Differential activation of frontoparietal attention networks by social and symbolic spatial cues

Center for the Study of Brain Mind and Behavior, Princeton University, Princeton, NJ 08540, USA.
Social Cognitive and Affective Neuroscience (Impact Factor: 7.37). 03/2010; 5(4):432-40. DOI: 10.1093/scan/nsq008
Source: PubMed


Perception of both gaze-direction and symbolic directional cues (e.g. arrows) orient an observer's attention toward the indicated location. It is unclear, however, whether these similar behavioral effects are examples of the same attentional phenomenon and, therefore, subserved by the same neural substrate. It has been proposed that gaze, given its evolutionary significance, constitutes a 'special' category of spatial cue. As such, it is predicted that the neural systems supporting spatial reorienting will be different for gaze than for non-biological symbols. We tested this prediction using functional magnetic resonance imaging to measure the brain's response during target localization in which laterally presented targets were preceded by uninformative gaze or arrow cues. Reaction times were faster during valid than invalid trials for both arrow and gaze cues. However, differential patterns of activity were evoked in the brain. Trials including invalid rather than valid arrow cues resulted in a stronger hemodynamic response in the ventral attention network. No such difference was seen during trials including valid and invalid gaze cues. This differential engagement of the ventral reorienting network is consistent with the notion that the facilitation of target detection by gaze cues and arrow cues is subserved by different neural substrates.

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Available from: Lauri Nummenmaa
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    • "A number of studies reported that the observation of averted eyes compared with straight eyes or other control stimuli, elicited more activation in several brain regions, including the posterior superior temporal sulcus/middle temporal gyrus (Calder et al., 2002;Engell and Haxby, 2007;Hoffman and Haxby, 2000;Hooker et al., 2003;Pelphrey et al., 2003;Puce et al., 1998;Sato et al., 2008;Wicker et al., 1998), fusiform gyrus (Calder et al., 2002;George et al., 2001;Pelphrey et al., 2003;Wicker et al., 1998), inferior parietal lobule (Calder et al., 2002;Hoffman and Haxby, 2000;Pelphrey et al., 2003;Sato et al., 2008;Wicker et al., 1998), and middle/inferior frontal gyrus (Calder et al., 2002;Hooker et al., 2003;Wicker et al., 1998). Several studies investigated the brain activation in response to averted versus straight eyes in the framework of the cueing paradigm (Callejas et al., 2013;Cazzato et al., 2012;Engell et al., 2010;Greene et al., 2009;Hietanen et al., 2006;Kingstone et al., 2004;Sato et al., 2009;Tipper et al., 2008). Although foci, methodologies, and results were not identical across these studies and disagreements persist, several of these studies (Greene et al., 2009;Sato et al., 2009;Tipper et al., 2008) were consistent in reporting that the temporal, parietal, and frontal regions were involved in attentional shifts triggered by eye gaze. "
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    ABSTRACT: Behavioral studies have shown that eye gaze triggers attentional shifts both with and without conscious awareness. However, the neural substrates of conscious and unconscious attentional shifts triggered by eye gaze remain unclear. To investigate this issue, we measured brain activity using event-related functional magnetic resonance imaging while participants observed averted or straight eye-gaze cues presented supraliminally or subliminally in the central visual field and then localized a subsequent target in the peripheral visual field. Reaction times for localizing the targets were shorter under both supraliminal and subliminal conditions when eye-gaze cues were directionally congruent with the target locations than when they were directionally neutral. Conjunction analyses revealed that a bilateral cortical network, including the middle temporal gyri, inferior parietal lobules, anterior cingulate cortices, and superior and middle frontal gyri, was activated more in response to averted eyes than to straight eyes under both supraliminal and subliminal conditions. Interaction analyses revealed that the right inferior parietal lobule was specifically active when participants viewed averted eyes relative to straight eyes under the supraliminal condition; the bilateral subcortical regions, including the superior colliculus and amygdala, and the middle temporal and inferior frontal gyri in the right hemisphere were activated in response to averted versus straight eyes under the subliminal condition. These results suggest commonalities and differences in the neural mechanisms underlying conscious and unconscious attentional shifts triggered by eye gaze.
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    • "Several studies have investigated the neural substrates of social attention in human and non-human primates with particular emphasis on the role of the gaze (Callejas, Shulman, & Corbetta, 2014; Deaner et al., 2003; Engell et al., 2010; Greene, Mooshagian, Kaplan, Zaidel, & Iacoboni, 2009; Sato, Kochiyama, Uono, & Yoshikawa, 2009; Shepherd et al., 2009; Tipper et al., 2008). Yet, the functional and neural bases underlying these processes are not completely understood. "
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    • "). The exact role of this region in social and symbolic cuing has remained unclear despite several studies (Engell et al., 2010), in part due to the limited temporal precision of imaging techniques. Electrophysiological investigation will no doubt help address these issues, but it must be noted that no direct parallel to arrow cues exists in animals; most modern-day humans learn to respond automatically to arrows through a lifetime of acculturation. "
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