Visual neurones responsive to faces in the monkey temporal cortex (original) (raw)
Summary
Of 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.
Access this article
Subscribe and save
- Get 10 units per month
- Download Article/Chapter or eBook
- 1 Unit = 1 Article or 1 Chapter
- Cancel anytime Subscribe now
Buy Now
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
Instant access to the full article PDF.
Similar content being viewed by others
References
- Aggleton JP, Burton MJ, Passingham RE (1980) Cortical and subcortical afferents to the amygdala in the rhesus monkey (Macaca mulatta). Brain Res 190: 347–368
Google Scholar - Bonin G von, Bailey P (1947) The neocortex of Macaca mulatta. University of Illinois Press, Urbana
Google Scholar - Bruce CJ, Desimone R, Gross CG (1977) Large receptive fields in a polysensory area in the superior temporal sulcus of the macaque. Soc Neurosci Abstr 3: 1756
Google Scholar - Bruce CJ, Desimone R, Gross CG (1981) Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J Neurophysiol 46: 369–384
CAS PubMed Google Scholar - Burton H, Jones EG (1976) The posterior thalamic region and its cortical projection in new world and old world monkeys. J Comp Neurol 168: 249–302
Google Scholar - Coss RG (1968) The ethological command in art. Int J Contemp Artist 1: 273–287
Google Scholar - Cowey A (1979) Cortical maps and visual perception. J Exp Psychol 37: 1–17
Google Scholar - Damasio AR, Damasio H, Van Hoesen GW (1982) Prosopagnosia: Anatomical basis and neurobehavioral mechanism. Neurology Minneap (in press)
- Desimone R, Gross CG (1979) Visual areas in the temporal cortex of the macaque. Brain Res 178: 393–380
Google Scholar - Goren C, Sarty M, Wu P (1975) Visual following and pattern discrimination of face-like stimuli by newborn infants. Pediatrics 56: 544–549
Google Scholar - Gross CG, Rocha-Miranda CE, Bender DB (1972) Visual properties of neurons in inferotemporal cortex of the macaque. J Neurophysiol 35: 96–111
Google Scholar - Hinde RA, Rowell TE (1962) Comminication by postures and facial expression in the rhesus monkey (Macaca mulatta). Proc Zoo Soc (Lond) 138: 1–21
Google Scholar - Horel JA, Keating EG, Misantone LG (1975) Partial Klüver-Bucy syndrome produced by destroying neocortex or amygdala. Brain Res 94: 347–359
Google Scholar - Jones EG, Powell TPS (1970) An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93: 793–820
CAS PubMed Google Scholar - Jacobsen S, Trojanowski JQ (1977) Pre-frontal granular cortex of the rhesus monkey. I. Intrahemispheric cortical afferents. Brain Res 132: 209–233
Google Scholar - Kling A, Steklis HD (1976) A neural substrate for affiliative behavior in nonhuman primates. Brain Behav Evol 13: 216–238
Google Scholar - Klüver H, Bucy PC (1939) Preliminary analysis of functions of the temporal lobes in monkeys. Arch Neurol Psychiatr 42: 979–1000
Google Scholar - Leinonen L, Nyman G (1979) Functional properties of cells in antero-lateral part of area 7 associative face area of awake monkeys. Exp Brain Res 34: 321–333
Google Scholar - Meadows JC (1974) The anatomical basis of Prosopagnosia. J Neurol Neurosurg Psychiatry 37: 489–501
Google Scholar - Meltzoff AN, Moore MK (1977) Imitation of facial and manual gestures by human neonates. Science 198: 75–78
Google Scholar - Perrett DI, Rolls ET, Caan W (1979) Temporal lobe cells of the monkey with visual responses selective for faces. Neurosci Lett [supl 3], S358
- Pigarev IN, Rizzolatti G, Scandolara C (1979) Neurones responding to visual stimuli in the frontal lobe of macaque monkeys. Neurosci Lett 12: 207–212
Google Scholar - Rolls ET (1981a) Processing beyond the inferior temporal visual cortex related to feeding, memory, and striatal function. In: Katsuki Y, Norgren R, Sato M. (eds) Brain mechanisms of sensation. Wiley, New York, pp 241–269
Google Scholar - Rolls ET (1981b) Responses of amygdaloid neurons in the primate. In: Ben-Ari Y (ed) The amygdaloid complex. Elsevier, Amsterdam, pp 383–393
Google Scholar - Rolls ET, Burton MJ, Mora F (1976) Hypothalamic neuronal responses associated with the sight of food. Brain Res 111: 53–66
Google Scholar - Rolls ET, Judge SJ, Sanghera MK (1977) Activity of neurones in the inferotemporal cortex of the alert monkey. Brain Res 130: 229–238
Google Scholar - Rolls ET, Sanghera MK, Roper-Hall A, (1979) The latency of activation of neurones in the lateral hypothalamus and substantia innominata during feeding in the monkey. Brain Res 164: 121–135
Google Scholar - Rosenfeld SA, Van Hoesen GW (1979) Face recognition in the rhesus monkey. Neuropsychologia 17: 503–509
Google Scholar - Sackett GP (1966) Monkeys reared in isolation with pictures as visual input: Evidence for innate releasing mechanism. Science 154: 1470–1473
Google Scholar - Sanghera MK, Rolls ET, Roper-Hall A (1979) Visual responses of neurons in the dorsolateral amygdala of the alert monkey. Exp Neurol 63: 610–626
Google Scholar - Scaife M (1976) Response to eye like shapes by birds. II. The importance of staring, pairedness and shape. Anim Behav 24: 200–206
Google Scholar - Seltzer B, Pandya DN (1978) Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Res 149: 1–24
Google Scholar - Whiteley AM, Warrington EK (1977) Prosopagnosia: A clinical, psychological, and anatomical study of three patients. J Neurol Neurosurg Psychiatry 40: 394–430
Google Scholar - Yin RK (1969) Looking at upside down faces. J Exp Psychol 81: 141–145
Google Scholar
Author information
Author notes
- D. I. Perrett
Present address: The Psychological Laboratory, University of St. Andrews, 16 9JU, St. Andrews, Fife, KY, Scotland
Authors and Affiliations
- Dept. of Experimental Psychology, University of Oxford, Oxford, England
D. I. Perrett, E. T. Rolls & W. Caan
Authors
- D. I. Perrett
You can also search for this author inPubMed Google Scholar - E. T. Rolls
You can also search for this author inPubMed Google Scholar - W. Caan
You can also search for this author inPubMed Google Scholar
Rights and permissions
About this article
Cite this article
Perrett, D.I., Rolls, E.T. & Caan, W. Visual neurones responsive to faces in the monkey temporal cortex.Exp Brain Res 47, 329–342 (1982). https://doi.org/10.1007/BF00239352
- Received: 09 November 1981
- Issue Date: September 1982
- DOI: https://doi.org/10.1007/BF00239352