Activation of frontoparietal attention networks by non-predictive gaze and arrow cues

Social Cognitive and Affective Neuroscience, Feb 2015

Gaze and arrow cues automatically orient visual attention, even when they have no predictive value, but the neural circuitry by which they direct attention is not clear. Recent evidence has indicated that the ventral frontoparietal attention network is primarily engaged by breaches of a viewer’s cue-related expectations. Accordingly, we hypothesized that to the extent that non-predictive gaze and arrow cues automatically engender expectations with regard to cue location, they should activate the ventral attention network when they cue attention invalidly. Using event-related fMRI, we found that invalid gaze but not arrow cues activated the ventral attention network, specifically in the area of the right temporal parietal junction (TPJ), as well as nodes along the dorsal attention network associated with a redirection of attention to the correct target location. In additional whole-brain analyses, facilitation of behavioral response time by valid gaze cues was linearly associated with the degree of activation in the right TPJ. We conclude from our findings that gaze direction elicits potent expectations in humans with regard to an actor’s intention that engage attention networks if not differently from, at least more robustly than, arrow cues.

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Activation of frontoparietal attention networks by non-predictive gaze and arrow cues

SCAN Activation of frontoparietal attention networks by non-predictive gaze and arrow cues Robert M. Joseph 2 Zachary Fricker 1 2 Brandon Keehn 0 0 Laboratories of Cognitive Neuroscience, Division of Developmental Medicine, Boston Children's Hospital , 1 Autumn St., Boston, MA, 02115 , USA 1 Department of Medicine, Massachusetts General Hospital , 55 Fruit St., Boston, MA 02114 , USA 2 Department of Anatomy and Neurobiology, Boston University School of Medicine , 72 E. Concord St., Boston, MA, 02118 , USA Gaze and arrow cues automatically orient visual attention, even when they have no predictive value, but the neural circuitry by which they direct attention is not clear. Recent evidence has indicated that the ventral frontoparietal attention network is primarily engaged by breaches of a viewer s cuerelated expectations. Accordingly, we hypothesized that to the extent that non-predictive gaze and arrow cues automatically engender expectations with regard to cue location, they should activate the ventral attention network when they cue attention invalidly. Using event-related fMRI, we found that invalid gaze but not arrow cues activated the ventral attention network, specifically in the area of the right temporal parietal junction (TPJ), as well as nodes along the dorsal attention network associated with a redirection of attention to the correct target location. In additional whole-brain analyses, facilitation of behavioral response time by valid gaze cues was linearly associated with the degree of activation in the right TPJ. We conclude from our findings that gaze direction elicits potent expectations in humans with regard to an actor s intention that engage attention networks if not differently from, at least more robustly than, arrow cues. gaze; arrow; visual attention; spatial orienting; intention INTRODUCTION There is abundant research evidence that a person’s direction of gaze automatically shifts a viewer’s attention to the gazed-at location (Friesen and Kingstone, 1998; Driver et al., 1999; Langton and Bruce, 1999; Ristic et al., 2002; Friesen et al., 2004) . Experimental studies of the visual orienting effects of gaze direction have typically been conducted with a modified version of the classic visuospatial cuing paradigm developed by Posner (1980) . In the standard task, a transient peripheral cue, such as a brief change in luminance, occurs momentarily to the left or right of a central point of fixation, and the viewer’s task is to report the location of a subsequent target. When valid, the cue accurately indicates the location of the forthcoming target. When invalid, the cue indicates the location opposite the target. At short cue-target intervals, even when the cue does not predict the target location, the viewer is quicker to detect validly than invalidly cued targets. Faster response times to validly cued targets have been taken as evidence that transient luminance cues automatically orient visuospatial attention prior to target onset. On invalid trials, the target’s appearance in the uncued location requires the viewer to reorient attention to that location, increasing response time. In the Posner-like gaze-cuing task, a face with the eyes directed either to the left or right is presented centrally and, as in the standard task, the viewer responds by indicating on which side a subsequent target appears. Viewers respond more quickly to targets that are in the direction of the gaze cue than those in the location opposite the gaze cue. The attention-orienting effect of gaze shifts has been viewed as automatic or reflexive because it is rapid, typically occurring within 100–200 ms of the cue, and because it occurs even when the viewer knows that the gaze cues are not predictive or are counterpredictive of the forthcoming target’s location. Initial evidence that centrally presented gaze direction cues, which require perceptual analysis and interpretation, orient visuospatial attention reflexively led to the proposal that gaze cuing has a special social–biological status in human evolution (Friesen and Kingstone, 1998; Langton et al., 2000) . This possibility, however, has been put into question by evidence that non-predictive, centrally presented symbolic cues, namely arrows, whose significance is culturally rather than biologically determined, also elicit reflexive orienting effects (Ristic et al., 2002; Tipples, 2002) . Some studies that have compared the effects of counterpredictive gaze and arrows cues have shown that automatic orienting to gaze direction is more resistant to top-down, volitional control (such as when a viewer orients attention in the direction of a gaze cue despite knowing that it is counterpredictive) and are thus ‘more reflexive’ than orienting responses to arrows (Driver et al., 1999; Friesen et al., 2004, 2007) . Nevertheless, other studies have demonstrated that arrows are as effective as gaze in overriding volitional control and orienting attention a (...truncated)


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Robert M. Joseph, Zachary Fricker, Brandon Keehn. Activation of frontoparietal attention networks by non-predictive gaze and arrow cues, Social Cognitive and Affective Neuroscience, 2015, pp. 294-301, 10/2, DOI: 10.1093/scan/nsu054