Separate Coding of Different Gaze Directions in the Superior Temporal Sulcus and Inferior Parietal Lobule

Electrophysiological recording in the anterior superior temporal sulcus (STS) of monkeys has demonstrated separate cell populations responsive to direct and averted gaze 1Perrett D.I. Smith P.A.J. Potter D.D. Mistlin A.J. Head A.S. Milner A.D. Jeeves M.A. Visual cells in the temporal cortex sensitive to face view and gaze direction.Proc. R. Soc. Lond. B. Biol. Sci. 1985; B223: 293-317Crossref Scopus (729) Google Scholar, 2Perrett D.I. Hietanen J.K. Oram M.W. Benson P.J. Organization and functions of cells responsive to faces in the temporal cortex.Philos. Trans. R. Soc. Lond. B Biol. Sci. 1992; B335: 23-30Crossref Scopus (674) Google Scholar. Human functional imaging has demonstrated posterior STS activation in gaze processing, particularly in coding the intentions conveyed by gaze 3Hoffman E.A. Haxby J.V. Distinct representations of eye gaze and identity in the distributed human neural system for face perception.Nat. Neurosci. 2000; 3: 80-84Crossref PubMed Scopus (975) Google Scholar, 4Puce A. Allison T. Bentin S. Gore J.C. McCarthy G. Temporal cortex activation in humans viewing eye and mouth movements.J. Neurosci. 1998; 18: 2188-2199PubMed Google Scholar, 5Pelphrey K.A. Morris J.P. McCarthy G. Neural basis of eye gaze processing deficits in autism.Brain. 2005; 128: 1038-1048Crossref PubMed Scopus (324) Google Scholar, 6Pelphrey K.A. Viola R.J. McCarthy G. When strangers pass: Processing of mutual and averted gaze in the superior temporal sulcus.Psychol. Sci. 2004; 15: 598-603Crossref PubMed Scopus (278) Google Scholar, but to date has provided no evidence of dissociable coding of different gaze directions. Because the spatial resolution typical of group-based fMRI studies (∼6–10 mm) exceeds the size of cellular patches sensitive to different facial characteristics (1–4 mm in monkeys), a more sensitive technique may be required. We therefore used fMRI adaptation, which is considered to offer superior resolution 7Grill-Spector K. Kushnir T. Edelman S. Avidan G. Itzchak Y. Malach R. Differential processing of objects under different viewing conditions in the human lateral occipital complex.Neuron. 1999; 24: 187-203Abstract Full Text Full Text PDF PubMed Scopus (975) Google Scholar, to investigate whether the human anterior STS contains representations of different gaze directions, as suggested by non-human primate research. Subjects viewed probe faces gazing left, directly ahead, or right. Adapting to leftward gaze produced a reduction in BOLD response to left relative to right (and direct) gaze probes in the anterior STS and inferior parietal cortex; rightward gaze adaptation produced a corresponding reduction to right gaze probes. Consistent with these findings, averted gaze in the adapted direction was misidentified as direct. Our study provides the first human evidence of dissociable neural systems for left and right gaze.