A model for experience-dependent changes in the responses of inferotemporal neurons

Neurons in inferior temporal (IT) cortex exhibit selectivity for complex visual stimuli and can maintain activity during the delay following the presentation of a stimulus in delayed match to sample tasks. Experimental work in awake monkeys has shown that the responses of IT neurons decline during presentation of stimuli which have been seen recently (within the past few seconds). In addition, experiments have found that the responses of IT neurons to visual stimuli also decline as the stimuli become familiar, independent of recency. Here a biologically based neural network simulation is used to model these effects primarily through two processes. The recency effects are caused by adaptation due to a calcium-dependent potassium current, and the familiarity effects are caused by competitive self-organization of modifiable feedforward synapses terminating on IT cortex neurons.

[1]  W. Nauta,et al.  Subcortical projections from the temporal neocortex in Macaca mulatta , 1956 .

[2]  D. B. Bender,et al.  Visual Receptive Fields of Neurons in Inferotemporal Cortex of the Monkey , 1969, Science.

[3]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[4]  M Mishkin,et al.  An analysis of short-term visual memory in the monkey. , 1975, Journal of experimental psychology. Animal behavior processes.

[5]  J. Delacour [Inferotemporal cortex and short term visual memory in monkeys. New data]. , 1977, Experimental brain research.

[6]  Roman Bek,et al.  Discourse on one way in which a quantum-mechanics language on the classical logical base can be built up , 1978, Kybernetika.

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

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

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

[10]  J M Fuster,et al.  Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  A. Sillito,et al.  Cholinergic modulation of the functional organization of the cat visual cortex , 1983, Brain Research.

[12]  M. Mesulam,et al.  Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1–Ch6) , 1983, Neuroscience.

[13]  M M Mesulam,et al.  Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. , 1984, Brain : a journal of neurology.

[14]  D. Amaral,et al.  The afferent connections of the substantia innominata in the monkey, Macaca fascicularis , 1985, The Journal of comparative neurology.

[15]  David Zipser,et al.  Feature discovery by competitive learning , 1986 .

[16]  P. Adams,et al.  Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. , 1986, Journal of neurophysiology.

[17]  James L. McClelland,et al.  Parallel distributed processing: explorations in the microstructure of cognition, vol. 1: foundations , 1986 .

[18]  M. W. Brown,et al.  Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory , 1987, Brain Research.

[19]  C. Woody,et al.  Acetylcholine reduces net outward currents measured in vivo with single electrode voltage clamp techniques in neurons of the motor cortex of cats , 1987, Brain Research.

[20]  B. Lancaster,et al.  Potassium currents evoked by brief depolarizations in bull‐frog sympathetic ganglion cells. , 1987, The Journal of physiology.

[21]  D. McCormick,et al.  Post‐natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. , 1987, The Journal of physiology.

[22]  P. Schwindt,et al.  Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. , 1988, Journal of neurophysiology.

[23]  H. Wigström,et al.  Physiological mechanisms underlying long-term potentiation , 1988, Trends in Neurosciences.

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

[25]  Edmund T. Rolls,et al.  The role responses of expression and identity in the face-selective of neurons in the temporal visual cortex of the monkey , 1989 .

[26]  T. Sejnowski,et al.  Associative long-term depression in the hippocampus induced by hebbian covariance , 1989, Nature.

[27]  W. Levy A computational approach to hippocampal function , 1989 .

[28]  M. Hasselmo,et al.  The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey , 1989, Behavioural Brain Research.

[29]  N. Weinberger,et al.  Acetylcholine produces stimulus-specific receptive field alterations in cat auditory cortex , 1989, Brain Research.

[30]  N. Weinberger,et al.  Acetylcholine modifies neuronal acoustic rate‐level functions in guinea pig auditory cortex by an muscarinic receptors , 1990, Synapse.

[31]  Robert D. Blitzer,et al.  Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus , 1990, Neuroscience Letters.

[32]  N. Weinberger,et al.  Acetylcholine modifies neuronal acoustic rate‐level functions in guinea pig auditory cortex by an muscarinic receptors , 1990 .

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

[34]  J. Sarvey,et al.  Muscarinic receptor activation facilitates the induction of long-term potentiation (LTP) in the rat dentate gyrus , 1990, Neuroscience Letters.

[35]  R. Dykes,et al.  Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. II. Cortical neurons excited by somatic stimuli. , 1990, Journal of neurophysiology.

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

[37]  M. Delong,et al.  Functional Implications of Tonic and Phasic Activity Changes in Nucleus Basalis Neurons , 1991 .

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

[39]  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.

[40]  W A Press,et al.  Long-term potentiation in slices of kitten visual cortex and the effects of NMDA receptor blockade. , 1992, Journal of neurophysiology.

[41]  T. A. Pitler,et al.  Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. , 1992, The Journal of physiology.

[42]  M. Hasselmo,et al.  Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex. , 1992, Journal of neurophysiology.

[43]  P. Schwindt,et al.  Calcium-dependent potassium currents in neurons from cat sensorimotor cortex. , 1992, Journal of neurophysiology.

[44]  R. Desimone,et al.  Activity of neurons in anterior inferior temporal cortex during a short- term memory task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  S. Grossberg,et al.  Normal and amnesic learning, recognition and memory by a neural model of cortico-hippocampal interactions , 1993, Trends in Neurosciences.

[46]  R. Desimone,et al.  Scopolamine affects short-term memory but not inferior temporal neurons. , 1993, Neuroreport.

[47]  R. Desimone,et al.  The representation of stimulus familiarity in anterior inferior temporal cortex. , 1993, Journal of neurophysiology.

[48]  D. Zipser,et al.  A spiking network model of short-term active memory , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  L. Cauller,et al.  Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  R. Desimone,et al.  Parallel neuronal mechanisms for short-term memory. , 1994, Science.

[51]  Earl K. Miller,et al.  The interaction of neural systems for attention and memory , 1994 .

[52]  M. Hasselmo,et al.  Modulation of the input/output function of rat piriform cortex pyramidal cells. , 1994, Journal of neurophysiology.

[53]  M. Hasselmo,et al.  Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3 , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  M. Hasselmo,et al.  Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  J. R. Baker,et al.  The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Nicolas Brunel,et al.  Hebbian Learning of Context in Recurrent Neural Networks , 1996, Neural Computation.

[57]  M. Hasselmo,et al.  Suppression of synaptic transmission may allow combination of associative feedback and self-organizing feedforward connections in the neocortex , 1996, Behavioural Brain Research.

[58]  B. Connors,et al.  Differential Regulation of Neocortical Synapses by Neuromodulators and Activity , 1997, Neuron.

[59]  R. Dykes,et al.  Mechanisms controlling neuronal plasticity in somatosensory cortex. , 1997, Canadian journal of physiology and pharmacology.

[60]  G. Wallis,et al.  Spatio-temporal influences at the neural level of object recognition. , 1998, Network.

[61]  G. Wallis Spatio-temporal influences at the neural level of object recognition , 1998 .

[62]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[63]  D J Amit What is and what is not a theory of context correlations. , 1999, Network.