Activity of neurons in anterior inferior temporal cortex during a short- term memory task

Inferior temporal (IT) cortex of primates is known to play an important role in visual memory. Previous studies of IT neurons during performance of working memory tasks have found modulation of responses when a current stimulus matched an item in memory; however, this effect was lost if other stimuli intervened in the retention interval. To examine how IT cortex retains memories while new stimuli are activating the cells, we recorded from IT neurons while monkeys performed a delayed matching-to-sample task, with multiple intervening items between the sample and matching test stimulus. About half of the cells responded differently to a test stimulus if it matched the sample, and this difference was maintained following intervening stimuli. For most of the affected cells, the responses to matching stimuli were suppressed; however, for a few cells the opposite effect was seen. Temporal contiguity alone could not explain the results, as there was no modulation of responses when a stimulus on one trial was repeated on the next trial. Thus, an active reset mechanism appears to restrict the memory comparison to just the stimuli presented within a trial. The suppressive effects appear to be generated within or before IT cortex since the suppression of response to matching stimuli began almost immediately with the onset of the visual response. The memory of the sample stimulus affected not only the responses to matching stimuli but also those to nonmatching stimuli. There was suggestive evidence that the more similar a nonmatching stimulus to the sample, the more the response was suppressed. About a quarter of the cells showed stimulus- selective activity in the delay interval following the sample. However, this activity appeared to be eliminated by intervening stimuli. Thus, it is unlikely that delay-interval activity in IT contributed to the performance of this particular version of delayed matching to sample. To determine how much information about the match-nonmatch status of the stimulus was conveyed by individual neurons, we analyzed the responses with discriminant analysis. The responses of an individual IT neuron could be used to classify a stimulus as matching or nonmatching on about 60% of the trials. To achieve the same performance as the animal would require averaging the responses of a minimum of 25 IT neurons. There was no evidence that mnemonic information was carried by temporal variations in the spike trains. By contrast, there was a modest amount of temporal variation in sensory responses to different visual stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  D. Robinson,et al.  A METHOD OF MEASURING EYE MOVEMENT USING A SCLERAL SEARCH COIL IN A MAGNETIC FIELD. , 1963, IEEE transactions on bio-medical engineering.

[2]  C. Gross Visual Functions of Inferotemporal Cortex , 1973 .

[3]  P. Dean The effect of inferotemporal lesions on memory for visual stimuli in rhesus monkeys. , 1974, Brain research.

[4]  D. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents , 1975, Brain Research.

[5]  Deepak N. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections , 1975, Brain Research.

[6]  Deepak N. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. II. Frontal lobe afferents , 1975, Brain Research.

[7]  M. Mishkin,et al.  Non-spatial memory after selective prefrontal lesions in monkeys , 1978, Brain Research.

[8]  M. Mishkin Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus , 1978, Nature.

[9]  D. B. Bender,et al.  Activity of inferior temporal neurons in behaving monkeys , 1979, Neuropsychologia.

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

[11]  R. E. Passingham,et al.  Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta) , 1980, Brain Research.

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

[13]  L. Weiskrantz,et al.  Recency effects and lesion effects in delayed non-matching to randomly baited samples by monkeys , 1980, Brain Research.

[14]  A. Mikami,et al.  Inferotemporal neuron activities and color discrimination with delay , 1980, Brain Research.

[15]  J. Fuster,et al.  Inferotemporal neurons distinguish and retain behaviorally relevant features of visual stimuli. , 1981, Science.

[16]  Joaquin M. Fuster,et al.  Effects of cooling inferotemporal cortex on performance of visual memory tasks , 1981, Experimental Neurology.

[17]  J. A. Horel,et al.  Behavioral effect of local cooling in temporal lobe of monkeys. , 1982, Journal of neurophysiology.

[18]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

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

[20]  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.

[21]  L. Squire,et al.  Preserved learning in monkeys with medial temporal lesions: sparing of motor and cognitive skills , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[23]  M. Mishkin,et al.  Monkeys with combined amygdalo-hippocampal lesions succeed in object discrimination learning despite 24-hour intertrial intervals. , 1984, Behavioral neuroscience.

[24]  J Allman,et al.  Direction- and Velocity-Specific Responses from beyond the Classical Receptive Field in the Middle Temporal Visual Area (MT) , 1985, Perception.

[25]  Leslie G. Ungerleider,et al.  Contour, color and shape analysis beyond the striate cortex , 1985, Vision Research.

[26]  J. Fuster,et al.  Functional interactions between inferotemporal and prefrontal cortex in a cognitive task , 1985, Brain Research.

[27]  L. Squire,et al.  Medial temporal lesions in monkeys impair memory on a variety of tasks sensitive to human amnesia. , 1985, Behavioral neuroscience.

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

[29]  D. Amaral,et al.  The entorhinal cortex of the monkey: II. Cortical afferents , 1987, The Journal of comparative neurology.

[30]  D. Amaral,et al.  The entorhinal cortex of the monkey: III. Subcortical afferents , 1987, The Journal of comparative neurology.

[31]  I. Ohzawa,et al.  Visual orientation and spatial frequency discrimination: a comparison of single neurons and behavior. , 1987, Journal of neurophysiology.

[32]  I. Ohzawa,et al.  The effects of contrast on visual orientation and spatial frequency discrimination: a comparison of single cells and behavior. , 1987, Journal of neurophysiology.

[33]  L. Optican,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. III. Information theoretic analysis. , 1987, Journal of neurophysiology.

[34]  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.

[35]  D. Amaral,et al.  The entorhinal cortex of the monkey: I. Cytoarchitectonic organization , 1987, The Journal of comparative neurology.

[36]  B J Richmond,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. II. Quantification of response waveform. , 1987, Journal of neurophysiology.

[37]  Stephen Grossberg,et al.  A massively parallel architecture for a self-organizing neural pattern recognition machine , 1988, Comput. Vis. Graph. Image Process..

[38]  J. A. Horel,et al.  The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold , 1987, Behavioural Brain Research.

[39]  Teuvo Kohonen,et al.  Self-Organization and Associative Memory , 1988 .

[40]  Y. Miyashita,et al.  Neuronal correlate of pictorial short-term memory in the primate temporal cortexYasushi Miyashita , 1988, Nature.

[41]  G. Orban,et al.  How well do response changes of striate neurons signal differences in orientation: a study in the discriminating monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  J. Fuster Inferotemporal units in selective visual attention and short-term memory. , 1990, Journal of neurophysiology.

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

[44]  J. Maunsell,et al.  Extraretinal representations in area V4 in the macaque monkey , 1991, Visual Neuroscience.

[45]  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.

[46]  S. Nelson,et al.  Temporal interactions in the cat visual system. I. Orientation- selective suppression in the visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  Leslie G. Ungerleider,et al.  Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[49]  I. Riches,et al.  The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gyrus and inferior temporal cortex of the primate , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  F M Miezin,et al.  Activation of the hippocampus in normal humans: a functional anatomical study of memory. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[52]  D. Perrett,et al.  Time course of neural responses discriminating different views of the face and head. , 1992, Journal of neurophysiology.

[53]  E. Murray,et al.  Monkeys (Macaca fascicularis) with rhinal cortex ablations succeed in object discrimination learning despite 24-hr intertrial intervals and fail at matching to sample despite double sample presentations. , 1992, Behavioral neuroscience.

[54]  L. Optican,et al.  Role of inferior temporal neurons in visual memory. I. Temporal encoding of information about visual images, recalled images, and behavioral context. , 1992, Journal of neurophysiology.

[55]  J. A. Horel,et al.  Cortical afferents to behaviorally defined regions of the inferior temporal and parahippocampal gyri as demonstrated by WGA‐HRP , 1992, The Journal of comparative neurology.

[56]  E. Murray Medial temporal lobe structures contributing to recognition memory: The amygdaloid complex versus the rhinal cortex. , 1992 .

[57]  D. Amaral,et al.  Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  L. Squire,et al.  Damage to the perirhinal cortex exacerbates memory impairment following lesions to the hippocampal formation , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.