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Effects of Unseen Stimuli on Reaction Times to Seen Stimuli in Monkeys with Blindsight
CONSCIOUSNESS AND COGNITION ARTICLE NO.
7, 312–323 (1998)
CC980359
Effects of Unseen Stimuli on Reaction Times to Seen Stimuli in Monkeys with Blindsight 1 Alan Cowey,* Petra Stoerig,† and Carolyne Le Mare* *University of Oxford, Department of Experimental Psychology, South Parks Road, Oxford OX1 3UD UK; †Heinrich-Heine-Universita¨t, Inst. Physiol. Psychology, Universita¨tsstr 1, Bldg 23.03, 40225 Du¨sseldorf, Germany In three macaque monkeys with unilateral removal of primary visual cortex and in one unoperated monkey, we measured reaction times to a visual target that was presented at a lateral eccentricity of 20° in the normal, left, visual hemifield. When an additional stimulus was presented at the corresponding position in the right hemifield (hemianopic in three of the monkeys), it significantly slowed the reaction time to the left target if it preceded it by delays from 100–500 msec. The most effective delay depended on the particular experimental paradigm and perhaps on the experience of the monkey with the task. The results show that reaction times to seen targets in the normal hemifield of monkeys are influenced by the presentation of ‘‘unseen’’ targets in the anopic hemifield, as in some patients with cortically blind visual field defects. 1998 Academic Press
INTRODUCTION
When the primary visual cortex (area V1) is destroyed or severed from its thalamocortical input, a human patient is cortically blind in the resulting field defect. Visual stimuli are no longer consciously seen, with the possible exception in a minority of patients that rapidly moving stimuli of high luminance contrast are sometimes perceived (Riddoch, 1917), for example, as faint moving shadows (Barbur, Watson, Frackowiak, & Zeki, 1993). Despite their lack of conscious vision, some patients show excellent detection, localization, and discrimination of visual targets when required to guess about the nature of targets presented within the blind region (see Stoerig & Cowey, 1997, for review). This paradoxical ability is termed ‘‘blindsight’’ (see Weiskrantz, 1986, for an historical review). Residual visual processing can also be uncovered by studying the effects (if any) of unseen stimuli on the overt response to consciously perceived targets in the normal part of the visual field. There are several examples of such implicit processing, e.g., the alteration in the perceptual judgment of shape when parts of the shape are genuinely absent, or are present but in the blind region (Torjussen, 1976; for review, see Walker & Mattingley, 1997). Here, we are concerned with the effects of a target confined to the blind field on reaction times to a seen stimulus in the sighted field, first demonstrated by Marzi, Tassinari, Aglioti, and Lutzemberger (1986) and since confirmed in human subjects in several ways (Corbetta, Marzi, Tassinari & Aglioti, 1990; Rafal, Smith, Krantz, Cohen, & Brennan, 1990). Implicit processing indirectly revealed in this way has Address correspondence and reprint requests to Professor Alan Cowey, University of Oxford, Department of Experimental Psychology, South Parks Road, Oxford OX1 3UD, UK. E-mail: [email protected]. 312 1053-8100/98 $25.00
Copyright 1998 by Academic Press All rights of reproduction in any form reserved.
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the advantage of not requiring the subject to guess or to make any subjective judgment about confidence levels or visual awareness. Whether cortically blind monkeys show such implicit processing of visual targets is not known, although their ability to detect and localize visual targets has been repeatedly demonstrated (Cowey, 1967; Cowey & Stoerig, 1997; Klu¨ver, 1949; Pasik & Pasik, 1971; Pasik & Pasik, 1982). We therefore studied four monkeys in a reaction time task, in which the animal itself initiated presentation of a target in its normal left hemifield and had to touch it promptly. On half of the trials, at random, a second light appeared at the same time or earlier in the opposite hemifield, which was blind in three of the animals. However, all three possessed blindsight in their hemianopic field (Cowey & Stoerig, 1995, 1997). The results reveal implicit processing in that the unseen target slowed the response to the seen target when it preceded it by several hundred msec. EXPERIMENTAL METHODS
Subjects We studied four macaque monkeys. One of them was normal (Rosie). In the other three, the striate cortex of the left hemisphere had been removed 10 years before the present investigations and when the monkeys were already adult. Details of the surgery, neurohistology on the excised occipital lobes, and magnetic resonance anatomical images of two of the operated monkeys have been published elsewhere (Cowey & Stoerig, 1997). Subsequent to the experiment reported here, the third operated monkey (Lennox) had to be perfused, because he was seropositive for Herpes simiae, and histological examination showed that the striate cortex of the left hemisphere had been totally excised and that the dorsal lateral geniculate nucleus was degenerated throughout its extent. Apparatus and Testing Procedure The apparatus has been described before (Cowey & Stoerig, 1997). The monkeys were trained, with food rewards, to squat in a primate chair and raise the head through a hole in an adjustable horizontal platform while plastic baffles were adjusted to prevent gross head movements. The chair was locked in position in front of a visual display unit (VDU), so that the monkey directly faced the display, with the eyes 27 cm from the center of the screen. The monkeys could reach out and touch any part of the display and also retrieve rewards from a food well beneath it. Visual stimuli were presented on a 35-cm color monitor (Microvitech 895) at the monkeys’ reaching distance. The stimuli were generated and controlled by a microcomputer. Their luminance was measured with a Minolta LS-110 digital luminance meter calibrated for human CIE photopic spectral sensitivity. Immediately in front of the VDU was an infrared touch screen that recorded, with a spatial resolution of about 0.5 cm, where the monkey touched the display. The effective response area on the screen was set to coincide with the area of the 4° start light and the target on the left. At the top and each side of the VDU was a 2° infrared light source, pointing at
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the monkey’s eyes. These lights provided three specular reflections on the pupil of each eye and allowed us to watch the eyes on a remote video monitor by means of an infrared sensitive camera mounted next to the topmost light. The camera provided a clear view of the eyes and showed that, when the monkeys reached out to start a trial, they always looked at the start light. Therefore, the visual stimuli could reliably be presented at known retinal positions. When the monkey touched the start-light to initiate each trial, both the disappearance of the start light and the appearance of the target light (unless it was deliberately delayed) occurred at the beginning of the next frame of the raster display, and only then did the reaction time count begin on the computer’s clock. The start of each trial was therefore time-locked to the appearance of the target on the left. However, as the scan time of the infrared touch screen was 17 msec, the mean error in its registration of a response was 8.5 msec. Although the registered response was instantly detected by the system clock, the error in measuring latencies was ⫹/⫺ 8.5 msec. The displays are shown schematically in Fig. 1. On each trial, the start light appeared at the center of the VDU and remained there until the monkey touched it. The start light, the target simulus on the left, and the stimulus on the right (when present) all subtended 4 ⫻ 4 degrees. The stimuli to the left and right of the start light were 20° eccentric to the vertical midline. They were present for 1 s and the monkeys almost invariably responded well before the target disappeared. On trials when they did not, no reaction time was recorded. As long as the monkey touched the target stimulus on the left before it disappeared, a reward (nut or raisin) was immediately delivered to the foodwell beneath the VDU. The trial ended after each response, and after a further delay of 3 s, the next trial began with the reappearance of the start light. The reaction time for each trial was recorded and saved for subsequent analysis. Each testing session consisted of 100 trials. During the first 10 sessions the target stimulus appeared on the left on every trial when the monkey pressed the start light (Fig. 1A). No stimulus was ever presented on the right. These sessions were used to establish baseline reaction times without possible interference from a simultaneous or prior stimulus on the right. On subsequent groups of sessions, described in more detail under Results, the target stimulus appeared with a delay of 100–500 msec after the monkey started the trial, but on half of the trials, an additional light appeared on the right as soon as the trial was started (Fig. 1B). In other words the additional stimulus on the right, which lay in the hemianopic field of three of the monkeys, preceded the target stimulus by 0–500 msec. This temporal difference is referred to as the stimulus onset asynchrony (SOA), and we analyzed the data in order to measure any difference in reaction time between trials when the target light on the left appeared alone, or with, or shortly after the light on the right. This difference in speed of reaction to the left target was measured for each SOA between the right and left stimuli. In the last testing condition, the target light could appear, at random, at any one of three vertically separated positions on the left, either alone (Fig. 1C), or with the ‘‘irrelevant’’ light on the right (Fig. 1D). The testing took place in a dimly lit room where the luminance of the white walls to either side of the monkey was about 4 cd.m ⫺2. The mean luminance of the VDU
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FIG. 1. Schematic representation of the visual display and the response sequence. Each trial began with the display shown in the center, which remained until the monkey touched the start light. In the first procedure, it was followed by the display shown in A and the monkey had to touch the target at the left. In the next procedure, A or B would occur but the required response was the same. In the final procedure, touching the start light always produced, at random, a target at one of three positions on the left (all three indicated in the figure) and with various delays. On half of these trials a light was also immediately presented on the right, i.e., at the same time as the target on the left or before it. On every trial, the monkey had to respond by touching the target on the left.
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TABLE 1 Reaction Times, msec, to a Target Presented by the Monkey Itself in the Left Visual Hemifield Mean RT and SD Dracula Lennox Rosie Wrinkle
469 516 404 623
sd sd sd sd
135 113 111 114
Standard Error of mean 4.4 3.8 3.9 3.9
Note. Means are based on a total of 1000 trials for each monkey over ten consecutive testing sessions.
was 2.0 cd.m ⫺2 and the luminance of the occasional stimulus in the right hemifield was always 40 cd.m ⫺2. The luminance of the target stimulus on the left was either 40 cd.m ⫺2 or 20 cd.m ⫺2, according to testing conditions described in Results. RESULTS
Initial Training For ten consecutive sessions, providing a total of 1000 trials, the monkeys were presented only with the display shown by route A at the top of Fig. 1. After starting the trial, the target light appeared instantly on the left at a luminance of 40 cd.m ⫺2. The results are shown in Table 1. Although the four monkeys responded at different speeds, each was highly consistent, as shown by the small standard error of the mean response latency. Testing with Dual Stimuli (a) SOA ⫽ 0 msec. Immediately after this initial training each monkey was tested for 200 trials on half of which, at random, a stimulus identical to the target stimulus appeared at the same time and for the same duration in the right visual hemifield, which was anopic in three of the monkeys. The purpose was to see whether this novel and additional stimulus in the hemianopic field influenced the reaction time to the target on the left. There were no statistically significant differences ( p ⬎ .05) between the mean reaction time on trials with one or with two stimuli, even for the monkey (Rosie) with both visual hemifields intact (see Table 2). Nor were there any differences detectable to us when watching the monkeys’ eyes or hands on the video monitor, with one exception. On the first few trials, the unoperated monkey, Rosie, seemed disconcerted by the dual simultaneous presentation and visibly paused and even oriented to the right before responding as usual on the left. (b) SOA ⫽ 0, 100, 200 or 300 msec. Although an unexpected stimulus on the right had no effect on the reaction time to the expected stimulus on the left when both were presented simultaneously, there might be an effect on reaction time if the irrelevant stimulus precedes the relevant one, as in some patients when it appeared in the
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TABLE 2 Reaction Times in msec to a Target Stimulus Presented on the Left, Either Alone or at the Same Time as an Identical but Irrelevant Stimulus on the Right
Dracula Lennox Rosie Wrinkle
Reaction times to single stimuli
Reaction time to double stimuli
Mean difference (msec)
Probability
t
490 517 363 639
501 540 365 642
11 23 2 3
⬎0.05 ⬎0.05 ⬎0.05 ⬎0.05
0.58 1.24 0.19 0.22
Note. There were no statistically significant differences for any monkey between the mean reaction time to 100 single and 100 dual presentations. The highest t value of 1.24 was well below the critical value of 1.96 required for p ⫽ ⬍.05.
clinically blind field defect (Marzi et al., 1986). In the next stage of the experiment, we therefore introduced a variable delay (0, 100, 200, or 300 msec) between the disappearance of the start-light and the appearance of the target on the left, but on half the trials, the irrelevant stimulus was presented on the right and without delay, i.e., coinciding with or preceding the target. There were eight testing sessions (800 trials) and a single SOA was used in each, first in ascending order from 0–300 and then in the reverse order. The results are shown in Fig. 2. In all four monkeys, the largest difference between reaction time on single and dual stimulus trials occurred at a SOA of either 200 or 300 msec. We carried out multiple t tests for each monkey (i.e., four t tests for each) on the basis of the z-scores, in view of uncertainties about the acceptability of an analysis of variance on difference scores. As we had already determined that there was no difference in reaction time to a single target or to two stimuli when the SOA was zero, we were concerned only with the possible effect of the three SOAs from 100–300 msec. Given that that were three comparisons for each monkey but that each monkey is considered independently, we used the appropriate correction for multiple comparisons on each monkey. The results are shown by the filled circles in Fig. 2. Each difference score indicated by an asterisk is significant at p ⬍ .03, z ⫽ ⬎2.58. The prior presentation of the stimulus on the right clearly affected reaction time in all monkeys, but only at a SOA of 200 msec in Dracula and 300 msec in Wrinkle. The prior stimulus on the right slowed the response to the target on the left, even though it was presented well within the field defect of the hemianopic monkeys. Could it have been detected by any artefact in the raster display on the left side of the VDU and therefore in the intact hemifield? Such artefacts can arise at the left edge of any raster line that contains a large change in luminance or can even be reflections along the curved left edge of the VDU. To control for these possibilities we covered the position of the stimulus on the right with black tape, 5 ⫻ 5° and therefore slightly larger than the stimulus as well as standing proud of it as a result of being on the protective glass panel in front of the CRT. The light was no longer directly visible but any artefacts on the left should remain and indeed did so when we lowered the screen mean luminance effectively to zero and ourselves viewed the display from the position of the monkey. Each monkey received 800 trials (200 for each SOA) as before. The results are shown by the unfilled circles in Fig. 2. The
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FIG. 2. The difference in reaction time between the response to a target presented on the left and the response to the same target when a light was presented on the right, at the same time or up to 300 msec earlier (the SOA). Filled circles show the results when the stimulus on the right was visible. Unfilled circles show the results of covering the stimulus on the right. Error bars show the standard error of the mean. In this and the following figures, the value for each SOA indicates the difference between the mean of all the trials when the target appeared alone and all those when it was preceded by a stimulus on the right at the SOA used in that session and a similar session repeated later. An asterisk indicates that the mean difference was statistically significant at p ⫽ ⬍ .05, after appropriate correction for multiple comparisons.
light on the right now had no effect on reaction time in any monkey. Screening the stimulus on the right in this way does not control for intraocular scatter, of course, but the luminance contrast should have been below the levels detectable by intraocular scatter (Stoerig, Faubert, Ptito, Diaconu, & Ptito, 1996). Furthermore, when an almost identical stimulus was presented binocularly (in the same apparatus but for reasons unconnected with the present experiment) in the phenomenally blind right hemifield of GY, a human hemianope with blindsight, he did not report any awareness
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FIG. 3. Differences in reaction time, again using the procedure shown in Fig. 1A and B, but where additional SOAs were introduced and the luminance of the target on the left was reduced in an attempt to make the prior stimulus on the right more salient. Statistically significant lengthening of reaction time to the left target occurred in three monkeys, but not in one of the hemianopic monkeys (Dracula).
of light generated by intraocular light scatter, even though he does report such a visual percept at much higher levels of stimulus contrast, well above those used with the monkeys. (c) SOA ⫽ 0–500 msec. As the greatest difference in reaction time to single and double presentations occurred at the longer SOAs, with no evidence that a maximum difference had been reached, longer SOAs of 400 and 500 msec were tested. In addition, the luminance of the target on the left was reduced from 40 to 20 cd.m ⫺2 while keeping the luminance of the stimulus on the right at 40 cd.m ⫺2. The monkeys were tested for 1200 trials over 12 sessions. The results are given in Fig. 3, and show that the normal monkey and two of the hemianopic monkeys lengthened their reaction time to the now relatively less intense left target when it was preceded by the stimulus
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on the right. Again allowing for multiple comparisons, the increase was statistically significant ( p ⬍ .05) at every SOA from 200 to 500 msec in two of the monkeys and from 300 to 500 in Wrinkle, as well as at 100. There was no indication that the maximum effect had been reached or passed at the longer SOAs. In hemianopic monkey Dracula, the effect of SOA was substantially smaller, and was not statistically significant at any SOA. We noticed that, in all four monkeys, but especially Dracula, the increase in reaction time when a longer SOA was present was greater in the earlier than in the later testing sessions. A likely explanation is that the monkeys were learning that, as the target stimulus on the left always appeared in the same position, they could anticipate its appearance by moving the responding hand towards the appropriate position even before the target had appeared. We therefore carried out a final procedure in which the target on the left appeared, randomly, at any of three positions on the left (see Fig. 1 C, D), meaning that the monkeys could not predict its position and could therefore not effectively preprogram their response to a particular location, although they could, possibly, begin to move to the left. The position of the prior stimulus on the right was unaltered. The monkeys were again tested for 1200 trials, over 12 sessions and the results are shown in Fig. 4. Monkeys Rosie (normal) and Lennox took significantly longer to respond at SOAs of 200–500 or 200–400 msec but Wrinkle was significantly slower only at a SOA of 400 msec (all p ⬍ .05 after correction for multiple comparisons). Dracula was still unaffected by the stimulus on the right at any SOA. Interestingly, the effect of SOA lessened at the longest interval for all monkeys, and Dracula was actually faster, but nonsignifiantly so, at an SOA of 500 msec. Two other aspects of Fig. 4 are noteworthy. First, the variance is much greater than before, presumably because of the uncertainty of the position of the target on the left and the fact that three slightly different hand movements were required. An unfortunate consequence of the increased standard errors is that a given difference in reaction time is less significant. Second, the mean differences are lower, some of them conspicuously so, than in the immediately preceding test (Fig. 3) despite the uncertainty of the target position, suggesting that with repeated testing the monkeys were habituating to the light on the right, or that the increased attention to the normal left hemifield in which the target position was no longer invariable, weakened or obliterated the effect of the unseen stimulus on the right. DISCUSSION
Our results show that when a small light is presented in the blind hemifield prior to an expected identical, or similar, light in the normal hemifield, the reaction time to the latter is lengthened in a manner determined by the difference in timing (the SOA) between the two lights. The effect was also present, and was even greater, in a monkey with no visual field defect. A similar effect has been reported in some patients when the prior stimulus was presented in a clinically blind region of the visual field (Marzi et al., 1986; Rafal et al., 1990), where the prior stimulus was not consciously registered. For our own results to be relevant to the findings with patients, it is important that for the hemianopic monkeys, too, the interfering stimulus should be perceptually invisible. Here
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FIG. 4. Differences in reaction time using the displays shown in Fig. 1C and D, where the exact position of the target on the left was unpredictable. In the normal monkey (Rosie) and the hemianopic monkeys Lennox and Wrinkle, the prior presentation of a stimulus on the right lengthened the reaction time to the target on the left, but at only one SOA in Wrinkle. None of the reaction time differences was statistically significant in Dracula.
we rely on our prior extensive investigation on the same monkeys in the same apparatus, which showed that although they readily detected brief stimuli of 40 cd.m ⫺2 in the blind hemifield when presented alone, they nevertheless categorized such stimuli as blanks when they were presented in a task that required the animals to discriminate between lights and blanks (Cowey & Stoerig, 1997). We can therefore be confident that, in the present experiment, the interfering targets on the right were unseen, i.e., phenomenally invisible, as with neurological patients with blindsight (Stoerig & Cowey, 1997). Could the effects of introducing an SOA be attributed to some unspecified and unwanted feature of the presence of a real visual stimulus on the right, for example, artefacts at the left of the screen in the intact visual field? The results of presenting but covering the stimulus on the right show this possibility to be unfounded. The
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difference scores for single and double presentations were no longer significantly different (Fig. 2). A notable feature of blindsight is that it has been reported in only a minority of patients with clinically blind field defects (e.g., Stoerig, 1987). Although the explanation is still unclear, this variability probably reflects the extent of the extra-striate as well as striate cortical damage, the type of visual stimuli used, and the method used, e.g., yes/no judgments or forced-choice guessing. Here, all three hemianopic monkeys showed evidence of implicit processing of visual stimuli presented in the hemianopic region, perhaps because the direct extrastriate damage was minimized and a direct manual response was required. Nevertheless, there was variation in the results, with monkey Dracula consistently showing less evidence of implicit processing than the other two hemianopic monkeys, despite our earlier demonstration, using forcedchoice responding, that his sensitivity to light in the hemianopic field was no less impaired than that of monkey Lennox and much less impaired than that of Wrinkle (Cowey & Stoerig, 1997). Nor can the relative ineffectiveness of the light in his hemianopic field in the present experiment be attributed to impetuousness in responding on the left because his reaction times, although shorter than those of the other two hemianopic monkeys, were longer than those of the normal monkey (Table 1). Further speculation on reasons for his different behaviour would be easy but unconvincing, since we know almost nothing about his extra-striate cortical damage, his cognitive strategies, and his physiological habituation to irrelevant visual stimuli. The more important result is that he too showed implicit processing initially. What is the basis of implicit processing as revealed by the effects of unseen targets on reaction time to seen targets? If a prior unseen target triggered a saccadic eye movement in its direction, the effects that we observe in monkeys and others have observed in patients would not be surprising. We know of no measurements or observations of this possibility in human subjects. However, apart perhaps from the first occasion on which dual targets were presented to the monkeys, we saw no eye movements towards the stimulus on the right, even at SOAs of several hundred msec. Even though the stimulus on the right was present for 1s, we saw no attempts to inspect it. Further, an actual and complete movement to the right would be expected to delay the response to the left more than it did. Of course, any tendency to make a rightward eye movement might have been suppressed by the monkeys and this could have delayed the response to the left, rather like the delay shown by human subjects when they have to make a saccadic eye movement in the opposite direction to a visual stimulus (an antisaccade) rather than towards it. We have no direct evidence bearing on this possibility. That an unseen stimulus presented before a seen one has an effect on reaction time has also been demonstrated in normal human observers when the first stimulus was followed by the second at SOAs below the visual temporal resolution required for conscious perception (Taylor & McCloskey, 1990). Targets that are not phenomenally detected can thus modulate visually guided behavior not only in blindsight, but in normal nonreflexive visual processing as well. ACKNOWLEDGMENT We thank the UK Medical Research Council (Programme Grant G971/397/B) and the Deutsche Forschungsgemeinshaft for their generous support. We also gratefully acknowledge statistical advice
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from Dr. David Popplewell and a network travel grant from the Oxford McDonnell–Pew Cognitive Neuroscience Centre.
REFERENCES Barbur, J. L., Watson, J. D., Frackowiak, R. S. J., & Zeki, S. (1993). Conscious visual perception without V1. Brain, 116, 1293–1302. Corbetta, M., Marzi, C. A., Tassinari, G., & Aglioti, S. (1990). Effectiveness of different task paradigms in revealing blindsight. Brain, 113, 603–616. Cowey, A. (1967). Perimetric study of field defects in monkeys after cortical and retina ablations. Quarterly Journal of Experimental Psychology, 19, 232–245. Cowey, A. (1995). Visual perception: Blindsight in real sight. Nature, News and Views, 377, 290–291. Cowey, A., & Stoerig, P. (1995). Blindsight in monkeys. Nature, 373, 247–249. Cowey, A., & Stoerig, P. (1997). Visual detection in monkeys with blindsight. Neuropsychologia, 35, 929–939. Klu¨ver, H. (1949). Visual functions after removal of the occipital lobes. Journal of Psychology, 11, 23– 45. Marzi, C. A., Tassinari, G., Aglioti, S., & Lutzemberger, L. (1986). Spatial summation across the vertical meridian in hemianopics: A test of blindsight. Neuropsychologia, 24, 749–758. Pasik, T., & Pasik, P. (1971). The visual world of monkeys deprived of striate cortex: Effective stimulus parameters and the importance of the accessory optic system. Vision Research, Suppl. 3, 419–435. Pasik, P., & Pasik, T. (1982). Visual function in monkeys after total removal of visual cerebral cortex. Contributions to Sensory Physiology, 7, 147–200. Rafal, R., Smith, W., Krantz, J., Cohen, A., & Brennan, C. (1990). Extrageniculate vision in hemianopic humans: Saccade inhibition by signals in the blind field. Science, 250, 118–121. Riddoch, G. (1917). Dissociation of visual perceptions due to occipital injuries, with especial reference to appreciation of movement. Brain, 40, 15–57. Stoerig, P. (1987). Chromaticity and achromaticity: Evidence for a functional differentiation in visual field defects. Brain, 110, 869–886. Stoerig, P., & Cowey, A. (1997). Blindsight in man and monkey. Invited review article. Brain, 120, 535–559. Stoerig, P., Faubert, J., Ptito, M., Diaconu, V. & Ptito, A. (1996). No blindsight following hemidecortication in human subjects? NeuroReport, 7, 1990–1994. Taylor, J. L., & McCloskey, D. I. (1990). Triggering of preprogrammed movements as reaction to masked stimuli. Journal of Neurophysiology, 63, 439–446. Torjussen, T. (1976). Residual function in cortically blind hemifields. Scandinavian Journal Psychology, 17, 320–323. Walker, R., & Mattingley, J. B. (1997). Ghosts in the machine? Pathological visual completion phenomena in the damaged brain. Neurocase, 3, 313–335. Weiskrantz, L. (1986). Blindsight: A case study and implications. Oxford UK: Oxford Univ Press. Received April 13, 1998
7, 312–323 (1998)
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Effects of Unseen Stimuli on Reaction Times to Seen Stimuli in Monkeys with Blindsight 1 Alan Cowey,* Petra Stoerig,† and Carolyne Le Mare* *University of Oxford, Department of Experimental Psychology, South Parks Road, Oxford OX1 3UD UK; †Heinrich-Heine-Universita¨t, Inst. Physiol. Psychology, Universita¨tsstr 1, Bldg 23.03, 40225 Du¨sseldorf, Germany In three macaque monkeys with unilateral removal of primary visual cortex and in one unoperated monkey, we measured reaction times to a visual target that was presented at a lateral eccentricity of 20° in the normal, left, visual hemifield. When an additional stimulus was presented at the corresponding position in the right hemifield (hemianopic in three of the monkeys), it significantly slowed the reaction time to the left target if it preceded it by delays from 100–500 msec. The most effective delay depended on the particular experimental paradigm and perhaps on the experience of the monkey with the task. The results show that reaction times to seen targets in the normal hemifield of monkeys are influenced by the presentation of ‘‘unseen’’ targets in the anopic hemifield, as in some patients with cortically blind visual field defects. 1998 Academic Press
INTRODUCTION
When the primary visual cortex (area V1) is destroyed or severed from its thalamocortical input, a human patient is cortically blind in the resulting field defect. Visual stimuli are no longer consciously seen, with the possible exception in a minority of patients that rapidly moving stimuli of high luminance contrast are sometimes perceived (Riddoch, 1917), for example, as faint moving shadows (Barbur, Watson, Frackowiak, & Zeki, 1993). Despite their lack of conscious vision, some patients show excellent detection, localization, and discrimination of visual targets when required to guess about the nature of targets presented within the blind region (see Stoerig & Cowey, 1997, for review). This paradoxical ability is termed ‘‘blindsight’’ (see Weiskrantz, 1986, for an historical review). Residual visual processing can also be uncovered by studying the effects (if any) of unseen stimuli on the overt response to consciously perceived targets in the normal part of the visual field. There are several examples of such implicit processing, e.g., the alteration in the perceptual judgment of shape when parts of the shape are genuinely absent, or are present but in the blind region (Torjussen, 1976; for review, see Walker & Mattingley, 1997). Here, we are concerned with the effects of a target confined to the blind field on reaction times to a seen stimulus in the sighted field, first demonstrated by Marzi, Tassinari, Aglioti, and Lutzemberger (1986) and since confirmed in human subjects in several ways (Corbetta, Marzi, Tassinari & Aglioti, 1990; Rafal, Smith, Krantz, Cohen, & Brennan, 1990). Implicit processing indirectly revealed in this way has Address correspondence and reprint requests to Professor Alan Cowey, University of Oxford, Department of Experimental Psychology, South Parks Road, Oxford OX1 3UD, UK. E-mail: [email protected]. 312 1053-8100/98 $25.00
Copyright 1998 by Academic Press All rights of reproduction in any form reserved.
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the advantage of not requiring the subject to guess or to make any subjective judgment about confidence levels or visual awareness. Whether cortically blind monkeys show such implicit processing of visual targets is not known, although their ability to detect and localize visual targets has been repeatedly demonstrated (Cowey, 1967; Cowey & Stoerig, 1997; Klu¨ver, 1949; Pasik & Pasik, 1971; Pasik & Pasik, 1982). We therefore studied four monkeys in a reaction time task, in which the animal itself initiated presentation of a target in its normal left hemifield and had to touch it promptly. On half of the trials, at random, a second light appeared at the same time or earlier in the opposite hemifield, which was blind in three of the animals. However, all three possessed blindsight in their hemianopic field (Cowey & Stoerig, 1995, 1997). The results reveal implicit processing in that the unseen target slowed the response to the seen target when it preceded it by several hundred msec. EXPERIMENTAL METHODS
Subjects We studied four macaque monkeys. One of them was normal (Rosie). In the other three, the striate cortex of the left hemisphere had been removed 10 years before the present investigations and when the monkeys were already adult. Details of the surgery, neurohistology on the excised occipital lobes, and magnetic resonance anatomical images of two of the operated monkeys have been published elsewhere (Cowey & Stoerig, 1997). Subsequent to the experiment reported here, the third operated monkey (Lennox) had to be perfused, because he was seropositive for Herpes simiae, and histological examination showed that the striate cortex of the left hemisphere had been totally excised and that the dorsal lateral geniculate nucleus was degenerated throughout its extent. Apparatus and Testing Procedure The apparatus has been described before (Cowey & Stoerig, 1997). The monkeys were trained, with food rewards, to squat in a primate chair and raise the head through a hole in an adjustable horizontal platform while plastic baffles were adjusted to prevent gross head movements. The chair was locked in position in front of a visual display unit (VDU), so that the monkey directly faced the display, with the eyes 27 cm from the center of the screen. The monkeys could reach out and touch any part of the display and also retrieve rewards from a food well beneath it. Visual stimuli were presented on a 35-cm color monitor (Microvitech 895) at the monkeys’ reaching distance. The stimuli were generated and controlled by a microcomputer. Their luminance was measured with a Minolta LS-110 digital luminance meter calibrated for human CIE photopic spectral sensitivity. Immediately in front of the VDU was an infrared touch screen that recorded, with a spatial resolution of about 0.5 cm, where the monkey touched the display. The effective response area on the screen was set to coincide with the area of the 4° start light and the target on the left. At the top and each side of the VDU was a 2° infrared light source, pointing at
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the monkey’s eyes. These lights provided three specular reflections on the pupil of each eye and allowed us to watch the eyes on a remote video monitor by means of an infrared sensitive camera mounted next to the topmost light. The camera provided a clear view of the eyes and showed that, when the monkeys reached out to start a trial, they always looked at the start light. Therefore, the visual stimuli could reliably be presented at known retinal positions. When the monkey touched the start-light to initiate each trial, both the disappearance of the start light and the appearance of the target light (unless it was deliberately delayed) occurred at the beginning of the next frame of the raster display, and only then did the reaction time count begin on the computer’s clock. The start of each trial was therefore time-locked to the appearance of the target on the left. However, as the scan time of the infrared touch screen was 17 msec, the mean error in its registration of a response was 8.5 msec. Although the registered response was instantly detected by the system clock, the error in measuring latencies was ⫹/⫺ 8.5 msec. The displays are shown schematically in Fig. 1. On each trial, the start light appeared at the center of the VDU and remained there until the monkey touched it. The start light, the target simulus on the left, and the stimulus on the right (when present) all subtended 4 ⫻ 4 degrees. The stimuli to the left and right of the start light were 20° eccentric to the vertical midline. They were present for 1 s and the monkeys almost invariably responded well before the target disappeared. On trials when they did not, no reaction time was recorded. As long as the monkey touched the target stimulus on the left before it disappeared, a reward (nut or raisin) was immediately delivered to the foodwell beneath the VDU. The trial ended after each response, and after a further delay of 3 s, the next trial began with the reappearance of the start light. The reaction time for each trial was recorded and saved for subsequent analysis. Each testing session consisted of 100 trials. During the first 10 sessions the target stimulus appeared on the left on every trial when the monkey pressed the start light (Fig. 1A). No stimulus was ever presented on the right. These sessions were used to establish baseline reaction times without possible interference from a simultaneous or prior stimulus on the right. On subsequent groups of sessions, described in more detail under Results, the target stimulus appeared with a delay of 100–500 msec after the monkey started the trial, but on half of the trials, an additional light appeared on the right as soon as the trial was started (Fig. 1B). In other words the additional stimulus on the right, which lay in the hemianopic field of three of the monkeys, preceded the target stimulus by 0–500 msec. This temporal difference is referred to as the stimulus onset asynchrony (SOA), and we analyzed the data in order to measure any difference in reaction time between trials when the target light on the left appeared alone, or with, or shortly after the light on the right. This difference in speed of reaction to the left target was measured for each SOA between the right and left stimuli. In the last testing condition, the target light could appear, at random, at any one of three vertically separated positions on the left, either alone (Fig. 1C), or with the ‘‘irrelevant’’ light on the right (Fig. 1D). The testing took place in a dimly lit room where the luminance of the white walls to either side of the monkey was about 4 cd.m ⫺2. The mean luminance of the VDU
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FIG. 1. Schematic representation of the visual display and the response sequence. Each trial began with the display shown in the center, which remained until the monkey touched the start light. In the first procedure, it was followed by the display shown in A and the monkey had to touch the target at the left. In the next procedure, A or B would occur but the required response was the same. In the final procedure, touching the start light always produced, at random, a target at one of three positions on the left (all three indicated in the figure) and with various delays. On half of these trials a light was also immediately presented on the right, i.e., at the same time as the target on the left or before it. On every trial, the monkey had to respond by touching the target on the left.
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TABLE 1 Reaction Times, msec, to a Target Presented by the Monkey Itself in the Left Visual Hemifield Mean RT and SD Dracula Lennox Rosie Wrinkle
469 516 404 623
sd sd sd sd
135 113 111 114
Standard Error of mean 4.4 3.8 3.9 3.9
Note. Means are based on a total of 1000 trials for each monkey over ten consecutive testing sessions.
was 2.0 cd.m ⫺2 and the luminance of the occasional stimulus in the right hemifield was always 40 cd.m ⫺2. The luminance of the target stimulus on the left was either 40 cd.m ⫺2 or 20 cd.m ⫺2, according to testing conditions described in Results. RESULTS
Initial Training For ten consecutive sessions, providing a total of 1000 trials, the monkeys were presented only with the display shown by route A at the top of Fig. 1. After starting the trial, the target light appeared instantly on the left at a luminance of 40 cd.m ⫺2. The results are shown in Table 1. Although the four monkeys responded at different speeds, each was highly consistent, as shown by the small standard error of the mean response latency. Testing with Dual Stimuli (a) SOA ⫽ 0 msec. Immediately after this initial training each monkey was tested for 200 trials on half of which, at random, a stimulus identical to the target stimulus appeared at the same time and for the same duration in the right visual hemifield, which was anopic in three of the monkeys. The purpose was to see whether this novel and additional stimulus in the hemianopic field influenced the reaction time to the target on the left. There were no statistically significant differences ( p ⬎ .05) between the mean reaction time on trials with one or with two stimuli, even for the monkey (Rosie) with both visual hemifields intact (see Table 2). Nor were there any differences detectable to us when watching the monkeys’ eyes or hands on the video monitor, with one exception. On the first few trials, the unoperated monkey, Rosie, seemed disconcerted by the dual simultaneous presentation and visibly paused and even oriented to the right before responding as usual on the left. (b) SOA ⫽ 0, 100, 200 or 300 msec. Although an unexpected stimulus on the right had no effect on the reaction time to the expected stimulus on the left when both were presented simultaneously, there might be an effect on reaction time if the irrelevant stimulus precedes the relevant one, as in some patients when it appeared in the
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TABLE 2 Reaction Times in msec to a Target Stimulus Presented on the Left, Either Alone or at the Same Time as an Identical but Irrelevant Stimulus on the Right
Dracula Lennox Rosie Wrinkle
Reaction times to single stimuli
Reaction time to double stimuli
Mean difference (msec)
Probability
t
490 517 363 639
501 540 365 642
11 23 2 3
⬎0.05 ⬎0.05 ⬎0.05 ⬎0.05
0.58 1.24 0.19 0.22
Note. There were no statistically significant differences for any monkey between the mean reaction time to 100 single and 100 dual presentations. The highest t value of 1.24 was well below the critical value of 1.96 required for p ⫽ ⬍.05.
clinically blind field defect (Marzi et al., 1986). In the next stage of the experiment, we therefore introduced a variable delay (0, 100, 200, or 300 msec) between the disappearance of the start-light and the appearance of the target on the left, but on half the trials, the irrelevant stimulus was presented on the right and without delay, i.e., coinciding with or preceding the target. There were eight testing sessions (800 trials) and a single SOA was used in each, first in ascending order from 0–300 and then in the reverse order. The results are shown in Fig. 2. In all four monkeys, the largest difference between reaction time on single and dual stimulus trials occurred at a SOA of either 200 or 300 msec. We carried out multiple t tests for each monkey (i.e., four t tests for each) on the basis of the z-scores, in view of uncertainties about the acceptability of an analysis of variance on difference scores. As we had already determined that there was no difference in reaction time to a single target or to two stimuli when the SOA was zero, we were concerned only with the possible effect of the three SOAs from 100–300 msec. Given that that were three comparisons for each monkey but that each monkey is considered independently, we used the appropriate correction for multiple comparisons on each monkey. The results are shown by the filled circles in Fig. 2. Each difference score indicated by an asterisk is significant at p ⬍ .03, z ⫽ ⬎2.58. The prior presentation of the stimulus on the right clearly affected reaction time in all monkeys, but only at a SOA of 200 msec in Dracula and 300 msec in Wrinkle. The prior stimulus on the right slowed the response to the target on the left, even though it was presented well within the field defect of the hemianopic monkeys. Could it have been detected by any artefact in the raster display on the left side of the VDU and therefore in the intact hemifield? Such artefacts can arise at the left edge of any raster line that contains a large change in luminance or can even be reflections along the curved left edge of the VDU. To control for these possibilities we covered the position of the stimulus on the right with black tape, 5 ⫻ 5° and therefore slightly larger than the stimulus as well as standing proud of it as a result of being on the protective glass panel in front of the CRT. The light was no longer directly visible but any artefacts on the left should remain and indeed did so when we lowered the screen mean luminance effectively to zero and ourselves viewed the display from the position of the monkey. Each monkey received 800 trials (200 for each SOA) as before. The results are shown by the unfilled circles in Fig. 2. The
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FIG. 2. The difference in reaction time between the response to a target presented on the left and the response to the same target when a light was presented on the right, at the same time or up to 300 msec earlier (the SOA). Filled circles show the results when the stimulus on the right was visible. Unfilled circles show the results of covering the stimulus on the right. Error bars show the standard error of the mean. In this and the following figures, the value for each SOA indicates the difference between the mean of all the trials when the target appeared alone and all those when it was preceded by a stimulus on the right at the SOA used in that session and a similar session repeated later. An asterisk indicates that the mean difference was statistically significant at p ⫽ ⬍ .05, after appropriate correction for multiple comparisons.
light on the right now had no effect on reaction time in any monkey. Screening the stimulus on the right in this way does not control for intraocular scatter, of course, but the luminance contrast should have been below the levels detectable by intraocular scatter (Stoerig, Faubert, Ptito, Diaconu, & Ptito, 1996). Furthermore, when an almost identical stimulus was presented binocularly (in the same apparatus but for reasons unconnected with the present experiment) in the phenomenally blind right hemifield of GY, a human hemianope with blindsight, he did not report any awareness
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FIG. 3. Differences in reaction time, again using the procedure shown in Fig. 1A and B, but where additional SOAs were introduced and the luminance of the target on the left was reduced in an attempt to make the prior stimulus on the right more salient. Statistically significant lengthening of reaction time to the left target occurred in three monkeys, but not in one of the hemianopic monkeys (Dracula).
of light generated by intraocular light scatter, even though he does report such a visual percept at much higher levels of stimulus contrast, well above those used with the monkeys. (c) SOA ⫽ 0–500 msec. As the greatest difference in reaction time to single and double presentations occurred at the longer SOAs, with no evidence that a maximum difference had been reached, longer SOAs of 400 and 500 msec were tested. In addition, the luminance of the target on the left was reduced from 40 to 20 cd.m ⫺2 while keeping the luminance of the stimulus on the right at 40 cd.m ⫺2. The monkeys were tested for 1200 trials over 12 sessions. The results are given in Fig. 3, and show that the normal monkey and two of the hemianopic monkeys lengthened their reaction time to the now relatively less intense left target when it was preceded by the stimulus
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on the right. Again allowing for multiple comparisons, the increase was statistically significant ( p ⬍ .05) at every SOA from 200 to 500 msec in two of the monkeys and from 300 to 500 in Wrinkle, as well as at 100. There was no indication that the maximum effect had been reached or passed at the longer SOAs. In hemianopic monkey Dracula, the effect of SOA was substantially smaller, and was not statistically significant at any SOA. We noticed that, in all four monkeys, but especially Dracula, the increase in reaction time when a longer SOA was present was greater in the earlier than in the later testing sessions. A likely explanation is that the monkeys were learning that, as the target stimulus on the left always appeared in the same position, they could anticipate its appearance by moving the responding hand towards the appropriate position even before the target had appeared. We therefore carried out a final procedure in which the target on the left appeared, randomly, at any of three positions on the left (see Fig. 1 C, D), meaning that the monkeys could not predict its position and could therefore not effectively preprogram their response to a particular location, although they could, possibly, begin to move to the left. The position of the prior stimulus on the right was unaltered. The monkeys were again tested for 1200 trials, over 12 sessions and the results are shown in Fig. 4. Monkeys Rosie (normal) and Lennox took significantly longer to respond at SOAs of 200–500 or 200–400 msec but Wrinkle was significantly slower only at a SOA of 400 msec (all p ⬍ .05 after correction for multiple comparisons). Dracula was still unaffected by the stimulus on the right at any SOA. Interestingly, the effect of SOA lessened at the longest interval for all monkeys, and Dracula was actually faster, but nonsignifiantly so, at an SOA of 500 msec. Two other aspects of Fig. 4 are noteworthy. First, the variance is much greater than before, presumably because of the uncertainty of the position of the target on the left and the fact that three slightly different hand movements were required. An unfortunate consequence of the increased standard errors is that a given difference in reaction time is less significant. Second, the mean differences are lower, some of them conspicuously so, than in the immediately preceding test (Fig. 3) despite the uncertainty of the target position, suggesting that with repeated testing the monkeys were habituating to the light on the right, or that the increased attention to the normal left hemifield in which the target position was no longer invariable, weakened or obliterated the effect of the unseen stimulus on the right. DISCUSSION
Our results show that when a small light is presented in the blind hemifield prior to an expected identical, or similar, light in the normal hemifield, the reaction time to the latter is lengthened in a manner determined by the difference in timing (the SOA) between the two lights. The effect was also present, and was even greater, in a monkey with no visual field defect. A similar effect has been reported in some patients when the prior stimulus was presented in a clinically blind region of the visual field (Marzi et al., 1986; Rafal et al., 1990), where the prior stimulus was not consciously registered. For our own results to be relevant to the findings with patients, it is important that for the hemianopic monkeys, too, the interfering stimulus should be perceptually invisible. Here
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FIG. 4. Differences in reaction time using the displays shown in Fig. 1C and D, where the exact position of the target on the left was unpredictable. In the normal monkey (Rosie) and the hemianopic monkeys Lennox and Wrinkle, the prior presentation of a stimulus on the right lengthened the reaction time to the target on the left, but at only one SOA in Wrinkle. None of the reaction time differences was statistically significant in Dracula.
we rely on our prior extensive investigation on the same monkeys in the same apparatus, which showed that although they readily detected brief stimuli of 40 cd.m ⫺2 in the blind hemifield when presented alone, they nevertheless categorized such stimuli as blanks when they were presented in a task that required the animals to discriminate between lights and blanks (Cowey & Stoerig, 1997). We can therefore be confident that, in the present experiment, the interfering targets on the right were unseen, i.e., phenomenally invisible, as with neurological patients with blindsight (Stoerig & Cowey, 1997). Could the effects of introducing an SOA be attributed to some unspecified and unwanted feature of the presence of a real visual stimulus on the right, for example, artefacts at the left of the screen in the intact visual field? The results of presenting but covering the stimulus on the right show this possibility to be unfounded. The
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difference scores for single and double presentations were no longer significantly different (Fig. 2). A notable feature of blindsight is that it has been reported in only a minority of patients with clinically blind field defects (e.g., Stoerig, 1987). Although the explanation is still unclear, this variability probably reflects the extent of the extra-striate as well as striate cortical damage, the type of visual stimuli used, and the method used, e.g., yes/no judgments or forced-choice guessing. Here, all three hemianopic monkeys showed evidence of implicit processing of visual stimuli presented in the hemianopic region, perhaps because the direct extrastriate damage was minimized and a direct manual response was required. Nevertheless, there was variation in the results, with monkey Dracula consistently showing less evidence of implicit processing than the other two hemianopic monkeys, despite our earlier demonstration, using forcedchoice responding, that his sensitivity to light in the hemianopic field was no less impaired than that of monkey Lennox and much less impaired than that of Wrinkle (Cowey & Stoerig, 1997). Nor can the relative ineffectiveness of the light in his hemianopic field in the present experiment be attributed to impetuousness in responding on the left because his reaction times, although shorter than those of the other two hemianopic monkeys, were longer than those of the normal monkey (Table 1). Further speculation on reasons for his different behaviour would be easy but unconvincing, since we know almost nothing about his extra-striate cortical damage, his cognitive strategies, and his physiological habituation to irrelevant visual stimuli. The more important result is that he too showed implicit processing initially. What is the basis of implicit processing as revealed by the effects of unseen targets on reaction time to seen targets? If a prior unseen target triggered a saccadic eye movement in its direction, the effects that we observe in monkeys and others have observed in patients would not be surprising. We know of no measurements or observations of this possibility in human subjects. However, apart perhaps from the first occasion on which dual targets were presented to the monkeys, we saw no eye movements towards the stimulus on the right, even at SOAs of several hundred msec. Even though the stimulus on the right was present for 1s, we saw no attempts to inspect it. Further, an actual and complete movement to the right would be expected to delay the response to the left more than it did. Of course, any tendency to make a rightward eye movement might have been suppressed by the monkeys and this could have delayed the response to the left, rather like the delay shown by human subjects when they have to make a saccadic eye movement in the opposite direction to a visual stimulus (an antisaccade) rather than towards it. We have no direct evidence bearing on this possibility. That an unseen stimulus presented before a seen one has an effect on reaction time has also been demonstrated in normal human observers when the first stimulus was followed by the second at SOAs below the visual temporal resolution required for conscious perception (Taylor & McCloskey, 1990). Targets that are not phenomenally detected can thus modulate visually guided behavior not only in blindsight, but in normal nonreflexive visual processing as well. ACKNOWLEDGMENT We thank the UK Medical Research Council (Programme Grant G971/397/B) and the Deutsche Forschungsgemeinshaft for their generous support. We also gratefully acknowledge statistical advice
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from Dr. David Popplewell and a network travel grant from the Oxford McDonnell–Pew Cognitive Neuroscience Centre.
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