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Previous Article | Next Article
The Journal of Neuroscience, December 15, 2001, 21(24):9824-9836
Selective Perceptual Impairments After Perirhinal Cortex Ablation
Mark J. Buckley, Michael C. A. Booth, Edmund T. Rolls, and David Gaffan Department of Experimental Psychology, Oxford University, Oxford, OX1 3UD United Kingdom
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
It has been suggested that the primate perirhinal cortex contributes exclusively to memory. However, recent studies in macaque monkeys have implied that the perirhinal cortex may also contribute to object perception. To investigate whether the perirhinal cortex does contribute to perception, we devised several perceptual oddity tasks in which monkeys had to choose which stimulus of several presented concurrently on a touch screen was different. Macaques with bilateral perirhinal cortex ablations were selectively impaired relative to controls at perceptually discriminating the odd stimulus when the odd stimulus was a different object and when the discrimination could not be done on the basis of simple differences in features between the stimuli. They remained unimpaired relative to controls on discriminating the odd stimulus when the odd stimulus was a different color, a different shape, or a different size even when these discriminations were extremely difficult. They were also impaired on human and monkey face oddity tasks and oddity tasks with scenes containing objects. Therefore, we reject the notion that the macaque perirhinal cortex has a role exclusive to memory and conclude that the macaque perirhinal cortex does contribute to perception. We argue that the perirhinal cortex is neither specialized for perception nor memory processes alone, but rather, is specialized for processing stimuli that require processing at a more abstract level such as at the level of an object and that the perirhinal cortex contributes to both memory and perception of such stimuli.
Key words: macaque; monkey; primate; perirhinal cortex; learning and memory; perception; amnesia; agnosia
INTRODUCTION
The macaque perirhinal cortex consists of Brodmann's areas 35 and 36 and is situated in the lateral bank of the rhinal sulcus and in the laterally adjacent cortex, although the recognized extent of the perirhinal cortex differs slightly between species and across investigators (Brodmann, 1909
; Amaral et al., 1987
Being located in the anterior medial part of the inferior temporal gyrus, the perirhinal cortex is sometimes considered part of the inferior temporal cortex visual system and therefore a cortical area primarily involved in object perception rather than stimulus memory. Indeed, the most prominent inputs to the perirhinal cortex (64%) are from the laterally adjacent unimodal visual areas TE and TEO (Suzuki and Amaral, 1994a
However, Buckley et al. (1997)
The perirhinal cortex is also characterized by robust interconnections with limbic system structures thought to be crucial for memory. There are strong interconnections with the hippocampal formation via the entorhinal cortex. Approximately 40% of the direct input to the anterior and lateral entorhinal cortex is provided by the perirhinal cortex, and there are also strong return projections from these same regions back to the perirhinal cortex (Insausti et al., 1987
However, Gaffan (1994)
Recently, Buckley and Gaffan (1998) showed that perirhinal cortex lesions further impaired object discrimination learning tasks when object identification demands increased but memory demands remain unchanged. This implied that the role of the perirhinal cortex extends to stimulus identification and is not restricted to stimulus memory. The first aim of this study was to verify that perirhinal cortex lesions impair perception. Because a previous study (Buckley et al., 1997
MATERIALS AND METHODS
Subjects
Eight experimentally naive juvenile rhesus monkeys (Macaca mulatta) took part in this experiment (seven females and one male). Their weights at the start of behavioral testing ranged from 2.2 to 3.7 kg. They were housed either individually or in pairs, in rooms with automatically regulated lighting, and they were given water ad libitum. After preoperative training the animals were assigned into two groups on the basis of preoperative learning scores. Three animals received bilateral perirhinal cortex ablation (PRh), and the remaining five animals remained unoperated controls (CON).Surgery
The operations were performed in sterile conditions with the aid of an operating microscope, and the monkeys were anesthetized throughout surgery with barbiturate (5% thiopentone sodium solution) administered through an intravenous cannula. A detailed description of the surgical procedure has been published elsewhere (Buckley and Gaffan, 1998cHistology
After the conclusion of all behavioral experiments, the animals with ablations were sedated, deeply anesthetized, and then perfused through the heart with saline solution (0.9%), which was followed by formol saline solution (10% formalin in 0.9% saline solution). The brains were blocked in the coronal stereotaxic plane posterior to the lunate sulcus, removed from the skull, allowed to sink in sucrose formalin solution (30% sucrose, 10% formalin), and sectioned coronally at 50 µm on a freezing microtome. Every 10th section through the temporal lobe was stained with cresyl violet and mounted. The intended and actual extents of the lesions are illustrated in Figures 1 and 2. The extents of the perirhinal lesions in two subjects (PRh-2 and PRh-3) were essentially as intended with only slight encroachment into laterally adjacent cortical area TE in one hemisphere of PRh-3. The extent of the intended lesion in one subject (PRh-1) was less than intended but within the area of the intended lesion. This lesion in PRh-3 spared some cortex bilaterally in the lateral bank of the rhinal sulcus and in the cortex immediately laterally adjacent on the anterior ventral surface of the temporal lobe; this lesion also did not extend as far as intended posteriorly in one hemisphere. Thus, one subject (PRh3) acquired a subtotal perirhinal cortex lesion. In none of the subjects did the actual lesion encroach bilaterally into area TE.
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Figure 1. Drawings of ventral views of the macaque brain. The intended location and extent of the ablation of the perirhinal cortex is illustrated by the shaded region on the drawing on the left. The shaded regions on the other three drawings illustrate the actual extents of the ablations in subjects PRh-1, PRh-2, and PRh-3. To aid in visual matching of these ventral views to the coronal sections in Figure 2, the left hemisphere is shown on the right of each of these figures, and the numerals represent the distance in millimeters from the interaural plane.
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Figure 2. Drawings of coronal sections through the area of the lesion. The column on the left (Intended Lesion) shows the intended location and extent of the lesion on drawings of coronal sections from a standard macaque monkey brain from the Laboratory of Neuropsychology (National Institutes of Health, Bethesda, MD). The other three columns (PRh-1, PRh-2, PRh-3) show drawings of actual coronal sections through our lesioned monkey's brains matching those in the Intended Lesion column. Different sections were required to match the levels for the left and right hemisphere for monkey PRh-3. To aid in visual matching of these coronal sections to the ventral views in Figure 1, the left hemisphere is shown on the right of each of these figures, and the numerals represent the distance in millimeters from the interaural plane.
Apparatus
The present tasks were performed on an automated test apparatus. The subject sat in a wheeled transport cage fixed in position in front of a touch-sensitive screen (380 mm × 280 mm) on which the stimuli could be displayed. The subject could reach out between the horizontal or vertical bars (spaced ~45 mm apart) at the front of the transport cage to touch the screen. An automated pellet delivery system, controlled by the computer, delivered reward pellets into a food well (~80 mm in diameter) that was positioned in front of and to the right of the subject. Banana-flavored reward pellets (190 mg supplied by Noyes Company Inc.) were only delivered in responses to a correct choice made by the subject to the touch screen. Pellet delivery was accompanied by an audible click. An automated lunch box (approximate dimensions were: length 200 mm, width 100 mm, height 100 mm) was positioned in front of and to the left of the subject. The lunch box was spring-loaded and opened immediately with a loud crack on completion of the whole task. The lunch box contained the subject's daily diet of wet monkey chow, proprietary primate pellets, nuts, raisins, and a slice of apple, banana, and orange. An infrared camera was positioned looking down into the transport cage from above to allow the subject to be observed while it was engaged in the task. The whole apparatus was housed in an experimental cubicle that was dark apart from the background illumination from the touch screen. The presentation of the visual stimuli on the touch screen was controlled by a computer. The computer also recorded the responses that subjects made to the touch screen and controlled the delivery of reward pellets after correct responses, and it controlled the opening of the lunch box after completion of the session.Stimuli
Each task in this study used different stimuli, which are described in detail below. In each task the resolution of the SVGA display was set at 800 × 600 pixels. Oddity pretraining stimuli. The stimuli for the oddity pretraining stages were multicolored clip art images of patterns and cartoon-like drawings of objects each with dimensions of 128 × 128 pixels. Five sets of 10 clip art images were used for the "oddity pretraining" stages. In each trial six stimuli were displayed concurrently on the touch screen on a black background in an array consisting of two rows of three stimuli. In each trial, five of the stimuli were identical clip art images, and one stimulus was different. Figure 3(Pre 1 and Pre 2) illustrates two sample trials from the oddity pretraining stage.
Task A stimuli. The stimuli for task A ("image-oddity" and "object-oddity") were digitized images of real objects presented on a touch screen. Two sets of 10 indestructible objects were used in task A. Five different views of each object were captured using a digital camera and converted to grayscale (256 levels) bitmap (BMP) files of dimensions 128 × 128 pixels before presentation on the touch screen. In each trial six stimuli were presented concurrently on the touch screen on a gray background. The stimulus positions were arranged in an array consisting of two rows of three stimuli with the positions of each stimulus randomized between these six stimulus positions. In the image oddity stages of task A, five of the six stimuli were identical views of one object (the particular view was chosen at random), whereas one stimulus was one view of a different object from the same set (the particular view was chosen at random). Figure 3, A1 and A2, illustrates sample trials from the image oddity stage of task A. In the object oddity stages of task A, five of the six stimuli were different views of one object, whereas one stimulus was one view of a different object from the same set (the particular view was chosen at random). Figure 3, C1 and C2, illustrates sample trials from the object oddity stage of task A. Task B stimuli. The stimuli for task B ("color oddity") were colored squares of dimensions 128 × 128 pixels. In each trial six colored squares were presented together on the touch screen on a black background and arranged in an array consisting of two rows of three stimuli. Nine colors were used in task B. One color designated as the base color and used in every trial together with one other color selected pseudorandomly. In each trial either five squares were the base color and one square was the other color or one square was the base color and five squares were the other color. The positions of each of the six stimuli were randomized between the six stimulus positions. Figure 3, B1 and B2, illustrates two sample trials from task B (color oddity). The base color was an equal mix of red and green, with the red and green gun values being set at 40, and the blue gun values being set at zero. Four of the other colors increased in relative "greenness" compared with the base color, whereas the other four colors increased in relative "redness." To generate the four colors increasing in relative greenness, we predetermined that the desired values of the green gun should be 0, 37, 38, and 39, respectively. To generate the four colors increasing in relative redness, we predetermined that the desired values of the red gun should be 0, 27, 34, and 37 respectively. Then the appropriate amount of the nonspecified color (red or green) to be added to equate luminance was determined empirically using a flicker fusion technique with human subjects. There is physiological (Lee, 1991
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Figure 3. Pre 1, Pre 2, Two representative trials from the oddity pretraining stage, in which the subjects have to choose the odd clip art image; A1, A2, two representative trials from the image oddity stage of task A in which the subjects have to choose the odd object; A3, A4, two representative trials from the object oddity stage of task A in which the subjects have to choose the odd object; B1, B2, two representative trials, easy and hard, respectively, from task B (color oddity), in which the subjects have to choose the odd colored square; C1, C2, two representative trials, easy and hard, respectively, from task C (shape oddity), in which the subjects have to choose the odd-shaped stimulus; D1, D2, two representative trials from task D (degraded object oddity), in which the subjects have to choose the odd object behind the mask; E1, E2, two representative trials from the human face image oddity stage of task E, in which the subjects have to choose the odd individual's face; E3, E4, two representative trials from the human face oddity stage of task E in which the subjects have to choose the odd individual's face; F1, F2, two representative trials, easy and hard, respectively, from task F (size oddity), in which the subjects have to choose the odd-sized stimulus; G1, G2, two representative trials from task G (scene oddity), in which the subjects have to choose the odd scene; H1, H2, two representative trials from the monkey face image oddity stage of task H, in which the subjects have to choose the odd individual's face; H3, H4, two representative trials from the monkey face oddity stage of task H, in which the subjects have to choose the odd individual's face.
Behavioral testing
Summary. The subjects were tested on many different tasks during the course of this study. Therefore, a brief summary of the rationale for the series of tasks and an outline of order of testing is provided here. First the subjects learned the oddity principle (selecting the stimulus that differs) extensively preoperatively and learned to transfer the principle to new sets of stimuli. After this pretraining, the subjects were trained on image oddity and object oddity preoperatively. Although both the image oddity and object oddity tasks incorporate objects as stimuli, only the harder object oddity problems require processing at a more abstract "view-invariant" or object level. The easier object oddity problems and all of the image oddity problems can be solved purely on the basis of simple feature discrimination. To assess whether the perirhinal cortex is required for making perceptual discriminations at an object level, the CON and PRh groups were then retested on both of these tasks postoperatively, both with the same stimuli and with new stimuli not seen preoperatively. To assess whether any lesion effect on object oddity was specific to discriminating at an object level and not simply an impairment on any hard oddity discrimination problems, they were subsequently tested postoperatively on several other oddity tasks in the following order: color oddity, shape oddity, degraded object oddity, human face oddity, size oddity, scene oddity, and monkey face oddity. Each of these tasks is described in detail below (some of these tasks were first reported in Abstract form by Buckley et al. (1998)) then all the stimuli immediately disappeared from the screen, and an intertrial interval of 20 sec was commenced. If the subject touched the screen during the intertrial interval, then the intertrial interval was restarted. After the touch screen had not been touched for the entire uninterrupted intertrial interval, the next trial began. Each session continued in this way using in each trial two clip art images taken from a set of 10 clip art images. The two clip art images selected in each trial were chosen at random without replacement so that no clip art image could be used again until all 10 clip art images had been used. In each trial one of the two clip art images selected was randomly assigned to be the S+ and the other the S
90% performance accuracy on that set. On the next day they were transferred to a new set of 10 different clip art images and continued daily training on this set until they reached the same criterion on this set. On the next day they were transferred to yet another set of 10 stimuli, and this process continued until the subjects had reached criterion on five different sets of 10 stimuli. Attaining criterion on the first set took on average of 25 sessions. Attaining criterion on subsequent sets took successively fewer days, demonstrating that the subjects were learning to transfer the oddity principle to new stimuli. Attaining criterion on the fifth set took only 1.5 sessions on average. At this point the subjects were deemed to have learned to perform the oddity principle, and on the next day they began training on the first experimental task. In each of the following oddity tasks there were no associations that the subject could learn to guide their performance from trial to trial. In each task the stimuli were randomly assigned to stimulus positions so that the position of the S+ varied from trial to trial. Each of the different stimuli in the tasks were equally likely to be used in a trial (paired and re-paired at random within the constraints of the task) and when chosen to be used were equally likely to be assigned to be the S+ or S
Task C: shape oddity. New postoperative training on task C (shape oddity) commenced on the next day. The shape oddity task was similar to the previous oddity tasks except that the stimuli were polygons of varying numbers of sides (described in detail in the stimulus section above). The subjects had to select the odd polygon in each trial by making a perceptual judgment that five of the stimuli were polygons of matching shape, and one stimulus was a polygon of a different shape. This task had a difficulty parameter that determined how many sides each of the two polygons had. In every trial one of the polygons had two more sides than the other polygon, but the difficulty parameter determined the mean number of sides of these two polygons. The difficulty parameter was confirmed subjectively. Human subjects judged it harder to distinguish between polygons in problems containing polygons with more sides than in problems containing polygons with fewer sides. Figure 3, C1 and C2, illustrates sample trials with an easier problem (three-sided versus five-sided polygons) and a harder problem (six-sided versus eight-sided polygons), respectively. The difficulty parameter was also confirmed by the performance of the control subjects, who made increasingly more errors on the increasingly difficult problems (Fig. 4C). Trials with different difficulty levels were pseudorandomly intermixed throughout the whole session. The subjects were trained on one session per day on this task following the same procedure as described for the previous oddity tasks. They continued training on this task with one session per day for 12 d. On the first four of these days the subjects were required to attain 50 correct responses to open the lunch box, and on the subsequent 8 d the subjects were required to obtain 100 correct responses to open the lunch box. Thus, the subjects made in total 1000 correct responses on this task in addition to a variable number of errors. Task D: degraded object oddity. New postoperative training on task D (degraded object oddity) commenced on the next day. The degraded object oddity task was similar to the previous oddity tasks except that the stimuli were digitized images of objects behind a mask of random grayscale pixels. The digitized images were the same set of stimuli used in the new postoperative testing of object oddity. This task was identical to that task except for the addition of the mask. Different levels of mask obscured the objects to differing degrees (the masks are described in detail in the stimulus section above). Despite the obscuring mask the subjects had to select the odd object in each trial by making a perceptual judgment that five of the stimuli were different views of a matching object and one stimulus was a view of a different object. Trials with different mask levels were pseudorandomly intermixed throughout the whole session. This level of the mask was designed to be a difficulty parameter to modulate how hard it was to perceive the stimuli. The difficulty parameter was confirmed subjectively in human subjects who judged it harder to perceive the stimuli through the masks that obscured the objects to a greater degree. Figure 3, D1 and D2, illustrates sample trials with less and greater degrees of masking, respectively. However, although there was some indication that the control subjects made more errors on trials with the most severe mask compared with trials with the least severe mask (Fig. 4D), there was not a statistically significant linear trend of increasing error rate made by controls with increasing mask level. Thus, increasing the level of the mask parameter in this task may not increase in a linear manner the difficulty that the subjects in this experiment have in perceiving the objects through the increasing levels of the mask. The monkeys were trained on one session per day on this task following the same procedure as described for the previous oddity tasks. They continued training on this task with one session per day for 7 d. Thus, the subjects made in total 700 correct responses on this task in addition to a variable number of errors. Task E: human face oddity. New postoperative training on task E (human face oddity) commenced on the next day. The human face oddity task was similar to the previous oddity tasks except that the stimuli were digitized images of human faces (described in detail in the stimulus section above). In the first stage "human face image oddity", the subjects had to select the odd stimulus in each trial by making a perceptual judgment that five of the faces were identical views of a matching face and the other stimulus was a view of a different face. Two example trials are illustrated in Figure 3, E1 and E2. The subjects were trained on this task following the same procedure as described for the previous oddity tasks. They performed one session per day until reaching criterion of
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Figure 4. Ai, Mean percentage of difference between the PRh and CON groups in terms of the difference in postoperative versus preoperative performance on problems of increasing difficulty level (1-6) in the object oddity stage of task A. Aii, Individual error scores and mean errors made by the PRh and CON group on a new set of postoperative object oddity discriminations. B, Mean percentage of error made by the PRh and CON groups on problems of increasing difficulty level (1-4) in task B (Color Oddity). C, Mean percentage of error made by the PRh and CON groups on problems of increasing difficulty level (1-6) in task C (Shape Oddity). D, Mean percentage of error made by the PRh and CON groups across different levels of masking (1-6) in task D (Degraded Object Oddity). E, Individual error scores and mean errors made by the PRh and CON group on the human face oddity stage of task. E, F, Mean percentage of error made by the PRh and CON groups on problems of increasing difficulty level (1-4) in task F (Size Oddity). G, Individual error scores and mean errors made by the PRh and CON groups on task G (Scene Oddity). H, Individual error scores and mean errors made by the PRh and CON groups on the monkey face oddity stage of task H.
RESULTS
Task A: image oddity and object oddity
Analysis of preoperative performance
Preoperatively the CON group made a mean of five errors learning the image oddity task to criterion, and the PRh group made a mean of seven errors. There was no significant difference between the performance of the groups on this stage of training (independent samples test: t =Analysis of postoperative reacquisition
Postoperatively the CON group made a mean of 29 errors relearning the image oddity task to criterion, and the PRh group made a mean of only 14 errors. There was no significant difference between the performance of the groups on this stage of training (independent samples test: t = 1.119; df = 6; p = 0.3; NS). This result is consistent with our hypothesis that the PRh group should not be impaired on discriminating between two stimuli, even if they are objects, when the stimuli differ in respect to many simple and moderately complex features. Postoperatively the CON group made a mean of 121 errors relearning the object oddity task to criterion, and the PRh group made a mean of 143 errors. Considering postoperative performance alone on the performance of both groups averaged over all the different problems, there was no significant difference in performance between the groups (independent samples test: t =Analysis of postoperative reacquisition relative to preoperative performance
The mean differences in performance between the two groups across different levels of our difficulty parameter are illustrated in Figure 4Ai (see Table 1 for individual scores averaged across difficulty levels). Analysis of this difference in postoperative performance relative to preoperative performance showed that the PRh group was highly significantly impaired relative to that of the CON group [repeated measures ANOVA: group, F = 11.1; df = (1,6); p = 0.016]. Figure 4Ai also shows that the mean difference in postoperative performance relative to preoperative performance between the PRh group, and the CON group tends to increase as problem difficulty increases. Analysis of the linear trend of increase in this deficit with respect to our difficulty parameter did not quite attain statistical significance in a one-tailed test [repeated measures ANOVA: group × difficulty-level, linear trend, F = 2.776; df = (1,6); p = 0.07; one-tailed]. This may be attributable to the fact that our difficulty parameter simply ranked problems, and therefore different levels of this parameter did not necessarily represent regular increases in difficulty. However, Figure 4Ai clearly shows that the deficit in performance of the PRh group relative to the CON group reaches its greatest level and is quite considerable on the hardest problems.
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Table 1. Scores for individual subjects on each task in order of testing together with a summary of the impairments (see Results for details of each analysis) Analysis of new postoperative performance
Postoperatively the CON group made a mean of 15 errors learning the image oddity task with a new set of stimuli to criterion, and the PRh group made a mean of seven errors (see Table 1 for individual scores). There was no significant difference between the performance of the groups on this stage of training (independent samples test: t =Task B: color oddity
For each subject we calculated the mean percentage of error made to each of the four different levels of problem difficulty (problem difficulty was determined by the relative difference in color of the base color from the second color present along either the red or green axis). The data for postoperative performance on the color oddity task are illustrated in Figure 4B (see Table 1 for individual scores averaged across difficulty levels). Analysis of the data shows that there was no interaction between the between-subjects factor, "group" and the within-subjects factor "difficulty level" [repeated measures ANOVA: group × difficulty level, F = 1.95; df = (3,18); p = 0.18; NS], nor was there a significant main effect of group [repeated measures ANOVA: group, F = 3.25; df = (1,6); p = 0.12; NS]. Thus, the PRh group is not impaired at perceptually discriminating between squares of different colors even when the task is very difficult.
Task C: shape oddity
For each subject we calculated the mean percentage of error made to each of the six different levels of problem difficulty. The data for postoperative performance on the shape oddity task are illustrated in Figure 4C (see Table 1 for individual scores averaged across difficulty levels). Analysis of the data shows that there was no interaction between the between-subjects factor, "group" and the within-subjects factor, "difficulty level" [repeated measures ANOVA: group × difficulty level, F < 1; df = (5,30)], nor was there a significant main effect of group [repeated measures ANOVA: group, F < 1; df = (1,6)]. Thus, the PRh group is not impaired at perceptually discriminating between polygons of different shape even when the task is very difficult.
Task D: degraded object oddity
For each subject we calculated the mean percentage of error made to problems under the six different levels of obscuring mask. The data for postoperative performance on the degraded object oddity task are illustrated in Figure 4D (see Table 1 for individual scores averaged across levels of mask). Analysis of the data shows that the interaction between the between-subjects factor, "group" and the within-subjects factor, "difficulty level" linear trend was not quite significant in a one-tailed test [repeated measures ANOVA: group × difficulty level linear trend, F = 3.237; df = (1,6); p = 0.06; one-tailed]. However, the PRh group was significantly impaired relative to the CON group across all levels of mask [repeated measures ANOVA: group, F = 5.584; df = (1,6); p = 0.028; one-tailed]. There was also a significant main effect of mask level [repeated measures ANOVA: mask level, F = 18.074; df = (5,30); p < 0.001].
This task used the same set of object stimuli as the new postoperative object oddity stage of task 1 in which the PRh group was shown to be impaired previously. This analysis shows that the PRh group remain impaired on tasks that involve making perceptual discriminations between objects on the basis of discriminating at the level of objects.
Caution needs to be exercised before concluding that increasing the mask does not increase the size of the deficit of the PRh group because the interaction term is almost significant. However, averaged across all levels and all problems the magnitude of the impairment of the PRh group on this degraded object oddity task is very similar to the magnitude of the impairment of the PRh group on the object oddity task without the mask. Thus, imposing a mask on the object oddity task does seem to make the task harder for all subjects in a perirhinal-independent manner.
Task E: human face oddity
The CON group made a mean of 190 errors learning the human face image oddity stage of task 5 to criterion, and the PRh group made a mean of 800 errors (see Table 1 for individual scores). One subject in the PRh group (PRh1) was deemed to have failed to learn the human face image oddity task after making >2000 errors in 30 sessions without attaining criterion. Therefore, we used a nonparametric test to analyze the mean error data. There was no significant difference between the performance of the groups on this stage of training (Mann-Whitney independent samples rank sum test: U = 4; p = 0.3; NS).
The CON group made a mean of 773 errors learning the human face oddity stage of task 5 to criterion, and the PRh group made a mean of 1278 errors (see Table 1 for individual scores). The data for postoperative performance on the human face oddity task are illustrated in Figure 4E. One subject in the PRh group (PRh1) was deemed to have failed to learn the human face oddity task after making >1500 errors in 32 sessions without attaining criterion. Therefore, we used a nonparametric test to analyze the mean error data. There was a highly significant difference between the performance of the groups on this stage of training because all of the PRh group performed worse than any of the CON group (Mann-Whitney independent samples rank sum test: U < 0.001; p = 0.036).
Thus, the PRh group was significantly impaired relative to the CON group on human face oddity stage of task E but was unimpaired on the human face image oddity stage of task E. This parallels the pattern of impairment on the earlier object image oddity and object oddity tasks.
Task F: size oddity
For each subject we calculated the mean percentage of error made to each of the four different levels of problem difficulty. The data for postoperative performance on the size oddity task are illustrated in Figure 4F (see Table 1 for individual scores averaged across difficulty levels). Analysis of the data shows that there was no interaction between the between-subjects factor "group" and the within-subjects factor "difficulty level" [repeated measures ANOVA: group × difficulty level, F = 1.478; df = (3,18); p = 0.25; NS]. Nor was there a significant main effect of group [repeated measures ANOVA: group, F < 1; df = (1,6)]. Thus, the PRh group is not impaired at perceptually discriminating between squares of different sizes even when the task is very difficult.
Task G: scene oddity
The CON group made a mean of 222 errors learning the scene oddity stage of task 7 to criterion, and the PRh group made a mean of 495 errors (see Table 1 for individual scores). The data for postoperative performance on the scene oddity task are illustrated in Figure 4G. The PRh group was significantly impaired relative to the CON group (independent samples test: t =
One may speculate regarding whether the monkeys view each one of the four scenes in every trial this task as a whole scene containing objects on a background or whether the monkeys view each digitized photograph of a scene as an object in itself. In either case it seems likely that the ability to process stimuli at an object level would facilitate performance on this task and is consistent with the impairment on this task.
Task H: monkey face oddity
The CON group made a mean of 311 errors learning the monkey face image oddity stage of task 8 to criterion, and the PRh group made a mean of 712 errors (see Table 1 for individual scores). However, the PRh group was not significantly impaired relative to the CON group on the monkey face image oddity stage of task 8 (independent samples test: t =
The CON group made a mean of 478 errors learning the monkey face oddity stage of task 5 to criterion, and the PRh group made a mean of 744 errors (see Table 1 for individual scores). The data for postoperative performance on the human face oddity task are illustrated in Figure 4H. The PRh group was found to be significantly impaired relative to the CON group on the monkey face oddity stage of task 8 (independent samples test: t =
Thus, the PRh group was significantly impaired relative to the CON group on monkey face oddity stage of task H but was unimpaired on the monkey face image oddity stage of task H. This parallels the pattern of impairment on the earlier object image oddity and object oddity tasks and also the earlier human face image oddity and human face oddity tasks.
Summary of results
In task 1 the PRh group was impaired relative to the CON group at hard object oddity problems but unimpaired at easier object oddity problems and image oddity problems. Thus, the PRh group was impaired relative to the CON group at making perceptual discriminations when the stimuli were objects and the discriminanda were all of different views and the discrimination could not easily be solved on the basis of simple or moderately complex features of objects. Because the PRh group was subsequently impaired on several further tasks, we can rule out that this impairment is only a relatively transient effect.
The PRh group remained completely unimpaired on very difficult color oddity problems (task B), very difficult shape oddity problems (task C), and very difficult size oddity problems (task F). Thus, we can rule out that the impairment may have been simply related to the perceptual difficulty of the discrimination.
The PRh group was impaired on degraded object oddity problems (task D), human face oddity problems (task D), scene oddity problems (task G), and monkey face oddity problems (task H). The PRh group remained unimpaired on human face image oddity problems (control stage for task D) and monkey face image oddity problems (control stage for task H). Therefore, taken together the pattern of impaired and unimpaired performance on every task shows that the nature of the perceptual impairment after PRh cortex damage is selective. Only problems that require perceptual discrimination at a more abstract level (such as at the level of an object) are impaired, whereas problems that can be solved purely by simple or moderately complex feature discrimination are unimpaired (regardless of whether the problems involve objects).
DISCUSSION
We trained monkeys to make perceptual discriminations to choose the one stimulus of several stimuli that were presented at the same time on the touch screen that was the odd stimulus. After learning the principle, the monkeys were able to easily transfer the principle to a range of different types of stimuli. We used this paradigm to assess whether after bilateral perirhinal cortex ablation there was any impairment in making perceptual discriminations, and if so, whether the impairment was selective to particular types of stimuli. The results from every stage of every task in this study are fully consistent with our hypothesis that the macaque perirhinal cortex contributes to making perceptual discriminations between stimuli when the discrimination requires processing of the stimuli to a more abstract level, such as at the level of an object, but not to perceptual discriminations that can be done on the basis of discriminating between simple or only moderately complex features of objects. Therefore, we conclude that role of the perirhinal cortex in the monkey extends beyond stimulus memory and contributes to object perception.
This is consistent with evidence from earlier lesion studies. Eacott et al. (1994)
This study confirms that the perirhinal cortex does indeed contribute to perception but that it plays a specific role in perception. It contributes when stimuli have to be processed to a more abstract level such as at the level of objects. Perirhinal lesions also disrupt configural learning (Buckley and Gaffan, 1998a
Anatomical evidence also supports the notion that the perirhinal cortex is specialized for processing objects. Saleem and Tanaka (1996)
Electrophysiological evidence also supports the notion that the perirhinal cortex is specialized for processing objects. Brown et al. (1987)
Higuchi and Miyashita (1996)
