Visual neurones responsive to faces in the monkey temporal cortex

SummaryOf 497 single neurones recorded in the cortex in the fundus of the superior temporal sulcus (STS) of three alert rhesus monkeys, a population of at least 48 cells which were selectively responsive to faces had the following response properties: (1) The cells' responses to faces (real or projected, human or rhesus monkey) were two to ten times as large as those to gratings, simple geometrical stimuli or complex 3-D objects. (2) Neuronal responses to faces were excitatory, sustained and were time-locked to the stimulus presentation with a latency of between 80 and 160 ms. (3) The cells were unresponsive to auditory or tactile stimuli and to the sight of arousing or aversive stimuli. (4) The magnitude of the responses of 28 cells tested was relatively constant despite transformations, such as rotation, so that the face was inverted or horizontal, and alterations of colour, size or distance. (5) Rotation to profile substantially reduced the responses of 21 cells (31 tested). (6) Masking out or presenting parts of the face (i.e. eyes, mouth or hair) in isolation revealed that different cells responded to different features or subsets of features. (7) For several cells, responses to the normal organisation of cut-out or line-drawn facial features were significantly larger than to jumbled controls. These findings indicate that explanations in terms of arousal, emotional or motor reactions, simple visual feature sensitivity or receptive fields are insufficient to account for the selective responses to faces and face features observed in this population of STS neurones. It appears that these neurones are part of a system specialised to code for faces or features present in faces, and it is suggested that damage to this system is related to prosopagnosia, or difficulty in face recognition, in man and to the tameness and social disturbances which follow temporal lobe damage and are part of the Klüver-Bucy syndrome in the monkey.

[1]  H. Klüver,et al.  PRELIMINARY ANALYSIS OF FUNCTIONS OF THE TEMPORAL LOBES IN MONKEYS , 1939 .

[2]  G. Kimble.  Conditioning as a function of the time between conditioned and unconditioned stimuli. , 1947, Journal of experimental psychology.

[3]  G. Bonin,et al.  The neocortex of Macaca mulatta , 1947 .

[4]  G. J. Romanes,et al.  The Neocortex of Macaca mulatta , 1948 .

[5]  G. Sackett.  Monkeys Reared in Isolation with Pictures as Visual Input: Evidence for an Innate Releasing Mechanism , 1966, Science.

[6]  R. Coss.  The Ethological Command in Art , 1968 .

[7]  R. Yin.  Looking at Upside-down Faces , 1969 .

[8]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

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

[10]  J. C. Meadows.  The anatomical basis of prosopagnosia , 1974, Journal of neurology, neurosurgery, and psychiatry.

[11]  J. A. Horel,et al.  Partial Klu¨ver-Bucy syndrome produced by destroying temporal neocortex or amygdala , 1975, Brain Research.

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

[13]  H. Burton,et al.  The posterior thalamic region and its cortical projection in new world and old world monkeys , 1976, The Journal of comparative neurology.

[14]  M. Scaife,et al.  The response to eye-like shapes by birds II. The importance of staring, pairedness and shape , 1976, Animal Behaviour.

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

[16]  H. D. Steklis,et al.  A neural substrate for affiliative behavior in nonhuman primates. , 1976, Brain, behavior and evolution.

[17]  E. T. Rolls,et al.  Activity of neurones in the inferotemporal cortex of the alert monkey , 1977, Brain Research.

[18]  E. Warrington,et al.  Prosopagnosia: a clinical, psychological, and anatomical study of three patients. , 1977, Journal of neurology, neurosurgery, and psychiatry.

[19]  John Q. Trojanowski,et al.  Prefrontal granular cortex of the rhesus monkey. I. Intrahemispheric cortical afferents , 1977, Brain Research.

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

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

[22]  E. Rolls,et al.  The latency of activation of neurones in the lateral hypothalamus and substantia innominata during feeding in the monkey , 1979, Brain Research.

[23]  E. Rolls,et al.  Visual responses of neurons in the dorsolateral amygdala of the alert monkey , 1979, Experimental Neurology.

[24]  Giacomo Rizzolatti,et al.  Neurons responding to visual stimuli in the frontal lobe of macaque monkeys , 1979, Neuroscience Letters.

[25]  A. Cowey.  Cortical Maps and Visual Perception the Grindley Memorial Lecture* , 1979, The Quarterly journal of experimental psychology.

[26]  G. V. Hoesen,et al.  Face recognition in the rhesus monkey , 1979, Neuropsychologia.

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

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

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

[30]  Taniguchi Kōgyō Shōreikai,et al.  Brain mechanisms of sensation , 1981 .

[31]  L. Leinonen,et al.  II. Functional properties of cells in anterolateral part of area 7 associative face area of awake monkeys , 1979, Experimental Brain Research.