RESPONSE PROPERTIES OF NEURONS IN TEMPORAL CORTICAL VISUAL AREAS OF INFANT MONKEYS

1. Inferior temporal cortex (IT) is a ''high-order'' region of primate temporal visual cortex implicated in visual pattern perception and re cognition. To gain some insight into the development of this area, we compared the properties of single neurons in IT in infant monkeys rang ing from 5 wk to 7 mo of age with those of neurons in IT in adult anim als. Both anesthetized and awake behaving paradigms were used. 2. In i mmobilized infant monkeys under nitrous oxide anesthesia, the incidenc e of visually responsive cells was markedly less than in adult monkeys studied under similar conditions. In infants 4-7 mo of age, only half of IT neurons studied were visually responsive, compared with >80% in adult monkeys. In monkeys <4 mo old, even fewer (<10%) could be visua lly driven. ''Habitution'' of IT cells to repeated stimulus presentati on appeared more pronounced in infant monkeys under nitrous oxide anes thesia than in adult animals. 3. IT cells in the anesthetized infant m onkeys that did respond showed receptive field properties similar to t hose of responsive adult IT neurons studied under similar conditions. Two thirds the receptive fields plotted in the anesthetized 4 to 7-mo- old group were bilateral, and median field size did not differ between the infants and comparable adult groups, being approximately 20-degre es on a side in each case. 4. In contrast to the results obtained unde r anesthesia, most IT cells in alert infant monkeys 5 wk-7 mo of age ( 80%) were responsive to visual stimuli, and this incidence of visually responsive IT neurons did not differ from that obtained in awake adul t macaques. However, response magnitude, measured as spikes per second above baseline rate, was significantly lower in the infant alert samp le than in the adult control (5.2 vs. 12.6 spikes/s, mean +/- SE, devi ation from spontaneous rate, respectively). 5. In addition to having l ower magnitudes of visual response IT cells in the awake infants also tended to have longer and more variable latencies. The overall mean fo r the infant cells was 196 ms, compared with an overall mean of 140 ms for IT neurons in the alert control adult. 6. Although the magnitude of response of neurons in alert infant IT cortex was lower overall, th e incidence and features of stimulus selectivity shown by alert infant IT neurons were strikingly similar to those of IT cells of both anest hetized and unanesthetized adult monkeys. Within the 2nd mo of life (i .e., as early we could test), individual IT neurons exhibited response s selective for shape (boundary curvature), for faces, for arbitrary g eometrical patterns, and for color. Several measures of form selectivi ty for the alert infant and adult samples indicated that the overall d egree of stimulus selectivity did not differ between the groups. 7. Fo r both anesthetized and alert infant groups, rates of spontaneous acti vity in IT cortex were lower than those seen under comparable conditio ns in adult monkeys. The low spontaneous rate in infant temporal corte x in both anesthetized and awake behaving paradigms suggest that the l ow response magnitudes in infant IT reflect general characteristics of cellular function in high-order cortical areas of infant monkeys. 8. We also recorded from neurons in the superior temporal polysensory are a (STP), another high-order region of temporal cortex, which appears t o be involved in analysis of complex visual motion and in orientation functions. The appearance of visual responses in STP paralleled that s een in IT cortex. In the anesthetized infants, responses were virtuall y absent in STP before 4 mo of age, but had adultlike properties when they first appeared in slightly older animals. All visually responsive STP cells studied in 4 to 7-mo-old infants had bilateral visual recep tive fields, and about half were multimodal. Virtually all STP cells s tudied in alert infant and adult animals were visually responsive. 9. As a control for the paucity of visually responsive neurons in IT and STP of the youngest infant monkeys under nitrous oxide anesthesia, we also recorded from striate cortex and extrastriate visual area MT in s everal sessions. Eighty-five percent of cells in these areas were resp onsive, arguing against a general suppression of cortical function. Ce lls in MT were selective for direction of stimulus motion, and cells i n striate cortex were selective for orientation of a bar of light. 10. The delayed contribution of IT cortex to visual behavior in monkeys a nd the slow development of adult capacity are not due to a nonspecific ity of neuronal responses in IT cortex in infancy. Rather, these pheno mena may reflect the weakness of signals deriving from IT within the f irst half year of life and possibly beyond. More generally, the develo pment of adultlike levels of neuronal excitability appears to be more protracted in high-order temporal areas subserving complex functions t han in cortical areas earlier in the monkey visual pathway.