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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    • "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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    ABSTRACT: In highly social groups like human and non human primates, gaze and pointing cues are fundamentally important for directing the attention of conspecifics. Although neuroimaging studies indicate that shifts of attention triggered by observation of social cues activate the onlookers’ fronto-parietal cortices, information on whether these regions play a causative role in orienting and re-orienting of social attention is lacking. To advance our understanding of this, we used event-related repetitive dual pulse transcranial magnetic stimulation to interfere with neural activity in the right frontal eye field (rFEF) and posterior parietal cortex (rPPC). This procedure allowed us to explore how inhibiting rFEF and rPPC influences shifts of attention triggered by the observation of body-related (gaze and hand) and non body-related (arrow) directional distractors. Participants were asked to perform a leftward or rightward pointing movement according to the color change of a central imperative signal while ignoring a distractor, which was either a gaze, a pointing hand or an arrow. Stimulation of rPPC in a region supposedly linked to attentional re-orienting and to planning and execution of upper limb movements increased the reflexive tendency to follow distracting pointing hands but not oriented gaze or arrows. These findings suggest that inhibition of cortical structures that control attentional shifts triggered by social stimuli brings forth an increase of the cost of attentional re-orienting. Moreover, our results provide the first causative evidence that reflexive social attention in humans may be coded according to body-part-centered frames of reference.
    Neuropsychologia 07/2014; 59(1). DOI:10.1016/j.neuropsychologia.2014.04.017 · 3.30 Impact Factor
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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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    ABSTRACT: Humans and other primates shift their attention to follow the gaze of others (gaze following, GF). This behavior is a foundational component of joint attention, which is severely disrupted in neurodevelopmental disorders such as autism and schizophrenia. Both cortical and subcortical pathways have been implicated in GF, but their contributions remain largely untested. While the proposed subcortical pathway hinges crucially on the amygdala, the cortical pathway is thought to require perceptual processing by a region in the posterior superior temporal sulcus (pSTS). To determine whether pSTS is necessary for typical GF behavior, we engaged rhesus macaques in a reward discrimination task confounded by leftward- and rightward-facing social distractors following saline or muscimol injections into left pSTS. We found that reversible inactivation of left pSTS with muscimol strongly suppressed GF, as assessed by reduced influence of observed gaze on target choices and saccadic reaction times. These findings demonstrate that activity in pSTS is required for normal GF by primates.
    Social Cognitive and Affective Neuroscience 11/2012; 9(2). DOI:10.1093/scan/nss123 · 7.37 Impact Factor
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    • "The present data, for the first time, provide unequivocal evidence that number-induced attentional shifts modulate the response of visual areas, as observed in more conventional attention paradigms on voluntary visuospatial orienting (e.g., Brefczynski & DeYoe, 1999). This is all the more remarkable since, contrary to other central symbolic cues like eye gaze or arrows (Thiel, Zilles, & Fink, 2004; Hietanen, Nummenmaa, Nyman, Parkkola, & Hämäläinen, 2006; Engell et al., 2010), Arabic digit stimuli provide no spatial information whatsoever . Consequently, the number-space association must arise at a purely semantic level related to long-term memory traces (Hubbard et al., 2009) and/or working memory rehearsal (van Dijck & Fias, 2011; Fias, van Dijck, & Gevers, 2011) of the central uninformative number cues. "
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    ABSTRACT: Number processing interacts with space encoding in a wide variety of experimental paradigms. Most intriguingly, the passive viewing of uninformative number symbols can shift visuo-spatial attention to different target locations according to the number magnitude, i.e., small/large numbers facilitate processing of left/right targets, respectively. The brain architecture dedicated to these attention shifts associated with numbers currently remains unknown. Evoked potential recordings indicate that both early and late stages are involved in this spatio-numerical interaction, but the neuro-functional anatomy needs to be specified. Here we use, for the first time, functional magnetic resonance imaging (fMRI) to investigate attentional orienting following uninformative Arabic digits. We show that BOLD response in occipital visual regions was modulated by the congruency between digit magnitude (small/large) and target side (left/right). Additionally, we report higher BOLD responses following large (8, 9) compared to small (1, 2) digits in two bilateral parietal regions, yielding a significant effect of digit magnitude. We propose and discuss the view that encoding of semantic representations related to number symbols in parietal cortex led to shifts in visuo-spatial attention and enhanced visual processing in the occipital cortex according to number-space congruency rules.
    Neuropsychologia 10/2012; 50(14). DOI:10.1016/j.neuropsychologia.2012.09.046 · 3.30 Impact Factor
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