Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex.

1. To analyze the selectivity and the sparseness of firing to visual stimuli of single neurons in the primate temporal cortical visual area, neuronal responses were measured to a set of 68 visual stimuli in macaques performing a visual fixation task. The population of neurons analyzed had responses that occurred primarily to faces. The stimuli included 23 faces, and 45 nonface images of real-world scenes, so that the function of this brain region could be analyzed when it was processing natural scenes. 2. The neurons were selected to meet the previously used criteria of face selectivity by responding more than twice as much to the optimal face as to the optimal nonface stimulus in the set. Application of information theoretic analyses to the responses of these neurons confirmed that their responses contained much more information about which of 20 face stimuli had been seen (on average 0.4 bits) than about which (of 20) nonface stimuli had been seen (on average 0.07 bits). 3. The sparseness of the representation of a scene or object provided by each of these neurons (which can be thought of as the proportion of stimuli to which the neuron responds, and which is fundamental to understanding the network operation of the system) can be defined as [formula: see text] where ri is the firing rate to the ith stimulus in the set of n stimuli. The sparseness has a maximal value of 1.0. It was found that the sparseness of the representation of the 68 stimuli by each neuron had an average across all neurons of 0.65. This indicates a rather distributed representation. 4. If the spontaneous firing rate was subtracted from the firing rate of the neuron to each stimulus, so that the changes of firing rate, i.e., the responses of the neurons, were used in the sparseness calculation, then the "response sparseness" had a lower value, with a mean of 0.33 for the population of neurons, or 0.60 if calculated over the set of faces. 5. Multidimensional scaling to produce a stimulus space represented by this population of neurons showed that the different faces were well separated in the space created, whereas the different nonface stimuli were grouped together in the space. 6. The information analyses and multidimensional scaling provided evidence that what was made explicit in the responses of these neurons was information about which face had been seen.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  Treves,et al.  Graded-response neurons and information encodings in autoassociative memories. , 1990, Physical review. A, Atomic, molecular, and optical physics.

[2]  D. Pandya,et al.  Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey , 1978, Brain Research.

[3]  E. T. Rolls,et al.  Hypothalamic neuronal responses associated with the sight of food , 1976, Brain Research.

[4]  Rolls Et Neurons in the cortex of the temporal lobe and in the amygdala of the monkey with responses selective for faces. , 1984 .

[5]  M. Tovée,et al.  Processing speed in the cerebral cortex and the neurophysiology of visual masking , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  Stefano Panzeri,et al.  The Upward Bias in Measures of Information Derived from Limited Data Samples , 1995, Neural Computation.

[7]  Terrence J. Sejnowski,et al.  The Computational Brain , 1996, Artif. Intell..

[8]  D. Perrett,et al.  Brain mechanisms of perception and memory : from neuron to behavior , 1993 .

[9]  A. Berthoz,et al.  Neurons responding to whole-body motion in the primate hippocampus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  E. Rolls,et al.  Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. , 1990, Journal of neurophysiology.

[11]  Joseph B. Travers,et al.  A metric for the breadth of tuning of gustatory neurons , 1979 .

[12]  R. Desimone Face-Selective Cells in the Temporal Cortex of Monkeys , 1991, Journal of Cognitive Neuroscience.

[13]  Edmund T. Rolls,et al.  What determines the capacity of autoassociative memories in the brain? Network , 1991 .

[14]  Y. Miyashita,et al.  Hippocampal neurons in the monkey with activity related to the place in which a stimulus is shown , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  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.

[16]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[17]  Edmund T. Rolls,et al.  The relative advantages of sparse versus distributed encoding for associative neuronal networks in the brain , 1990 .

[18]  E. Rolls Neural organization of higher visual functions , 1991, Current Opinion in Neurobiology.

[19]  E. Rolls Learning mechanisms in the temporal lobe visual cortex , 1995, Behavioural Brain Research.

[20]  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.

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

[22]  E. Rolls,et al.  Computational analysis of the role of the hippocampus in memory , 1994, Hippocampus.

[23]  E. Rolls,et al.  Functional subdivisions of the temporal lobe neocortex , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  M. Tovée,et al.  Information encoding in short firing rate epochs by single neurons in the primate temporal visual cortex , 1995 .

[25]  E. Rolls,et al.  Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey , 1985, Brain Research.

[26]  John H. R. Maunsell,et al.  Visual processing in monkey extrastriate cortex. , 1987, Annual review of neuroscience.

[27]  B. McNaughton,et al.  Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. , 1990, Progress in brain research.

[28]  B. McNaughton,et al.  Spatial selectivity of unit activity in the hippocampal granular layer , 1993, Hippocampus.

[29]  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.

[30]  E. Rolls Brain mechanisms for invariant visual recognition and learning , 1994, Behavioural Processes.

[31]  E. T. Rolls,et al.  Responses of hippocampal formation neurons in the monkey related to delayed spatial response and object-place memory tasks , 1989, Behavioural Brain Research.

[32]  N Suga,et al.  Principles of auditory information-processing derived from neuroethology. , 1989, The Journal of experimental biology.

[33]  Bruce L. McNaughton,et al.  Spatial representation in the rat: Conceptual, behavioral, and neurophysiological perspectives , 1990 .

[34]  E T Rolls,et al.  Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network , 1992, Hippocampus.

[35]  A. W. Macrae,et al.  On calculating unbiased information measures. , 1971 .

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

[37]  Edmund T. Rolls,et al.  Neurophysiology and functions of the primate amygdala. , 1992 .

[38]  E. Rolls Functions of neuronal networks in the hippocampus and neocortex in memory , 1989 .

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

[40]  M. Tovée,et al.  Translation invariance in the responses to faces of single neurons in the temporal visual cortical areas of the alert macaque. , 1994, Journal of neurophysiology.

[41]  L. Weiskrantz,et al.  Impairments of visual object transforms in monkeys. , 1984, Brain : a journal of neurology.

[42]  M. Young,et al.  Sparse population coding of faces in the inferotemporal cortex. , 1992, Science.

[43]  Keinosuke Fukunaga,et al.  Introduction to Statistical Pattern Recognition , 1972 .

[44]  E. Rolls Neurons in the cortex of the temporal lobe and in the amygdala of the monkey with responses selective for faces. , 1984, Human neurobiology.

[45]  R. Desimone,et al.  Inferior Temporal Cortex and Pattern Recognition , 1985 .

[46]  Geoffrey E. Hinton,et al.  Distributed Representations , 1986, The Philosophy of Artificial Intelligence.

[47]  H B Barlow,et al.  Single units and sensation: a neuron doctrine for perceptual psychology? , 1972, Perception.

[48]  M. Tovée,et al.  Information encoding and the responses of single neurons in the primate temporal visual cortex. , 1993, Journal of neurophysiology.

[49]  E T Rolls,et al.  Neurophysiological mechanisms underlying face processing within and beyond the temporal cortical visual areas. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.