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)