou, K., Arrighi, R., Aghakhanyan, G., Tinelli, F., Frijia, F., Crespi, S., Morrone,
M.C., 2017a. Plasticity of the human visual brain after an early cortical lesion.
Neuropsychologia 0–1. http://dx.doi.org/10.1016/j.neuropsychologia.2017.10.033.
Mikellidou, K., Kurzawski, J.W., Frijia, F., Montanaro, D., Greco, V., Burr, D.C., Morrone,
M.C., 2017b. Area prostriata in the human brain. Curr. Biol. 27 (19), 3056–3060.
http://dx.doi.org/10.1016/j.cub.2017.08.065.
Milner, A.D., Goodale, M.A., 1995. The Visual Brain in Action. Oxford University Press,
Oxford, U.K.
Morel, A., Magnin, M., Jeanmonod, D., 1997. Multiarchitectonic and stereotactic atlas of
the human thalamus. J. Comp. Neurol. 387 (4), 588–630. (Retrieved from). 〈http://
www.ncbi.nlm.nih.gov/pubmed/9373015〉.
Mundinano, I.-C., Chen, J., de Souza, M., Sarossy, M.G., Joanisse, M.F., Goodale, M.A.,
Bourne, J.A., 2017. More than blindsight: case report of a child with extraordinary
visual capacity following perinatal bilateral occipital lobe injury. Neuropsychologia.
http://dx.doi.org/10.1016/j.neuropsychologia.2017.11.017.
Palmer, S.M., Rosa, M.G.P., 2006. A distinct anatomical network of cortical areas for
analysis of motion in far peripheral vision. Eur. J. Neurosci. 24 (8), 2389–2405.
http://dx.doi.org/10.1111/j.1460-9568.2006.05113.x.
Pegna, A.J., Khateb, A., Lazeyras, F., Seghier, M.L., 2005. Discriminating emotional faces
without primary visual cortices involves the right amygdala. Nat. Neurosci. 8 (1),
24–25. http://dx.doi.org/10.1038/nn1364.
Phu, J., Al-Saleem, N., Kalloniatis, M., Khuu, S.K., 2016. Physiologic statokinetic dissociation is eliminated by equating static and kinetic perimetry testing procedures. J.
Vision. 16 (14), 5. http://dx.doi.org/10.1167/16.14.5.
Pitzalis, S., Galletti, C., Huang, R.-S., Patria, F., Committeri, G., Galati, G., Sereno, M.I.,
2006. Wide-field retinotopy defines human cortical visual area V6. J. Neurosci. 26
(30), 7962–7973. http://dx.doi.org/10.1523/JNEUROSCI.0178-06.2006.
Pitzalis, S., Sereno, M.I., Committeri, G., Fattori, P., Galati, G., Tosoni, a., Galletti, C.,
2013. The human homologue of macaque area V6A. NeuroImage 82, 517–530.
http://dx.doi.org/10.1016/j.neuroimage.2013.06.026.
Radoeva, P.D., Prasad, S., Brainard, D.H., Aguirre, G.K., 2008. Neural activity within area
V1 reflects unconscious visual performance in a case of blindsight. J. Cogn. Neurosci.
20 (11), 1927–1939. http://dx.doi.org/10.1162/jocn.2008.20139.Neural.
Riddoch, G., 1917. Dissociation of visual perceptions due to occipital injuries, with
especial reference to appreciation of movement. Brain 40, 15–57.
Rockland, K.S., 2012. Visual system: prostriata–a visual area off the beaten path. Curr.
Biol. 22 (14), R571–R573. http://dx.doi.org/10.1016/j.cub.2012.05.030.
Rodman, H.R., Gross, C.G., Albright, T.D., 1990. Afferent basis of visual response properties in area MT of the macaque. II. Effects of superior colliculus removal. J.
Neurosci. 10 (4), 1154–1164. (Retrieved from). 〈http://www.ncbi.nlm.nih.gov/
pubmed/2329373〉.
Safran, A.B., Glaser, J.S., 1980. Statokinetic dissociation in lesions of the anterior visual
pathways. A reappraisal of the Riddoch phenomenon. Arch. Ophthalmol. 98 (2),
291–295. http://dx.doi.org/10.1001/archopht.1980.01020030287009.
Schade, O.H., 1956. Optical and photoelectric analog of the eye. J. Opt. Soc. Am. 46 (9),
721–739. (Retrieved from). 〈http://www.ncbi.nlm.nih.gov/pubmed/13358013〉.
Schmid, M.C., Mrowka, S.W., Turchi, J., Saunders, R.C., Wilke, M., Peters, A.J., Leopold,
D.A., 2010. Blindsight depends on the lateral geniculate nucleus. Nature 466 (7304),
373–377. http://dx.doi.org/10.1038/nature09179.
Schmid, M.C., Schmiedt, J.T., Peters, A.J., Saunders, R.C., Maier, A., Leopold, D.A., 2013.
Motion-sensitive responses in visual area V4 in the absence of primary visual cortex.
J. Neurosci. 33 (48), 18740–18745. http://dx.doi.org/10.1523/JNEUROSCI.392313.2013.
Schoenfeld, M.A., Noesselt, T., Poggel, D., Tempelmann, C., Hopf, J.M., Woldorff, M.G.,
Hillyard, S.A., 2002. Analysis of pathways mediating preserved vision after striate
cortex lesions. Ann. Neurol. 52 (6), 814–824. http://dx.doi.org/10.1002/ana.10394.
Snow, J.C., Goodale, M.A., Culham, J.C., 2015. Preserved Haptic Shape Processing after
Bilateral LOC Lesions. J. Neurosci. 35 (40), 13745–13760. http://dx.doi.org/10.
1523/JNEUROSCI.0859-14.2015.
Stoerig, P., Kleinschmidt, A., Frahm, J., 1998. No visual responses in denervated V1: highresolution functional magnetic resonance imaging of a blindsight patient.
Neuroreport 9 (1), 21–25. http://dx.doi.org/10.1097/00001756-199801050-00005.
Striemer, C.L., Whitwell, R.L., Goodale, M.A., 2017. Affective blindsight in the absence of
input from face processing regions in occipital-temporal cortex. Neuropsychologia
1–8. http://dx.doi.org/10.1016/j.neuropsychologia.2017.11.014.
Thaler, L., Paciocco, J., Daley, M., Lesniak, G.D.G.D., Purcell, D.W.D.W., Fraser, J.A.A.,
Culham, J.C.J.C., 2016. A selective impairment of perception of sound motion direction in peripheral space: a case study. Neuropsychologia 80, 79–89. http://dx.doi.
org/10.1016/j.neuropsychologia.2015.11.008.
Tootell, R.B.H., Mendola, J.D., Hadjikhani, N.K., Ledden, P.J., Liu, A.K., Reppas, J.B.,
Dale, A.M., 1997. Functional analysis of V3A and related areas in human visual
cortex. J. Neurosci. 17 (18), 7060–7078. (Retrieved from). 〈http://www.ncbi.nlm.
nih.gov/pubmed/9278542〉.
Tootell, R.B.H., Reppas, J.B., Kwong, K.K., Malach, R., Born, R.T., Brady, T.J., Belliveau,
J.W., 1995. Functional analysis of human MT and related visual cortical areas using
magnetic resonance imaging. J. Neurosci. 15 (4), 3215–3230. (Retrieved from).
〈http://www.ncbi.nlm.nih.gov/pubmed/7722658〉.

164

Neuropsychologia 128 (2019) 150–165

M.J. Arcaro et al.

Yu, H., Chaplin, T.A., Davies, A.J., Verma, R., Rosa, M.G.P., 2012. A specialized area in
limbic cortex for fast analysis of peripheral vision. Curr. Biol. 22 (14), 1351–1357.
http://dx.doi.org/10.1016/j.cub.2012.05.029.
Zappia, R.J., Enoch, J.M., Stamper, R., Winkelman, J.Z., Gay, A.J., 1971. The Riddoch
phenomenon revealed in non-occipital lobe lesions. Br. J. Ophthalmol. 55 (6),
416–420. http://dx.doi.org/10.1136/bjo.55.6.416.
Zeki, S., Ffytche, D.H., 1998. The Riddoch syndrome: insights into the neurobiology of
conscious vision. Brain 121 (1), 25–45. http://dx.doi.org/10.1093/brain/121.1.25.
Zeki, S., Watson, J.D., Lueck, C.J., Friston, K.J., Kennard, C., Frackowiak, R.S., 1991. A
direct demonstration of functional specialization in human visual cortex. J. Neurosci.
11 (3), 641–649. (Retrieved from). 〈http://www.ncbi.nlm.nih.gov/pubmed/
2002358〉.
Zihl, J., von Cramon, D., Mai, N., 1983. Selective disturbance of movement vision after
bilateral brain damage. Brain 106 (Pt 2), 313–340. (Retrieved from). 〈http://www.
ncbi.nlm.nih.gov/pubmed/6850272〉.
Zihl, J., von Cramon, D., Mai, N., Schmid, C., 1991. Disturbance of movement vision after
bilateral posterior brain damage. Further evidence and follow up observations. Brain
114 (Pt 5), 2235–2252. (Retrieved from). 〈http://www.ncbi.nlm.nih.gov/pubmed/
1933243〉.

Wang, L., Mruczek, R.E.B., Arcaro, M.J., Kastner, S., 2015. Probabilistic maps of visual
topography in human cortex. Cereb. Cortex 25 (10), 3911–3931. http://dx.doi.org/
10.1093/cercor/bhu277.
Warner, C.E., Kwan, W.C., Wright, D., Johnston, L.A., Egan, G.F., Bourne, J.A., 2015.
Preservation of vision by the pulvinar following early-life primary visual cortex lesions. Curr. Biol. 25 (4), 424–434. http://dx.doi.org/10.1016/j.cub.2014.12.028.
Watson, A.B., 2000. Visual detection of spatial contrast patterns: evaluation of five simple
models. Opt. Express 6 (1), 12–33. (Retrieved from). 〈http://www.ncbi.nlm.nih.
gov/pubmed/12238521〉.
Watson, J.D., Myers, R., Frackowiak, R.S., Hajnal, J.V., Woods, R.P., Mazziotta, J.C., Zeki,
S., 1993. Area V5 of the human brain: evidence from a combined study using positron
emission tomography and magnetic resonance imaging. Cereb. Cortex 3 (2), 79–94.
(Retrieved from). 〈http://www.ncbi.nlm.nih.gov/pubmed/8490322〉.
Weiskrantz, L., Warrington, E.K., Sanders, M.D., Marshall, J., 1974. Visual capacity in the
hemianopic field following a restricted occipital ablation. Brain 97 (4), 709–728.
(Retrieved from). 〈http://www.ncbi.nlm.nih.gov/pubmed/4434190〉.
Yarkoni, T., Poldrack, R.A., Nichols, T.E., Van Essen, D.C., Wager, T.D., 2011. Large-scale
automated synthesis of human functional neuroimaging data. Nat. Methods 8 (8),
665–670. http://dx.doi.org/10.1038/nmeth.1635.

165