Gaze but not arrows: A dissociative impairment after right superior temporal gyrus damage

https://doi.org/10.1016/j.neuropsychologia.2006.03.007Get rights and content

Abstract

Superior temporal sulcus (STS) activation has consistently been demonstrated in the normal brain when viewing eyes, and thus this area is implicated as a gaze processing region in humans. In a recent report, we have presented a case, M.J., with a well-circumscribed lesion to the right superior temporal gyrus (STG), who demonstrated impaired discrimination of gaze direction. In the aim to make distinct whether this impairment is unique to gaze, we have applied a spatial cueing paradigm established by Kingstone and colleagues. In our experiment, pictorial gaze and symmetrical arrows were centrally presented as non-predictive, spatial cues in detecting peripheral targets. Fifteen normal subjects and M.J. participated in the experiment. In concordance with previous reports, controls demonstrated a significant facilitation of reaction times in detecting targets cued by congruent gaze/arrows, compared with incongruent cues. In striking contrast, M.J. showed no such congruency advantage for gaze, in the face of a normal congruency advantage for arrows. We have demonstrated that a circumscribed lesion to the right STG impairs the ability to utilize biological directional information such as gaze, but leaves the non-biological counterpart (arrows) intact. This dissociation implies that indeed, the STS specializes in processing gaze.

Introduction

Gaze understanding and interaction are perhaps essential in making humans the uniquely social beings that we are. Its cognition is one of the most primitive of a variety of biological motion, since the motor intention of others can be inferred from their gaze. There are even 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). The behavior of humans toward gaze has recently been enthusiastically studied by applying a spatial cueing paradigm first introduced by Posner (1980), and renewed by Kingstone and colleagues (Friesen & Kingstone, 1998). In their elegant experiments, central schematic gaze is used as a cue to orient attention in that direction. Normally, subjects shift attention in the direction indicated by the cue gaze, which is reflected as faster reaction times (RTs) in detecting targets presented congruently to the gaze direction, opposed to incongruently presented targets (‘gaze effect’). The tremendousness of the impact that gaze displays on attention is easily imagined when subjects are explicitly instructed to attend opposite to gaze direction in counter-predictive conditions, but simply just cannot, at shorter (300 ms) cue-target intervals (Driver et al., 1999). It takes much longer intervals, in this case 700 ms, to strategically inhibit this automatic orientation triggered by gaze direction.

An interesting non-biological counterpart to gaze is an arrow sign, which has a directional property just like gaze, but no biological significance. When arrows are used as cues in the same experimental paradigm, normal subjects behave more or less in the same manner as to gaze (Tipples, 2002); faster reaction when targets appear congruent to arrows, slower when incongruent (‘arrow effect’). Subtle but profound differences lie between gaze and arrows, however, with closer scrutiny, or when specific patient groups are tested. Normal subjects have been demonstrated to overcome cue-target conflicts for counter-predictive arrows with more ease than for counter-predictive gaze (Friesen, Ristic, & Kingstone, 2004). Autistic spectrum patients, whose lack of reciprocal gaze interaction is one of the cardinal manifestations, have been reported to demonstrate a behavior pattern different to that of normal controls; they have a harder time overcoming cue-target conflicts for counter-predictive arrows than for counter-predictive gaze (Senju, Tojo, Dairoku, & Hasegawa, 2004). A split-brain subject who demonstrated dissociative gaze effect between hemispheres of target presentation (Kingstone, Friesen, & Gazzaniga, 2000), showed no hemispheric dissociation for arrow effect (Ristic, Friesen, & Kingstone, 2002). These findings implicate that although the behavior towards gaze and arrows normally appear quite similar, the neural ground for processing them might be different.

The brain region that is implicated in gaze processing, the superior temporal sulcus (STS), has repeatedly been activated when viewing gaze in the normal brain (Hoffman & Haxby, 2000; Hooker et al., 2003; Kingstone, Tipper, Ristic, & Ngan, 2004; Pelphrey, Singerman, Allison, & McCarthy, 2003; Puce, Allison, Bentin, Gore, & McCarthy, 1998; Puce, Smith, & Allison, 2000; Taylor, Itier, Allison, & Edmonds, 2001; Wicker, Michel, Henaff, & Decety, 1998). This same region has recently been reported to be smaller in two patient groups that are well-documented for the loss of, or for the lack in acquirement of social abilities, namely schizophrenia (Onitsuka et al., 2004; Rajarethinam, Sahni, Rosenberg, & Keshavan, 2004; Rajarethinam, DeQuardo, Nalepa, & Tandon, 2000) and autism (Boddaert et al., 2004; Pelphrey, Morris, & McCarthy, 2005), who are without exception impaired in gaze interaction. We have also presented a case, M.J., in a recent report, with a circumscribed lesion in the right superior temporal gyrus (STG) due to a cerebrovascular accident, who manifested a puzzling difficulty in obtaining eye-contact (Akiyama et al., 2006). As the STG comprises a part of the STS, we investigated her ability in processing gaze in this previous report. Indeed, M.J. demonstrated a unique impairment in discriminating gaze direction, which is the first neuropsychological evidence that establishes the right STS as a gaze processor, so often implicated in animals and human neuroimaging studies.

However, some issues remained to be clarified for M.J. The true significance of gaze as a visual stimulus lies perhaps in its irresistible pull to orient attention toward that same direction, which is undoubtedly a precursor to functions of social cognition such as joint attention. Although M.J. has been demonstrated to show impairment in rote discrimination of gaze direction, it still remains to be seen whether she is able to feel that ‘pull’. Given the difficulty that has been observed for M.J. in understanding the inner thoughts of characters depicted in a one-frame comic situation where gaze direction is essential in reading the line, we hypothesize that she might be hyposensitive to this ‘pull’. The specificity of her impairment to gaze also remains somewhat inconclusive. The misfortune of her hemianopia remains an obstacle, for the contribution of the visual field defect cannot be completely ruled out from M.J.'s gaze discrimination impairment. To address these issues, we have made further investigations by using the spatial cueing paradigm for gaze and arrows. This methodology of comparing behavior toward gaze versus arrows would be an ideal tool for M.J.; it gives us an opportunity to directly compare the impact of biological versus non-biological directional signals under practically the same conditions, while eliminating the constraints of her hemianopia by evaluating responses to targets presented in her intact visual field only. If the STS specializes in processing gaze and its social significance, and not in processing directional signals in general, M.J. should show normal arrow effect, but impaired gaze effect in such a paradigm. In this report, we will show that this is indeed the case.

Section snippets

Subjects

The case subject, M.J., is a 60 year-old dextral female with a circumscribed lesion in the right STG due to a cerebral hemorrhage 5 years ago (Fig. 1). Present neuropsychological status demonstrates no compromise in intellect, and a close-to-full recovery from the neglect syndrome seen earlier. Neurologically, she demonstrates left hemianopia. Her vision for the intact right field was corrected to normal. She has previously been demonstrated to show a gaze processing impairment, where left gaze

Results

Errors, defined as anticipations (RTs < 100 ms), RTs longer than 1000 ms, time-outs (no response), and incorrect responses (pressing a key other than the correct spacebar), were first discarded from further analysis, which eliminated less than 1% of normal data. M.J. performed flawlessly on trials with right targets. The mean RTs, standard deviations, and error rates of all trials for the control group, and of trials with right targets for M.J., are presented in Table 1. M.J. showed significantly

Discussion

In this experiment, we have first confirmed that normal subjects demonstrate faster detection of targets when cued by central gaze or arrows that are directionally congruent with target location, opposed to incongruent or neutral cues, as have been previously reported in a number of studies (Driver et al., 1999; Friesen & Kingstone, 1998; Friesen et al., 2004, Ristic et al., 2002, Tipples, 2002; Zorzi, Mapelli, Rusconi, & Umilta, 2003). This facilitation of RTs in congruent conditions might be

References (35)

  • S.P. Vecera et al.

    What are you looking at? Impaired 'social attention’ following frontal-lobe damage

    Neuropsychologia

    (2004)
  • S.P. Vecera et al.

    Eye gaze does not produce reflexive shifts of attention: Evidence from frontal-lobe damage

    Neuropsychologia

    (2006)
  • B. Wicker et al.

    Brain regions involved in the perception of gaze: A PET study

    Neuroimage

    (1998)
  • I.A. Apperly et al.

    Frontal and temporo-parietal lobe contributions to theory of mind: Neuropsychological evidence from a false-belief task with reduced language and executive demands

    Journal of Cognitive Neuroscience

    (2004)
  • J.J. Barton et al.

    Ocular search during line bisection. The effects of hemi-neglect and hemianopia

    Brain

    (1998)
  • J. Driver et al.

    Gaze perception triggers reflexive visuospatial orienting

    Visual Cognition

    (1999)
  • C.K. Friesen et al.

    The eyes have it! Reflexive orienting is triggered by non-predictive gaze

    Psychonomic Bulletin Review

    (1998)
  • Cited by (92)

    • Gaze-cueing and endogenous attention operate in parallel

      2019, Acta Psychologica
      Citation Excerpt :

      Furthermore, similar to the findings for exogenous cueing, other studies have indicated that there is a double dissociation between endogenous attention and gaze-cueing. For instance, neglect patients have been found to show intact gaze-cueing but disrupted arrow-cueing (Vuilleumier, 2002), while those with schizophrenia and patients with damage to the temporal lobes have specific difficulties with gaze-cueing but show intact arrow-cueing and can orient attention in response to pointing cues (Akiyama et al., 2006, 2008; Dalmaso, Galfano, Tarqui, Forti, & Castelli, 2013 but see also Langdon, Seymour, Williams, & Ward, 2017). Gaze and arrow-cueing tasks also elicit different ERP waveforms (Hietanen, Leppanen, Nummenmaa, & Astikainen, 2008).

    View all citing articles on Scopus
    View full text