A deficit in discriminating gaze direction in a case with right superior temporal gyrus lesion

Abstract

The superior temporal sulcus (STS) region is well recognized as being heavily involved in detecting and discriminating gaze. Lesions confined to this area are quite rare in humans, and so the research has mainly depended on animal studies and functional neuroimaging in normal human subjects. We report one such rare case, a 54-year-old Japanese female with a possible congenital s anomaly who, after a cerebral hemorrhage, demonstrated a lesion almost completely confined to the entire right superior temporal gyrus (STG). In the subacute phase, the patient showed evidence of left hemispatial neglect, from which she gradually recovered. In the chronic phase, she showed a puzzling difficulty in obtaining eye-contact. We have conducted, in conjunction with conventional neuropsychological evaluations, experimental assessment of her ability in gaze cognition. Her performance on neuropsychological testing demonstrated no compromise in intellect, memory, or language skills, and a close-to-full recovery from neglect. On gaze cognition experiments, she was repeatedly shown to perceive left gaze as straight, and to a lesser degree, straight gaze as right. We suggest that the function of the STG in detecting gaze, together with the directional information it receives from earlier visual areas, may be associated, when damaged, with this deficit in detecting contra-directional gaze. We have demonstrated for the first time that a single circumscribed lesion to the STG results in both gaze processing deficit and concurrent aberrant gaze behavior of the victim herself, implicating a mechanism within the STG as an interface between gaze of others and gaze of self.

Introduction

The superior temporal sulcus (STS) has attracted much interest due to its intriguing function as a detector of biological motion. Since the 1980s, single-cell studies in monkey brains have shown that a number of neurons in the STS region show preference in the direction of head and gaze when viewing faces of conspecifics and humans, so that some neurons respond maximally to straight gaze while others respond more to averted gaze (Perrett, Hietanen, Oram, & Benson, 1992). Investigations of STS-lesioned monkeys showed disrupted gaze discrimination after lesioning (Campbell, Heywood, Cowey, Regard, & Landis, 1990; Eacott, Heywood, Gross, & Cowey, 1993), more or less supporting the findings from single-cell studies. Research of the STS in humans has found a homologous function; gaze as well as head direction, movement of mouth and hands, body gestures, geometric figures simulating biological motion have all been shown to activate the STS in functional imaging studies and electrophysiological studies (see Allison, Puce, & McCarthy, 2000; Puce & Perrett, 2003 for review). Thus, the function of the STS in humans can be summarized as the detection of biological motion, which composes a major contribution to social perception.

Gaze, in particular, is undoubtedly special, perhaps without a match in its significance as a biological signal. There are suggestions for the innateness of gaze cognition, in that newborns show a preference for faces with eyes open versus eyes closed (Batki, Baron-Cohen, Wheelwright, Connellan, & Ahluwalia, 2000), and that infants as early as 10 weeks of age follow the gaze of others (Hood, Willen, & Driver, 1998). Moreover, children as young as 4–5 years of age show much more organized ERPs (N190) to eyes compared to full faces (Taylor, Edmonds, McCarthy, & Allison, 2001a), implicating a system within the human brain which is dedicated, at least in part, to gaze cognition. Such a system has been suggested to be localized in the posterior region of the STS in question, particularly in the right hemisphere: In a PET study, faces with visible gaze compared with obscured gaze, was shown to differentially activate the STS (Wicker, Michel, Henaff, & Decety, 1998). Gaze processing, such as perception of apparent eye motion (Puce, Allison, Bentin, Gore, & McCarthy, 1998) and detection of gaze direction (Hoffman & Haxby, 2000), has also been demonstrated to elicit significant STS activation in fMRI studies. ERP studies have shown that N170 from the posterior temporal region is also sensitive to gaze (Puce, Smith, & Allison, 2000; Taylor, Itier, Allison, & Edmonds, 2001b).

Intriguing as it may be, however, the function of the STS in humans remains tentative in that most studies are based on functional findings of the intact brain. Neuropsychological studies of human cases with circumscribed STS lesions might be more conclusive, and would afford a wealth of insight into these issues. Since left STS damage would leave most humans aphasic with little understanding of any verbal input, study of a patient with right STS damage is likely to be more informative. To date, and to our knowledge, such a neuropsychological case has never been reported. In this paper, we report one such case, who, after a cerebrovascular accident, presented a very rare circumscribed lesion almost confined to the entire right superior temporal gyrus (STG), which constitutes the upper bank of the STS. The rarity of this lesion might have partly been due to a co-existing cerebrovascular anomaly in this patient. One of the most striking features of the sequelae in this patient was the inability to engage in mutual eye-contact. Given the functional data suggesting STS involvement in gaze cognition, a quantitative evaluation of the patient's gaze processing would offer the first neuropsychological data for the STS and its suggested role in gaze cognition. We have therefore conducted, in addition to conventional neuropsychological assessments, some behavioral experiments in gaze processing which revealed a unique impairment in gaze cognition.