Cognitive Neuroscience and Neuropsychology

neurof@eport

ALTHOUGH patients with blindsight are usually unable to
discriminate forms, recent neuropsychological data have
suggested that they could still use some form attributes
in object-oriented actions. One patient with a complete
right hemianopia due to a medial occipital lesion has been
tested for his capacities to process orientation and size of
visual objects. He was presented with either a slot of
variable orientation or with rectangular objects of the
same surface but variable length. His performance was
studied in three types of tasks: motor, in which he had to
insert a card in the slot or to grasp the rectangle between
thumb and indexfinger; verbal, in which forced-choice
verbal guesses were required; and matching, which
required matching orientation or size with wrist or
fingers. Although responses were at chance level in the
two latter conditions, motor responses were system-
atically influenced by both orientation and size of the
stimulus. These data provide further evidence for two
dissociable modes of visual information processing deal-
ing respectively with ‘what"’ the object is vs ‘how’ to
grasp it. They also indicate that the neural pathway
controlling visuomotor transformation in humans is
much less dependent on V1 input than the pathway
involved in visual discrimination and identification.

Key Words: Blindsight; Striate cortex lesions; Object-
oriented actions; Form discrimination; Implicit processing;
Neuropsychology

NeuroReport 7, 793-797 (1996)

Grasping without form
discrimination in a
hemianopic field

M. T. Perenin™ and Y. Rossetti

Vision et Motricité, INSERM Unité 94,
69500 Bron, France

©ACorresponding Author

Introduction

Blindsight - the unconscious residual vision present
in patients with visual field defects of occipital
origin—has raised important questions concerning
the neural basis of consciousness as well as the role of
extrageniculostriate vision in man. Although various
residual functions have been demonstrated in corti-
cally blind fields, the majority of them appears related
to extrinsic properties of the object (e.g. location,
motion). Patients with extensive damage to the
primary visual cortex typically show remarkable
capacities to orient their gaze or to point at targets
presented in their ‘blind’ field, while being virtually
unable to discriminate simple forms when forced to
guess.'* This apparent dissociation between spatial
and object vision may explain why little attention has
been paid so far to the distal, grasping component of
prehension.

In recent years, neuropsychological studies have
suggested that two separate visual systems are
involved in perception and action. More specifically,
a double dissociation has been found between
perceiving objects and grasping them. Patients with
optic ataxia are unable to reach and grasp accurately
objects that they can see and describe normally.*

© Rapid Science Publishers

Conversely, accurate prehension of objects that are
neither recognized nor described has been observed in
visual agnosia.” This finding has created interest in
the study of the grasping component of object
prehension in blindsight patients, in search of a
similar dissociation.

In the present paper we report for the first time
positive evidence for such a dissociation in a patient
with a restricted left medial occipital lesion. This
patient retained a capacity to process orientation and
size of objects inside his hemianopic field, when asked
to perform visually guided movements, but could not
discriminate these same attributes using verbal or
motor matching responses.

Materials and Methods

Case report: PJG was a 32-year-old man who had
sustained a vascular infarction in the territory of the
posterior cerebral artery following a migraine attack.
MRI showed that the lesion was lying on the medial
side of the left occipital lobe, mostly invading the
primary visual cortex and optic radiations; it partially
spared the occipital pole and did not extend dorsally
beyond the paricto-occipital sulcus (Fig. 1). The only

Vol 7 No 3 29 February 1996 793
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FIG. 1. Magnetic resonance images of PJG’s brain (T1-weighted
images) showing a hypodense lesion (dark zone) on the internal side
of the left occipital lobe. Horizontal sections respectively at the level of
the bicommissural plane (a) and 1¢m above (b), and left parasigittal
section (¢).

clinical deficit was a nearly complete hemianopia, as
assessed by Tiibinger perimetry (Fig. 2). PJG did not
complain much about his visual deficit; he did not
stop driving following his vascular accident as he was
aware of movement of the vehicles on his right
(although without a genuine visual experience). He
has been tested in several blindsight paradigms before
the present study and usually showed good perfor-
mance in pointing, discrimination of motion direc-
tion® and completion of figures across the vertical
meridian. However, he performed at chance level in
discriminating simple geometrical forms (e.g. triangles
vs circles) or lines of different orientations (c.g.
horizontal from vertical) in his hemianopic field.

Procedure: In the present study, performed 7 years
after the stroke, the capacity of PJG to process
orientation and size of target objects was tested in
different experimental conditions. At each trial white
stimuli fixed on a black vertical panel were brightly
illuminated (contrast 95%) for 2s. The patient was
seated 57cm from the panel, the head restrained with
a forehead and chin rest, the left eye patched. He was
required to fixate a central diode during each
stimulation; this was controlled through a peephole
with a precision of greater than 2°. Very few trials
involving eye movements had to be discarded. Each

794 Vol7 No 3 29 February 1996

M. T. Perenin and Y. Rossetti

90

180

270

FIG. 2. Visual field of the patient's right eye using dynamic perimetry.
A bright and large target (320cd m, 116’) is moved on a mesopic
background (3.2cd m “).

task was first carried out in the normal field (in order
to ensure a better understanding of the task) and then
in the hemianopic field.

Orientation processing was assessed using a white
slot (18cm long, 3 cm wide) which could be rotated in
45° steps inside the dark panel, either in the left or
right visual field, on symmetrical locations, at more
than 10° of eccentricity (x,y coordinates of the slot
center: 20° from the vertical meridian, 10° below the
horizontal meridian). The patient’s performance was
explored with three different tasks, in blocks of 40
trials each. In the first task, he was asked to make a
quick reaching movement in order to insert a hand-
held card into the slot (to ‘post’ the card). Corrections
following contact with the panel were not allowed. In
the second task, PJG had to provide a forced-choice
verbal response, by reading the letter corresponding
to one of the four orientations drawn ona card. In the
third task, he had to match manually the orientation
of the slot by turning the card with the hand without
reaching to the stimulus.

Size processing was studied using white plaques of
equal area but varying in dimensions by 1.5cm
horizontal steps; they ranged from a square to an
elongated rectangle (5 and 9.5cm respectively). They
were fixed one by one on the black panel. PJG was
first required to reach out and grasp the plaques
between finger and thumb, with the fingers
horizontally oriented. He was not allowed to
perform any correction following contact with the
panel. In the second task, he had to make a verbal
guess, also using a multiple-choice card. Finally, he
had to match the length of the plaque with the
thumb and forefinger, without moving the arm. In
Residual grasping in blindsight

neurofpeport

each motor task, the hand ipsilateral to the
stimulated visual field was used.

Performance analysis: Responses were video-taped
and then scored through frame-by-frame analysis. For
the orientation experiment, card orientation was
measured on frontal, posterior views, in the 0-180°
range, with an accuracy of 2°. In the ‘posting’ task
angular values were recorded at the time the card
made contact with the stimulus. For the size
experiment, the aperture between index finger and
thumb was measured on top views, with a precision of
0.5 cm. In the grasping task, both final aperture (hand
in contact with the panel) and maximal aperture
during the reach (known to be closely related to
object size in normal subjects”) were considered.

In order to determine whether PJG’s performance
was systematically influenced by stimulus orientation
and/or size, linear regressions were computed in each
condition. An additional analysis was applied to
verbal responses: as they could be classified as
correct vs incorrect, their departure from chance
was also tested by comparing their dichotomous
distribution with the law of Laplace-Gauss_,.

Results

Orientation: In his left normal visual field, PJG
performed normally in the different tasks. In
particular, his verbal responses were always correct
and he succeeded in ‘posting’ the card into the slot at
each trial; motor matching was also very accurate
(r=0.70, p<0.0005). Obviously he could not reach
the same level of accuracy in his right, hemianopic
field. Nevertheless, video analysis of the posting task
showed that the final orientation of the card was
significantly related to the slot orientation (r=0.314,
p<0.05, r=0.463, p<0.005, respectively, in two
different sessions, several months apart). Correct
orientation was often achieved at an early stage
during the movement. In contrast with his good
performance in this task, PJG’s performance in the
other two forced-choice discrimination tasks was very
poor, whether he had to provide a verbal response
(r=0.066, p >0.6) or to match the orientation of the
slot by turning the card with the hand (r=0.078,
p>0.6; Fig. 3). Verbal responses were also at chance
level when classified in two categories: they were
correct in only 12 out of 40 trials (p > 0.40). Strikingly,
PJG took more time to respond (responses often
occurred near the end of the illumination period) in
the two latter tasks (despite encouragements to
perform faster) than in the aiming task. Reaction
times ranged between 450 and 600 ms in the ‘posting’
task but were often close to 2s in the two
discrimination tasks.

120
ORIENTATION

Reach 2

1007]

oe
Sc

D
3

Response (deg)

40

Verbal~o

2014 . .
0 45 90 135
Target orientation (deg)

FIG. 3. Task-dependent responses of PJG to target orientation inside
his hemianopic field. While verbal (circles) and manual matching
(triangles) responses are at chance level, reaching responses
{orientation of a hand-held card when ‘posting’ it in a slot) (squares
and rectangles, 2 different sessions) are significantly related to target
orientation.

Response (cm)

Verbal ©
7

5 65 8 9.5

Object size (cm)

FIG. 4. Task-dependent responses of PJG to object size inside his
hemianopic field. While verbal (circles) and manual matching {open
triangles) responses are at chance level, grasping responses at time of
maximal (filled triangles} and final (squares) grip aperture are
systematically influenced by object size.

Size: As in the previous experiment, PJG had no
difficulty carrying out the different tasks in his left
normal field. He succeeded picking up the plaques
between forefinger and thumb at all trials and always

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M. T. Perenin and Y. Rossetti

gave correct responses in the verbal task. Of course,
he could not reach the same level of accuracy in his
right, hemianopic field. However, his performance in
the grasping task was well above chance. His finger
grip aperture correlated remarkably well with the size
of the object: this was true for both final grip aperture
(in contact with the panel; r= 0.494, p< 0.001) and for
the maximal grip aperture (during the arm transporta-
tion phase; r=0.414, p<0.01). By contrast, PJG
performed poorly in the other two tasks. He did
not score better than chance, whether he had to give
verbal responses (r=0.20, p >0.20) or to match with
the index finger and thumb the length of the plaques
flashed on the panel (r = 0.068, p > 0.60; Fig. 4). Verbal
responses were also at chance level when classified
into two categories: they were correct in only eight of
40 trials (p>0.40). Again responses in these two
discrimination tasks were delayed with respect to the
grasping task.

Discussion

Our findings show that a patient with a striate
cortex lesion may retain a capacity to adjust
prehension movements with respect to orientation
and size of objects in his hemianopic field (see Ref. 10
for a brief qualitative mention of a similar observa-
tion), despite a total inability to discriminate these
same visual attributes by means of verbal or manual
matching responses. PJG’s difficulty in the latter task
was not one of understanding: he performed fairly
well in his normal field with the same task. Moreover,
when required to imagine a slot at different orienta-
tions with his eyes closed, he could turn the card to
the imagined orientation with a very good precision
using his right hand (r=0.99, p < 0.0001).

At first glance, the relative sparing of grasping in
PJG could be explained by the fact that object-
oriented actions requires less information than form
discrimination. However this cannot apply to our
experimental conditions, as the same amount of
information was available in the corresponding two
kinds of tasks, with the same single object feature used
as a variable. In fact the behaviour of our patient was
very reminiscent of that observed in a patient with
visual agnosia,°” who could not use visual informa-
tion for perceptual purposes, even though this
information was accurately used in visuomotor
action. The best account for this dissociation is that
separate visual processes underly visually directed
actions such as the automatic movements of prehen-
sion and more demanding and usually conscious act
of identification and categorization of objects (see
Refs 11 and 12 for different formulations of this
dichotomy). In our patient, this is further illustrated
by the different reaction times observed in the two
types of tasks; they were more than twice as fast in the

796 Vol 7 No 3 29 February 1996

goal-directed hand movements than in the two
discrimination tasks. This difference recalls the
temporal dissociation shown in normal subjects
required to grasp an object which is briskly displaced
at movement onset; they are much faster at correcting
their movement than at signalling the time at which
they become aware of the object displacement by a
vocal response.'? It also fits with the view that
visuomotor processes taking place in the dorsal
visual stream would be concerned with the instanta-
neous characteristics of objects, while identification
processes in the ventral stream would require more
enduring characteristics.'*

The idea of two distinct visual pathways each
dealing with a specific utilization of visual parameters
is strongly supported by neurophysiological findings
in the monkey. In particular, it has been shown
recently that the dorsal occipito-parietal system is not
only involved in the spatial location and reaching of
objects, but also in object shape perception and
manipulation.'>-!” Interestingly, the neural activity
of the main input areas (MT and V3A) of the dorsal
pathway is only partially affected by inactivation or
removal of area V1 in the monkey:'*”° in particular, a
high percentage (60-80%) of MT neurones retain
their direction selectivity while about one-third
remain orientation specific in V3A. By contrast,
neurones of areas TE, TEO and V4 of the ventral
stream are silent in the absence of V1 input??? Our
results support the view that the dorsal pathway can
process intrinsic properties of objects during action
and that it remains active following striate cortex
lesion in man.

Conclusions

Residual visual functions in cortically blind fields
are not only related to ‘where’ objects are but also
relate to ‘how’ to act on these objects. Orientation and
size attributes may still be used in object-oriented
actions, although these same attributes cannot access
more elaborated representations underlying verbal
and matching tasks.

Received 22 November 1995;
accepted 3 January 1996
Residual grasping in blindsight

neurofpeport

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General Summary

Blindsight patients typically show good abilities to orient their gaze or to point at targets in their ‘blind’ field, while being unable to
discriminate simple forms when forced to guess. The present study aimed to determine whether some form attributes could nevertheless
be used in object-oriented actions. One patient with a complete hemianopia of occipital origin has been tested for his capacities to process
orientation and size of visual objects in different conditions. Although responses were at chance level when he was required to provide

forced-choice verbal guesses or matching responses, motor responses were systematically influenced by both orientation and size of the
stimulus. These data provide further evidence for two dissociable modes of visual information processing dealing respectively with ‘what’
the object is vs ‘how’ to grasp it. They also suggest that V1 lesions in humans have different functional consequences on the two cortical
visual pathways.

Vol 7 No 3 29 February 1996 797