Motivation, Emotion, Feeding, Drinking, Sexual Behaviour 1111 2 3 4 5 6 7 8 9 10111 1 2 3 4 5 6 7 8 9 20111 1 2 3 4 5 6 7 8 9 30111 1 2 3 4 5 6 7 8 9 40111 1 2 3 4 5 6 7 8 9 50111 1 2 3 4 5 6111p Website publication 22 September 1998 NeuroReport 9, 2919–2925 (1998) PATIENTS with striate cortical damage causing a hemianopic field defect can nevertheless demonstrate residual visual capacities in their blind field. Previous research investigating blindsight required patients to respond explicitly to stimuli appearing in the blind field by making forced choice judgements. We present data from a patient with a left occipital lesion resulting in a homonymous hemianopia, using the flanker task. This patient displayed a significant flanker congruency effect (FCE) for colour and letter stimuli even when they appeared in the blind field. A control patient with a lesion of the right thalamus showed no FCE in the blind field. This suggests that thalamo-extrastriate neural pathways are necessary for residual functioning in blindsight. NeuroReport 9: 2919–2925 © 1998 Lippincott Williams & Wilkins. Investigating form and colour perception in blindsight using an interference task Key words: Blindsight; Extrastriate cortex; Flanker task; Thalamus Introduction Lesions of the striate visual cortex lead to visual field defects in the contralateral hemifield corresponding topographically to the damaged region of cortex.1 Despite their visual field defects, patients with lesions of striate cortex may retain some residual visual capacities in their blind field.2 This ‘blindsight’ has been demonstrated on tasks which require the localization of stimuli in the blind field by saccades or finger pointing, and the discrimination of motion, wavelengths and simple forms.1,3–11 These tasks typically require patients to make forced choice guesses regarding stimuli presented in the blind field.2,4 That is, patients are asked to respond to stimuli they confidently assert they cannot see! However, guessing paradigms have been criticized, as factors such as changes in decision criteria and uncontrolled eye movements that bring stimuli into the sighted field may produce a pattern of results suggestive of blindsight when, in reality, blindsight is not occurring.12,13 0959-4965 © 1998 Lippincott Williams & Wilkins James Danckert,1,2,CA Paul Maruff,2,3 Glynda Kinsella,1,4 Steven de Graaff4 and Jon Currie2,5 1 School of Psychological Science, Faculty of Science and Technology, La Trobe University, Bundoora, Victoria, Australia 3083; 2 Neurophysiology and Neurovisual Research Unit, Mental Health Research Institute of Victoria, Locked Bag 11, Parkville, Victoria, Australia 3052; 3School of Biophysics and Electrical Engineering, Swinburne University of Technology, Hawthorn, Victoria, Australia 3122; 4 Caulfield General Medical Centre, Caulfield, Victoria, Australia 3162; 5Brain Research Unit, Drug and Alcohol Services, Westmead Hospital, Sydney, New South Wales, Australia 2145 CA,2 Corresponding Author and Address Several recent papers have addressed these criticisms in well controlled experimental conditions with findings generally suggesting that near threshold vision, changes in decision criteria and light scatter are unlikely to be responsible for the performances of patients with blindsight.14 A more elegant method for assessing the processing of information in the blind field, has been to measure the interference caused by stimuli presented in the blind field on responses to targets presented in the sighted field.5,15–17 For example, both saccades and attentional shifts towards targets in the sighted field are slowed by prior presentation of stimuli to the blind field.5,15 In addition, normal spatial summation effects are observed when targets are presented simultaneously in the sighted and blind visual fields.16,17 The advantage of these paradigms is that patients are never asked to respond explicitly to stimuli appearing in their blind field, avoiding some of the problems of the forced choice guessing paradigms mentioned above.12,17 Vol 9 No 13 14 September 1998 2919 J. Danckert et al. 1111 2 3 4 5 6 7 8 9 10111 1 2 3 4 5 6 7 8 9 20111 1 2 3 4 5 6 7 8 9 30111 1 2 3 4 5 6 7 8 9 40111 1 2 3 4 5 6 7 8 9 50111 1 2 3 4 5 6111p The flanker task is an interference paradigm that may be useful for assessing blindsight. The task requires participants to respond to central targets while ignoring flanking stimuli that can be either congruent or incongruent with the target.18 Reaction times (RT) to identify targets are faster when flankers and targets are congruent (e.g. both red) than when targets and flankers are incongruent (e.g. red target/green flanker). This RT difference has been termed the flanker congruency effect (FCE) and has been demonstrated for a wide range of stimuli, including letters, colours and line orientation.19,20 With targets presented in the sighted field and flankers presented in the blind field, the FCE may provide a reliable index of processing in the blind field. We used two flanker tasks, one with colour stimuli and the other with letter stimuli, to investigate the residual visual capacities of a patient with a left occipital lobe infarct (patient AG) and a patient with a lesion of the right thalamus (patient CP). CP’s lesion gave rise to a visual field defect that was qualitatively similar to that of AG’s, however the site of the lesion was such that visual processing in both the thalamus and thalamo-extrastriate neural pathways were disrupted. It was hypothesized that AG would show a significant FCE when flankers appeared in the blind field, whereas CP would not show any FCE when flankers appeared in the blind field. Materials and Methods Patient AG is a 66-year-old male, admitted to hospital for abdominal surgery. After surgery he experienced hypertensive episodes and an acute confusional state. Upon recovery from these episodes he exhibited mild aphasia, cerebellar ataxia and a mild left hemiplegia, which has since resolved. CT scans indicated an area of hypodensity with a well defined border in the left occipital lobe involving both grey and white matter, suggestive of recent infarction. CT showed no evidence of any intracerebral haemorrhages and sulcal and ventricular sizes were within normal limits (Fig. 1A). Goldman Perimetry testing of AG’s visual fields indicated a dense, macula splitting right visual field (RVF) homonymous hemianopia. Experimental testing with patient AG was conducted approximately 6 weeks after the onset of his stroke. CP is an 80-year-old male who suffered a right hemisphere stroke affecting deep grey matter structures in 1995. An MRI scan indicated substantial FIG. 1. Outline of area of infarction as traced from CT scan results for patient AG (A) and patient CP (B). Lesion areas are depicted in cross-hatched regions and ventricles are depicted in black. 2920 Vol 9 No 13 14 September 1998 Form and colour perception in blindsight 1111 2 3 4 5 6 7 8 9 10111 1 2 3 4 5 6 7 8 9 20111 1 2 3 4 5 6 7 8 9 30111 1 2 3 4 5 6 7 8 9 40111 1 2 3 4 5 6 7 8 9 50111 1 2 3 4 5 6111p damage to the right thalamic nuclei with destruction of the lateral geniculate nucleus and surrounding white matter (Fig. 1B). No other mass affects were observed and ventricular and sulcal dimensions were within normal limits. Goldman Perimetry testing indicated a dense, macular splitting left visual field (LVF) homonymous hemianopia. Ten healthy, older controls completed each experiment (eight female, two male; mean (± s.d.) age 65.9 ± 5.1 for the colour flanker, and six female, four male; age 69.4 ± 7.1 for the letter flanker). Controls were recruited from the community and exclusion criteria included a past history of neurological or psychiatric disorders, drug abuse, vascular pathology or traumatic brain injury. The protocol was approved by the institutional ethics committee and informed consent was obtained prior to commencement. All tasks were created using Micro-Electronic Laboratory software (MEL-2)21 and were presented on a standard PC. Participants were seated 50 cm from the screen in a dimly lit, sound attenuated room. Background luminance of all displays was 1 cd/m2, and all stimuli were presented at 1.2 log units above background luminance. Prior to completing the flanker tasks, each patient performed simple detection tasks using both letter and colour stimuli to ensure they were unaware of flanker task stimuli when it appeared in their blind field. Targets in these tasks appeared 6.5° and 13° to the left and right of a central fixation cross. Stimuli remained present for between 3000 and 7000 ms or until a response was made. Each task consisted of 50 trials and lasted ~5 min. Neither patient was able to detect any targets appearing in their blind field at either eccentricity. Two versions of the flanker task were used, one using colour targets and a second using letter targets. Patients had to verbally identify targets in each task. Colour targets consisted of a red or green colour patch subtending 1.7° of visual angle. Flankers were also either red or green in colour as previous research has shown that patients with blindsight can make wavelength discriminations corresponding to these colours in the blind field.1,3 Colour flanker stimuli subtended 4.6° of visual angle. Targets for the letter flanker task consisted of the upper case letters E and O subtending 1.4° of visual angle. Flankers were also upper case E and O subtending 2° of visual angle. Flankers and targets were monochromatic. All other aspects of the flanker tasks were identical. Flankers could appear to the left or right of the target with equal probability. Targets also appeared without flankers (no-flanker condition) and equivalent numbers of trials with and without flankers were included in each task. The latency of verbal responses was recorded using a microphone and vocal reaction times (VRT) were defined as the time between stimulus onset and voice onset as detected by the microphone. Following each trial the experimenter entered the participant’s response via a button box to measure accuracy. The factors of visual field (i.e. LVF vs RVF) and congruency of flankers (ie. congruent, incongruent or no flanker) were randomized within tasks. Each participant completed 20 practice trials for calibration of the microphone and to allow participants to become familiar with the task. On the basis of the results from the simple detection tasks, flankers appeared 6.5° to the left or right of the target. For both tasks, a single trial consisted of the appearance of a central fixation stimulus which signalled the beginning of the trial and informed the participant to fix their eyes on the centre of the screen where targets appeared. After a variable period of time the target and flanker appeared simultaneously and remained present until the participant responded. The next trial began after the experimenter had entered the participant’s response. Participants completed three blocks of 60 trials with rest periods in between. At the end of each block both patients were asked if they had seen any stimuli appearing in their blind field to obtain a subjective verbal report concerning conscious perception of stimuli in the blind field. Neither patient reported seeing any stimuli in their blind field. Eye movements were monitored by the experimenter and trials in which eye movements occurred were abandoned and rescheduled to the end of the block.15 Patient AG made eye movements away from fixation on < 3% of trials in both flanker tasks, with some indication that he was more likely to make eye movements towards flankers appearing in the sighted field. Similarly, patient CP made very few eye movements in either flanker task (< 2%) with no suggestion of any trend or pattern in the trials on which CP made eye movements. For each participant in each task, individual VRT distributions were inspected for anticipatory responses (VRT < 2nd percentile) and abnormally slow responses (VRT > 98th percentile).15 These data were excluded from further analysis. For controls, performance in each flanker task was compared by submitting mean VRT for each congruency condition (congruent, incongruent and no flanker) in each visual field (LVF, RVF) to repeated measures ANOVA. For the patients, median RT from the congruent, incongruent and no flanker conditions in both the sighted and blind fields were compared using Wilcoxin matchedpairs signed ranks test. For all participants a FCE was also calculated by subtracting VRT to the congruent condition from VRT to the incongruent condition.20 The magnitude of this effect was compared between visual fields using paired samples t-tests. Vol 9 No 13 14 September 1998 2921 J. Danckert et al. 1111 2 3 4 5 6 7 8 9 10111 1 2 3 4 5 6 7 8 9 20111 1 2 3 4 5 6 7 8 9 30111 1 2 3 4 5 6 7 8 9 40111 1 2 3 4 5 6 7 8 9 50111 1 2 3 4 5 6111p Results For controls performance on the colour flanker task, ANOVA indicated a significant main effect of congruency (F(1,9) = 16.71, p < 0.005), but no effect of visual field and no two-way interaction (Fig. 2A). Similarly, for the letter flanker task, ANOVA indicated a significant main effect of congruency (F(1,9) = 10, p < 0.05), but no effect of visual field and no two-way interaction (Fig. 2B). With data collapsed across visual fields, there was no significant difference between VRT to the congruent and no flanker conditions. In contrast, VRTs in the incongruent condition were significantly slower than those in the congruent condition for both tasks (colour flanker: t(9) = –4.09, p < 0.005; letter flanker: t(9) = –3.67, p < 0.01). This pattern of performance yielded a positive FCE in both tasks (Table 1). On the colour flanker task patient AG showed a significant difference between median VRTs in the congruent and incongruent conditions when flankers appeared in both the sighted (FCE = 118 ms; Z = –1.99, p < 0.05) and blind fields (FCE = 74; Z = –2.25, p < 0.05; Fig. 3A), which gave rise to a positive FCE in both AG’s sighted and blind visual fields (Table 1). Patient CP showed a significant difference between median VRT in the congruent and incongruent conditions when flankers appeared in the sighted field (FCE = 144 ms; Z = –3.376, p < 0.001; Fig. 3B) but not when flankers appeared in the blind field (FCE = –9 ms). Thus, CP demonstrated a positive FCE only when colour flankers appeared in his sighted visual field (Table 1). For the letter flanker task patient AG showed a significant difference between median VRT in the congruent and incongruent conditions when flankers appeared in both the sighted (FCE = 114 ms; Z = –2.2, p < 0.05) and blind fields (FCE = 53 ms; Z = –2.94, p < 0.005; Fig. 4A), which gave rise to a positive FCE in both AG’s sighted and blind visual fields (Table 1). Patient CP showed a significant difference between median VRT in the congruent and incongruent conditions when flankers appeared in his sighted field (FCE = 64 ms; Z = –1.66, p < 0.05; Fig. 4B) but not when flankers appeared in the blind field (FCE = 2 ms). Therefore, CP only demonstrated a positive FCE when flankers appeared in his sighted visual field (Table 1). Discussion These experiments show that AG could process colour and form information in his blind field. This blindsight was inferred from the pattern of interference from flankers presented in the blind field on VRT to targets presented in the sighted field. Thus, AG exhibited a normal FCE when flankers appeared in his blind field even though he was unaware of their presence (Table 1; Figs 3A,4A). In contrast, CP showed no FCE when flankers appeared in his blind field (Table 1; Figs 3B,4B). These results suggest that residual visual processing in the blind field may depend upon the integrity of thalamo-extrastriate pathways in the damaged hemisphere.1,4,5 AG’s performances in these tasks are unlikely to be due to eye movements for three reasons. First, in the detection tasks, AG failed to detect any stimuli appearing in his blind field for periods of ⭓ 3 s, which would have allowed many eye movements to be made. This suggests that AG had no difficulty maintaining central fixation. Second, in the flanker tasks, the goal was to identify a central target, making it FIG. 2. Performance of healthy older control participants in both the colour (A) and letter (B) flanker tasks. c, congruent condition; n, no flanker condition; i, incongruent condition. All measurements are in ms and figures represented are means ± s.e. 2922 Vol 9 No 13 14 September 1998 Form and colour perception in blindsight 1111 2 3 4 5 6 7 8 9 10111 1 2 3 4 5 6 7 8 9 20111 1 2 3 4 5 6 7 8 9 30111 1 2 3 4 5 6 7 8 9 40111 1 2 3 4 5 6 7 8 9 50111 1 2 3 4 5 6111p Table 1. FCE for both controls and patients on the colour and letter flanker tasks. All figures are in milliseconds. For the controls figures represent means (±s.e.) while for the patients median figures are given. colour flanker task letter flanker task Controls AG sighted AG blind CP sighted CP blind 38.4 ± 35.2* 39.2 ± 32.5* 118* 114* 74* 53* 144* 64* –9 2 * indicates a significant FCE unnecessary for AG to make eye movements in order to prepare a response. Third, the minimal number of trials in which AG made eye movements occurred mainly on trials in which flankers appeared in his sighted field, suggesting he was distracted by flankers he had conscious awareness of. To date there have been three major criticisms of theories of blindsight that invoke a second visual pathway to explain the residual visual functions of patients with striate lesions.12,13 First, it has been suggested that patients asked to make guesses regarding stimuli in their blind field may adopt lax decision criteria.12 However, AG was not required to make decisions about stimuli appearing in his blind field. Instead, he had to identify central targets. Therefore, the differential effects of flankers presented to the blind field could not be due to changes in decision criteria.14,16,17 A second criticism is that light from stimuli in the blind field may scatter to regions of the retina projecting to intact regions of striate cortex.12 While we cannot conclusively eliminate this explanation in the current set of experiments, it would seem unlikely to completely account for AG’s blindsight. If the light from flankers presented in the blind field had scattered into the sighted field, then the same interference effects from flankers should have been observed in both patients. This was not the case. In addition, flankers were presented 6.5° away from central fixation making it unlikely that light scattered into the intact visual field. A final criticism is that the residual capacities in patients with blindsight may arise as a result of processing in spared ‘islands’ of striate cortex.13 Even though the results of AG’s CT scans (Fig. 1A) suggest that the possibility of spared islands of striate cortex is remote, this is by no means conclusive. However, the results of this previous research implying that spared islands of cortex mediate blindsight, have proven difficult to replicate.22 Furthermore, AG was never aware of stimuli presented in his blind field. Therefore, while further research placing flankers in different positions within the blind field would be necessary to comprehensively address this issue, it would seem unlikely that spared islands of cortex could account for AG’s blindsight.13,22 Although it is not possible from the present data to determine precisely the neural pathways responsible for AG’s residual visual capacities, it is possible that processing in geniculo-extrastriate neural pathways was involved. Patient CP did not show any effects of flanking stimuli appearing in his blind field. CP’s thalamic lesion suggests that the integrity of visual pathways involving the thalamus are necessary for effective processing of visual information to FIG. 3. Median VRT for AG (A) and CP (B) on the colour flanker task. All measurements are in ms. c, congruent condition; n, no flanker condition; i, incongruent condition. Vol 9 No 13 14 September 1998 2923 J. Danckert et al. 1111 2 3 4 5 6 7 8 9 10111 1 2 3 4 5 6 7 8 9 20111 1 2 3 4 5 6 7 8 9 30111 1 2 3 4 5 6 7 8 9 40111 1 2 3 4 5 6 7 8 9 50111 1 2 3 4 5 6111p FIG. 4. Median VRT for AG (A) and CP (B) on the letter flanker task. All measurements are in ms. c, congruent condition; n, no flanker condition; i, incongruent condition. occur. In contrast, striate visual cortex does not appear to be essential for visual processing to occur, although it may be necessary for visual stimuli to reach conscious awareness.3,4,23 As previous neurophysiological research suggests that the superior colliculus does not contain colour opponent cells3 it is unlikely that AG’s residual visual processing was mediated by retino-tectal pathways.5 Therefore, the implicit processing of colour and form stimuli exhibited by AG in his blind field suggests that this residual function is mediated by thalamic and extrastriate neural pathways.24,25 Neurophysiological research in monkeys has shown that the thalamus has rich connections with extrastriate regions such as V3 and V4, that have been shown to be necessary for processing of colour and form.6 Similarly, neuroimaging studies in humans suggest that the thalamus, and in particular the pulvinar nucleus, is important in tasks requiring attention to both colour and form.25 The results of the current experiments suggest that while striate visual cortex is not essential for normal interference effects to occur, the integrity of neural pathways between the thalamus and extrastriate cortical regions may mediate processing of visual properties such as colour and form. An interesting question arising from the processing of form in the blind field is whether or not it was the congruence of form (ie. the outline or orientation of letters) or the congruence of identity (i.e. semantic meaning) that determined the interference effects observed in the blind field. The results of this study suggest that the flanker task represents a reliable new methodology for assessing the residual visual capacities of patients with 2924 Vol 9 No 13 14 September 1998 blindsight. As with several other paradigms, the flanker task avoids the need for patients to respond explicitly to stimuli appearing in their blind field, eliminates issues of changes in decision criteria and avoids any confounding effects of eye movements that may bring stimuli in the blind field into the sighted field.5,15–17 Finally, the flanker task explicitly addresses the link between perception and response and has potential utility for presenting a wide variety of stimuli to the blind field of hemianopic patients.18,19 Conclusion The flanker task has proven to be a reliable means for assessing the residual visual capacities of patients with lesions of the striate visual cortex leading to specific visual field defects. One patient with a lesion of the left occipital lobe showed a reliable interference effect of flanking stimuli appearing in his blind field on responses made to targets appearing in his sighted field. This was true for both colour and letter stimuli. This task can now be used to investigate in greater detail the nature and extent of implicit processing of stimuli presented to the blind field of patients with lesions of striate cortex. A challenge that arises from this research is the problem of delineating the nature of the implicit processing. That is, do patients with lesions of the striate cortex simply respond to primitive aspects of stimuli appearing in their blind field (i.e. form outline, wavelength, orientation) or does the information presented in the blind visual field receive more detailed analysis (i.e. identification of semantic or categorical meaning)? Form and colour perception in blindsight 1111 2 3 4 5 6 7 8 9 10111 1 2 3 4 5 6 7 8 9 20111 1 2 3 4 5 6 7 8 9 30111 1 2 3 4 5 6 7 8 9 40111 1 2 3 4 5 6 7 8 9 50111 1 2 3 4 5 6111p References 1. Stoerig P. Trends Neurosci 19, 401–406 (1996). 2. Weiskrantz L, Warrington EK, Sanders MD et al. Brain 97, 709–728 (1974). 3. Cowey A and Stoerig P. 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