Categorical representation of visual stimuli in the primate prefrontal and inferior temporal cortices

Abstract

The ability to group stimuli into meaningful categories is a fundamental cognitive process though little is known its neuronal basis. To address this issue, we trained monkeys to perform a categorization task in which they classified visual stimuli into well defined categories that were separated by a "category-boundary". We recorded from neurons in the prefrontal (PFC) and inferior temporal (ITC) cortices during task performance. This allowed the neuronal representation of category membership and stimulus shape to be independently examined. In the first experiment, monkeys were trained to classify the set of morphed stimuli into two categories, "cats" and "dogs". Recordings from the PFC of two monkeys revealed a large population of categorically tuned neurons. Their activity made sharp distinctions between categories, even for stimuli that were visually similar but from different classes. Likewise, these neurons responded similarly to stimuli from the same category even if they were visually dissimilar from one another. In the second experiment, one of the monkeys used in the first experiment was retrained to classify the same stimuli into three new categories. PFC recordings collected after the monkeys were retrained revealed that the population of neurons reflected the three new categories but not the previous (now irrelevant) two categories. In the third experiment, we recorded from neurons in the ITC while a monkey performed the two-category "cat" vs. "dog" task. There were several differences between ITC and PFC neuronal properties. Firstly, a greater proportion of ITC neurons were only stimulus selective but not category tuned.

(cont.) Secondly, while many PFC neurons displayed category tuning that persisted into the memory delay, such tuning in the ITC was primarily observed during stimulus presentation. Thirdly, whereas many PFC neurons reflected the monkeys' decisions about whether a stimulus indicated a behavioral response, most ITC neurons conveyed information about the visual stimuli only, and not about the monkey's task-related decisions. In conclusion, our results suggest that neurons in the PFC and ITC can convey information about the category of visual stimuli. The differences in neuronal responses between the ITC and PFC support the hypothesis that the ITC plays an important role in object recognition and visual learning while the PFC is more involved in cognitive functions related to executive control.