The figures in the left, middle, and right columns show the results for Monkeys T, K, and G, respectively. Our results are consistent with the view that area TE is unlikely to be required for discriminations requiring such basic comparisons. To test whether the monkeys would be able to learn a new pair of categories after the ablations, a new stimulus set of 20 cars low incentive and 20 trucks high incentive was introduced.
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Again, the errors were spread across the whole stimulus set Fig. Thus, not only do these monkeys generalize to categories learned before their TE ablation, but they also quickly learn to distinguish between members of a new pair of categories. The results above demonstrate that the monkeys with TE ablations are sensitive to the categorical differences in the cue sets; for example, they make more errors in the unfavorable trials as signaled by the appearance of a cat than in the favorable ones, even though the most advantageous behavior would be to perform all of the trials correctly.
The categorization task Task 1 used above did not require the monkeys to make an explicit choice; we only observed their errors in the face of greater and lower incentives.
We transformed our implicit task into an explicit 2-IFC task with asymmetrical reward, comparable to those used throughout the psychophysical literature Green ; Farah ; Magnussen et al. The two alternative choices were, 1 if a cat appeared release during the red target Interval 1 , to terminate the current trial and move on to the next, and 2 if a dog appeared release during the green target Interval 2 , to collect the reward.
In the simplest terms, that is, the task was to release on red for cat and on green for dog. Within seven sessions, all six monkeys three with TE removals, three unoperated controls learned that the most advantageous response pattern was to release on red when the low-incentive cue appeared and to wait and release on green to collect the liquid reward for the high-incentive cue. Two TE monkeys and one control monkey learned this in four sessions, the other TE monkey in five sessions, and the other two control monkeys in seven sessions the last two control monkeys were naive, never having worked with cues before.
The monkeys were then trained on the set of 20 dogs and 20 cats for four consecutive sessions before being exposed to sets of trial-unique cats and dogs, with cats and dogs each session for four consecutive sessions total, cats, dogs. Thus, when compared to controls in this sequential response task, the TE monkeys show a mild deficit in assigning the pictures correctly to the categories. Symbols and bars indicate correct rates for individual monkeys and their averages, respectively.
To control for the possibility that any impairment in the TE-lesioned monkeys' performance on the categorization and discrimination learning tasks could be accounted for by a simple loss of ability to perceive fine-grained visual attributes, visual acuity was measured in the form of contrast sensitivity across a range of sine wave grating frequencies and compared to that of controls.
Consistent with the human literature Blakemore and Campbell, , control monkeys had difficulty detecting the very lowest and several of the highest frequencies Fig. Contrast sensitivity is plotted on a logarithmic scale against spatial frequency.
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The fitted curves are quadratic functions. The postoperative ability to learn a new categorization rapidly and the ability to generalize all the categorizations on which we tested the monkeys was especially surprising to us, given that TE is thought to play a critical role in discrimination and memory for complex visual stimuli. One explanation for this would be if our ablations did not match those reported in the past where pattern discrimination was severely impaired after bilateral TE removals Iwai and Mishkin, ; Buffalo et al.
Therefore, we tested our three monkeys with TE removals using three additional visual discrimination tasks traditionally used to characterize this type of deficit Iwai and Mishkin, ; Cowey and Gross, This testing was perfomed in a Wisconsin General Testing Apparatus. Our monkeys with TE lesions showed a pattern of behavior across the three discrimination tasks that was consistent with the pattern reported previously Iwai and Mishkin, ; Buffalo et al.
Symbols and bars indicate the numbers of trials for individual monkeys and their averages, respectively. The random sampling cross-validation was repeated with random splits to permit all stimuli to be used in the training and test sets multiple times. Comparing the above results to the classification performance of monkeys in Task 2, it is apparent that normal monkeys perform considerably better than the SVM, and that monkeys with TE lesions perform at the upper limit of what might be expected from the classifier.
To arrive at an explanation of how categorization based on visual similarity occurs in the brain requires first the identification of brain regions that are necessary for this process. As a conjecture, the region or regions that are essential for categorization should receive high-level visual input and be involved in visual memory.
The prefrontal cortex is a candidate region for categorization Freedman et al. Area TE, a lateral temporal brain region, has also been proposed as a candidate region for categorization because it plays a central role in high-level visual processing, object recognition, and object discrimination Iwai and Mishkin, ; Cowey and Gross, ; Gross et al. The results presented here, however, seem to, at least partially, refute this prediction.
In Tasks 1 and 2, monkeys showed only a mild impairment in visual perceptual categorization after TE removal, rather than a severe impairment as might be expected.
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Nevertheless, these monkeys were severely impaired in pattern discrimination learning and eight-item concurrent learning, as has been reported for monkeys with TE lesions Iwai and Mishkin, ; Buffalo et al. Thus, our monkeys with TE lesions have the same pattern of visual learning deficits that have been classically reported for monkeys with TE lesions.
The contrast sensitivity analysis serves a twofold purpose as a control for the explicit test of categorization: it indicates, first, that the visual acuity of the TE-lesioned monkeys is unimpaired, and second, that their ability to grasp the procedural components of the explicit task Task 2 is intact, including high-incentive versus low-incentive contingencies and the two-interval forced choice design. That the results for the explicit task Task 2 parallel those for the implicit task suggests that the mild deficit observed after TE lesions in the implicit task is unlikely to arise from a reduction in attention or motivation, or from a general ceiling effect on the error rate as a result of the lack of an explicit choice option in the implicit task.
One important issue for interpreting these results is whether the monkeys learned to use some single key feature to perform this task. Because these images comprise such a broad, and overlapping, array of parameters, it seems unlikely that any simple feature could be used to distinguish the cats from dogs. To support this qualitative conclusion, we performed an analysis using a linear SVM classifier to discriminate the dogs and cats.
Although it is widely acknowledged that feedback and other interactions are important for object-based visual recognition, it would probably still be assumed that a system with a feedforward circuit leading into area TE and then perhaps to frontal cortex has a central role in the type of visual perceptual categorization studied here Kravitz et al. Even tasks with fixed reward contingencies, such as those reported here, would be expected to recruit TE if the perceptual discriminations required were sufficiently challenging. The effects of aspiration lesions must always be interpreted in light of the possibility of damage to underlying fibers of passage.
In this study, however, the main finding is the relative ineffectiveness of the TE removal for impairing visual generalization; thus, potential damage to fibers of passage does not represent a confound to the interpretation of these results. There are at least four explanations for why lesions of lateral prefrontal cortex Minamimoto et al. First, categorization might be a distributed function, so there is no single critical area. In that case, there should be no single lesion that catastrophically disrupts visual perceptual categorization.
Second, if there is a single critical brain area, it has not been yet identified. Candidates that might yet be consistent with the hierarchical model are the perirhinal cortex, which follows TE in the visual processing hierarchy and is important for stimulus—stimulus and stimulus—reward associations Liu et al.
The difficulty with invoking a vital role for perirhinal cortex is that our TE lesions should have deafferented perirhinal cortex from nearly all of its primary visual input, although it is possible that sufficient information arrives from other areas with major projections to perirhinal cortex, such as TEO and TF Suzuki and Amaral, Third, image analysis within the brain for visual pattern generalization might occur before fine pattern analysis, a result hinted at in single neuronal physiology, where coarse pattern information appears earlier in responses of TE neurons than the information used for fine discriminations Sugase et al.
Finally, it might be that the image analysis used for categorization arises in parallel with and separately from the image analysis that underlies the final steps of pattern discrimination, which would provide an explanation of how rodents might do visual generalization Zoccolan et al.pierreducalvet.ca/39205.php
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Up to this point, there does not seem to be any evidence for separation of image analysis and image categorization; they are generally treated as properties of the same ventral stream process and, at least implicitly, as properties of the same stages of visual processing Poggio et al.
If, as the work described here implies, image analysis and pattern discrimination might be subserved by different tissue, there would need to be a revision of most theoretical models of primate visual processing, which posit that classification and pattern recognition occur concurrently in a mutually dependent manner Poggio et al. Previous studies showed that monkeys with TE lesions are markedly impaired in a delayed nonmatch-to-sample DNMS task even with a short delay period Mishkin, ; Buffalo et al. A categorical DNMS task requires two types of visual memory: longer-term memory for the category and a shorter-term or working memory for a sample cue to compare with the test stimulus that appears after a delay period Freedman et al.
Tasks 1 and 2 only require memory for the category; the cue remains on throughout the trial until the monkey responds, and hence there is no working memory demand. Our results raise questions about how categorization based on visual generalization is perfomed. When a perceptually more ambiguous distinction, dogs versus cats, was presented to the linear classifier, it struggled, whereas normal monkeys did well.
It is possible that the monkeys adopted an alternative strategy based on the functions of cortical areas that remained intact, but a question remains: For what level of ambiguity in categorical discrimination is area TE critical? We thank A. Young, A. Horovitz, and M. Malloy for their technical help. We also thank Drs. Bouret, J. Wittig, A. Clark, W.
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Lercher, J. Simmons, Y. Sugase-Miyamoto, and K. Gothard for their useful discussions. We thank Dr.
Gothard for providing photos of monkey faces. NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses. Skip to main content. Previous Next. Narihisa Matsumoto , Mark A.
Eldridge , Richard C. Saunders , Rachel Reoli and Barry J. Narihisa Matsumoto. Abstract In primates, visual recognition of complex objects depends on the inferior temporal lobe.
Introduction Categorizing visual stimuli through generalization of visual features seems effortless, but has been difficult to replicate in artificial systems Poggio et al. Figure 1. Behavior An overview is provided in Table 1. View this table: View inline View popup.
Table 1. Behavior overview. Initial training. Figure 2. Task 1: implicit categorization task.
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