Face-selective neurons during passive viewing and working memory performance of rhesus monkeys: evidence for intrinsic specialization of neuronal coding.

The functional organization of prefrontal cortex (PFC) is a central issue in cognitive neuroscience. Previous physiological investigations have often failed to reveal specialization within the PFC. However, these studies have generally not been designed to examine this issue. Methodological issues such as statistical criteria for specificity, the number of neurons sampled, the extent of cortex sampled, and the number, location and nature of the stimuli used are among the variables that need to be considered in evaluating the results of studies on functional localization. In the present study, we have examined neurons in macaque monkeys trained to fixate while viewing visual stimuli, including faces, or to use them as memoranda on a working memory task. Visual responses of over 1500 neurons were recorded throughout a wide expanse of the PFC (areas 12, 9, 46, 8 and 45). Neurons were considered selective for faces if the best response to a face was over twice as strong as that to any of a wide variety of non-face stimuli. Full electrode track reconstructions in three monkeys revealed in each that neurons which met this criterion were concentrated almost exclusively in three distinct subregions within the projection region of the temporal lobe visual areas. We further show that for all neurons, the most visually selective neurons (for faces, objects or color patterns) were also the most concentrated in the temporal lobe recipient PFC. Similar face selectivity, regional specialization, and delay or delay-like activity were observed in monkeys whether trained on memory tasks or not, which suggests that these are naturally occurring properties of prefrontal neurons. These results confirm neuronal and regional specialization for information processing in PFC and elucidate how heretofore unexamined experimental variables have a strong influence on the detection of regional specialization.