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 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.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  H F HARLOW,et al.  Performance of infant rhesus monkeys on discrimination learning, delayed response, and discrimination learning set. , 1960, Journal of comparative and physiological psychology.

[2]  H. Harlow,et al.  Learned behavior following lesions of posterior association cortex in infant, immature, and preadolescent monkeys. , 1965, Journal of comparative and physiological psychology.

[3]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

[4]  G L Gerstein,et al.  Single-unit activity in temporal association cortex of the monkey. , 1967, Journal of neurophysiology.

[5]  D. B. Bender,et al.  Visual properties of neurons in inferotemporal cortex of the Macaque. , 1972, Journal of neurophysiology.

[6]  C. C. Goren,et al.  Visual following and pattern discrimination of face-like stimuli by newborn infants. , 1975, Pediatrics.

[7]  R. Boothe,et al.  9 – Perception and Learning in Infant Rhesus Monkeys , 1975 .

[8]  A. Meltzoff,et al.  Imitation of Facial and Manual Gestures by Human Neonates , 1977, Science.

[9]  R. Desimone,et al.  Visual areas in the temporal cortex of the macaque , 1979, Brain Research.

[10]  R. Desimone,et al.  Prestriate afferents to inferior temporal cortex: an HRP study , 1980, Brain Research.

[11]  R. Desimone,et al.  Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. , 1981, Journal of neurophysiology.

[12]  J. Movshon,et al.  Visual neural development. , 1981, Annual review of psychology.

[13]  M. Mishkin A memory system in the monkey. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[14]  J. F. Zolman Ontogeny of Learning , 1982 .

[15]  R. Wurtz,et al.  Visual responses of inferior temporal neurons in awake rhesus monkey. , 1983, Journal of neurophysiology.

[16]  R. Desimone,et al.  Shape recognition and inferior temporal neurons. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[17]  D. Maurer,et al.  Newborn's following of natural and distorted arrangements of facial features , 1983 .

[18]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  T. Albright Direction and orientation selectivity of neurons in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[20]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[21]  Mortimer Mishkin,et al.  Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys , 1986, Behavioural Brain Research.

[22]  P. Goldman-Rakic,et al.  Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. , 1986, Science.

[23]  H. Rodman,et al.  Coding of visual stimulus velocity in area MT of the macaque , 1987, Vision Research.

[24]  H. Spitzer,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. , 1987, Journal of neurophysiology.

[25]  H. Sakai,et al.  Enhancement of inferior temporal neurons during visual discrimination. , 1987, Journal of neurophysiology.

[26]  K. Hikosaka,et al.  Inferotemporal neurons of the monkey responsive to auditory signal , 1987, Brain Research.

[27]  C. Blakemore,et al.  Development of stimulus selectivity and functional organization in the suprasylvian visual cortex of the cat , 1988, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[28]  P. D. Spear,et al.  Development of neuronal responses in cat posteromedial lateral suprasylvian visual cortex , 1988, Brain Research.

[29]  Y. Miyashita Neuronal correlate of visual associative long-term memory in the primate temporal cortex , 1988, Nature.

[30]  D I Perrett,et al.  Frameworks of analysis for the neural representation of animate objects and actions. , 1989, The Journal of experimental biology.

[31]  J. Bachevalier,et al.  Ontogenetic Development of Habit and Memory Formation in Primates , 1990, Annals of the New York Academy of Sciences.

[32]  Age and sex differences in the effects of selective temporal lobe lesion on the formation of visual discrimination habits in rhesus monkeys (Macaca mulatta). , 1990, Behavioral neuroscience.

[33]  E. Miller,et al.  Habituation-like decrease in the responses of neurons in inferior temporal cortex of the macaque , 1991, Visual Neuroscience.

[34]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TE and TEO with medial temporal- lobe structures in infant and adult monkeys , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  Methods for repeated recording in visual cortex of anesthetized and awake behaving infant monkeys , 1991, Journal of Neuroscience Methods.

[36]  Keiji Tanaka,et al.  Coding visual images of objects in the inferotemporal cortex of the macaque monkey. , 1991, Journal of neurophysiology.

[37]  C G Gross,et al.  Stimulus selectivity and state dependence of activity in inferior temporal cortex of infant monkeys. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[38]  R. Desimone,et al.  A neural mechanism for working and recognition memory in inferior temporal cortex. , 1991, Science.

[39]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[40]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[41]  D I Perrett,et al.  Organization and functions of cells responsive to faces in the temporal cortex. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[42]  C. Gross,et al.  Representation of visual stimuli in inferior temporal cortex. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[43]  C. Gross,et al.  Inferior Temporal Cortex: Neuronal Properties and Connections in Adult and Infant Macaques , 1992 .

[44]  B R Payne,et al.  Evidence for visual cortical area homologs in cat and macaque monkey. , 1993, Cerebral cortex.

[45]  H. Rodman,et al.  Cortical projections to anterior inferior temporal cortex in infant macaque monkeys , 1994, Visual Neuroscience.