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14 octobre 2007
Journal of Neurophysiology
1993;70(3):1115-1136
Response properties of neurons
in temporal cortical visual areas of infant monkeys
H. R. Rodman, S. P. Scalaidhe and C. G. Gross
Department of Psychology, Princeton University

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temporal cortex
 
1. Inferior temporal cortex (IT) is a "high-order" region of primate temporal visual cortex implicated in visual pattern perception and recognition. To gain some insight into the development of this area, we compared the properties of single neurons in IT in infant monkeys ranging from 5 wk to 7 mo of age with those of neurons in IT in adult animals. Both anesthetized and awake behaving paradigms were used.
 
2. In immobilized infant monkeys under nitrous oxide anesthesia, the incidence 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 visually driven. "Habituation" of IT cells to repeated stimulus presentation appeared more pronounced in infant monkeys under nitrous oxide anesthesia than in adult animals.
 
3. IT cells in the anesthetized infant monkeys that did respond showed receptive field properties similar to those of responsive adult IT neurons studied under similar conditions. Two thirds of 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 degrees on a side in each case.
 
4. In contrast to the results obtained under 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 adult macaques. However, response magnitude, measured as spikes per second above baseline rate, was significantly lower in the infant alert sample than in the adult control (5.2 vs. 12.6 spikes/s, mean +/- SE, deviation from spontaneous rate, respectively).
 
5. In addition to having lower magnitudes of visual response, IT cells in the awake infants also tended to have longer and more variable latencies. The overall mean for 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, the incidence and features of stimulus selectivity shown by alert infant IT neurons were strikingly similar to those of IT cells of both anesthetized and unanesthetized adult monkeys. Within the 2nd mo of life (i.e., as early as we could test), individual IT neurons exhibited responses selective for shape (boundary curvature), for faces, for arbitrary geometrical patterns, and for color. Several measures of form selectivity for the alert infant and adult samples indicated that the overall degree of stimulus selectivity did not differ between the groups.
 
7. For both anesthetized and alert infant groups, rates of spontaneous activity in IT cortex were lower than those seen under comparable conditions in adult monkeys. The low spontaneous rates in infant temporal cortex in both anesthetized and awake behaving paradigms suggest that the low 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 area (STP), another high-order region of temporal cortex, which appears to be involved in analysis of complex visual motion and in orientation functions. The appearance of visual responses in STP paralleled that seen in IT cortex. In the anesthetized infants, responses were virtually absent in STP before 4 mo of age, but had adultiike 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 receptive fields, and about half were multimodal. Virtually all STP cells studied 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 several sessions. Eighty-five percent of cells in these areas were responsive, arguing against a general suppression of cortical function. Cells in MT were selective for direction of stimulus motion, and cells in striate cortex were selective for orientation of a bar of light.
 
10. The delayed contribution of IT cortex to visual behavior in monkeys and the slow development of adult capacity are not due to a nonspecificity of neuronal responses in IT cortex in infancy. Rather, these phenomena may reflect the weakness of signals deriving from IT within the first half year of life and possibly beyond. More generally, the development of adultlike levels of neuronal excitability appears to be more protracted in high-order temporal areas subserving complex functions than in cortical areas earlier in the monkey visual pathway.
 
Responses of an IT neuron in an anesthetized infant monkey that responded preferentially to face stimuli. For each stimulus, the line underneath the PSTH corresponds to the 2-s period during which the stimulus was presented. Stimuli 1-11 were colored slides; stimuli 12-18 were white on a black background. Face stimuli consisted of images of different facial expressions from 2 stimulus monkeys, a profile view of a 3rd, and scrambles of the faces. The stimuli were presented at the fovea and were 3-6° diam.