SUMMARY Inferior temporal (IT) object representations have been intensively studied in monkeys and humans, but representations of the same particular objects have never been compared between the species. Moreover, IT’s role in categorization is not well understood. Here, we presented monkeys and humans with the same images of real-world objects and measured the IT response pattern elicited by each image. In order to relate the representations between the species and to computational models, we compare response-pattern dissimilarity matrices. IT response patterns form category clusters, which match between man and monkey. The clusters correspond to animate and inanimate objects; within the animate objects, faces and bodies form subclusters. Within each category, IT distinguishes individual exemplars, and the within-category exemplar similarities also match between the species. Our findings suggest that primate IT across species may host a common code, which combines a categorical and a continuous representation of objects.
Our mental representation of object categories is hierarchically organized, and our rapid and seemingly effortless categorization ability is crucial for our daily behavior. Here, we examine responses of a large number (>600) of neurons in monkey inferior temporal (IT) cortex with a large number (>1,000) of natural and artificial object images. During the recordings, the monkeys performed a passive fixation task. We found that the categorical structure of objects is represented by the pattern of activity distributed over the cell population. Animate and inanimate objects created distinguishable clusters in the population code. The global category of animate objects was divided into bodies, hands, and faces. Faces were divided into primate and nonprimate faces, and the primate-face group was divided into human and monkey faces. Bodies of human, birds, and four-limb animals clustered together, whereas lower animals such as fish, reptile, and insects made another cluster. Thus the cluster analysis showed that IT population responses reconstruct a large part of our intuitive category structure, including the global division into animate and inanimate objects, and further hierarchical subdivisions of animate objects. The representation of categories was distributed in several respects, e.g., the similarity of response patterns to stimuli within a category was maintained by both the cells that maximally responded to the category and the cells that responded weakly to the category. These results advance our understanding of the nature of the IT neural code, suggesting an inherently categorical representation that comprises a range of categories including the amply investigated face category.
The inferior temporal cortex (IT) of primates is thought to be the final visual area in the ventral stream of cortical areas responsible for object recognition. Consistent with this hypothesis, single IT neurons respond selectively to highly complex visual stimuli such as faces. However, a direct causal link between the activity of face-selective neurons and face perception has not been demonstrated. In the present study of macaque monkeys, we artificially activated small clusters of IT neurons by means of electrical microstimulation while the monkeys performed a categorization task, judging whether noisy visual images belonged to 'face' or 'non-face' categories. Here we show that microstimulation of face-selective sites, but not other sites, strongly biased the monkeys' decisions towards the face category. The magnitude of the effect depended upon the degree of face selectivity of the stimulation site, the size of the stimulated cluster of face-selective neurons, and the exact timing of microstimulation. Our results establish a causal relationship between the activity of face-selective neurons and face perception.
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