Social signals analyzed at the single cell level : someone is looking at me, something touched me, something moved!

In the superior temporal sulcus (STS) of the macaque brain there are populations of cells which respond selectively to faces. Studies of these cells reveal that they are very sensitive to the direction of eye gaze and posture of the head of other subjects. It is argued that one function of the cells is to enable analysis of where other individuals are directing their attention. Given this selectivity for complex socially relevant stimuli it is surprising that the STS contains cells that respond to touch anywhere on the body or to any movement seen in the visual environment. We have investigated these tactile and motion sensitive cells to determine their behavioural significance. In the awake, behaving monkey we found that the critical dimension for polymodal coding is whether or not the sensations are expected. Tactile stimulation out of sight cannot be predicted and elicits neuronal responses. By contrast, when the monkey can see and, therefore, predict impending contact, or when the monkey touches a familiar surface in a predictable location, cell responses are reduced or abolished. In an analogous way some cells are unresponsive to the sight of the monkey's own limbs moving but respond to the sight of other moving stimuli. Since unpredictable sensations are often caused by other animals, the STS area appears well suited to defining sensory stimuli that are important in social or predator/prey interactions.

[1]  R. Sperry Neural basis of the spontaneous optokinetic response produced by visual inversion. , 1950, Journal of comparative and physiological psychology.

[2]  Van Hooff,et al.  The Facial Displays of the Catarrhine Monkeys and Apes. , 1967 .

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

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

[5]  Donald M. MacKay,et al.  Visual Stability and Voluntary Eye Movements , 1973 .

[6]  J. Hyvärinen,et al.  Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys. , 1974, Brain : a journal of neurology.

[7]  V. Mountcastle,et al.  Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. , 1975, Journal of neurophysiology.

[8]  V. Mountcastle,et al.  Parietal lobe mechanisms for directed visual attention. , 1977, Journal of neurophysiology.

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

[10]  D. Marr,et al.  Representation and recognition of the spatial organization of three-dimensional shapes , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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

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

[13]  R. Gregory Perceptions as hypotheses. , 1980, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[15]  A. J. Mistlin,et al.  Neurones responsive to faces in the temporal cortex: studies of functional organization, sensitivity to identity and relation to perception. , 1984, Human neurobiology.

[16]  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.

[17]  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.

[18]  A. J. Mistlin,et al.  Visual analysis of body movements by neurones in the temporal cortex of the macaque monkey: A preliminary report , 1985, Behavioural Brain Research.

[19]  Hans Wallach,et al.  Perceiving a Stable Environment , 1985 .

[20]  J. Feldman Four frames suffice: A provisional model of vision and space , 1985, Behavioral and Brain Sciences.

[21]  A. J. Mistlin,et al.  Visual cells in the temporal cortex sensitive to face view and gaze direction , 1985, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[22]  Somatosensory and associated visual properties of neurones in a polysensory region of macaque temporal cortex: A preliminary study , 1986, Behavioural Brain Research.

[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]  Keiji Tanaka,et al.  Polysensory properties of neurons in the anterior bank of the caudal superior temporal sulcus of the macaque monkey. , 1988, Journal of neurophysiology.

[25]  D I Perrett,et al.  Characteristic Views and the Visual Inspection of Simple Faceted and Smooth Objects: ‘Tetrahedra and Potatoes’ , 1988, Perception.

[26]  A. J. Mistlin,et al.  Specialized face processing and hemispheric asymmetry in man and monkey: Evidence from single unit and reaction time studies , 1988, Behavioural Brain Research.

[27]  D I Perrett,et al.  Frameworks of analysis for the neural representation of animate objects and actions. , 1989, The Journal of experimental biology.

[28]  C. Bell,et al.  Sensory coding and corollary discharge effects in mormyrid electric fish. , 1989, The Journal of experimental biology.

[29]  M. Harries,et al.  Visual Processing of Faces in Temporal Cortex: Physiological Evidence for a Modular Organization and Possible Anatomical Correlates , 1991, Journal of Cognitive Neuroscience.

[30]  M. Argyle,et al.  Gaze and Mutual Gaze , 1994, British Journal of Psychiatry.