An fMRI study of joint attention experience

Williams, Justin H. G.; Waiter, Gordon D.; Perra, Oliver; Perrett, David I.; Whiten, Andrew

doi:10.1016/j.neuroimage.2004.10.047

Cited by 158 publications

(141 citation statements)

References 41 publications

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“…This latter brain region has been proposed, together with rTPJ, as supporting uniquely human social cognition (36). Specifically, dorsal mPFC is implicated in the uniquely human representation of triadic relations between two minds and an object, supporting JA, and has been observed in single-participant JA experiments (37), and in a dualparticipant JA experiment with one subject in the scanner (9,35). However, our observation was not replicated in the second sample we studied and must therefore be considered preliminary until followed up by larger studies using a hyperscanning framework.…”

Section: Discussionmentioning

confidence: 82%

Information flow between interacting human brains: Identification, validation, and relationship to social expertise

Bilek¹,

Ruf

Schäfer³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

144

131

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Social interactions are fundamental for human behavior, but the quantification of their neural underpinnings remains challenging. Here, we used hyperscanning functional MRI (fMRI) to study information flow between brains of human dyads during real-time social interaction in a joint attention paradigm. In a hardware setup enabling immersive audiovisual interaction of subjects in linked fMRI scanners, we characterize cross-brain connectivity components that are unique to interacting individuals, identifying information flow between the sender's and receiver's temporoparietal junction. We replicate these findings in an independent sample and validate our methods by demonstrating that cross-brain connectivity relates to a key real-world measure of social behavior. Together, our findings support a central role of human-specific cortical areas in the brain dynamics of dyadic interactions and provide an approach for the noninvasive examination of the neural basis of healthy and disturbed human social behavior with minimal a priori assumptions.fMRI | hyperscanning | joint attention H uman social interactions have likely shaped brain evolution and are critical for development, health, and society. Defining their neural underpinnings is a key goal of social neuroscience. Interacting dyads, the simplest and fundamental form of human interaction, have been examined with behavioral setups that used real movement interactions during communication in real time as a proxy (1-4), providing mathematical models representing human interaction, goal sharing, mutual engagement, and coordination. To identify the neural systems supporting these behaviors, neuroimaging would be the tool of choice, but studying dyadic interactions with this method is both experimentally and analytically challenging. Consequently, the neural processes underlying human social interactions remain incompletely understood.Experimentally, studying dyads with neuroimaging technology that allows only one participant per scanner provides challenges that have been addressed in the literature in one of two ways. First, the audiovisual experiences of human social contact have been simulated using stimuli such as photographs, recorded videos, or computerized avatars in the absence of human interaction (5-7), or, recently, immersive audiovisual linkups have been used with one of the two participants being scanned (8, 9). Secondly, pioneering neuroimaging experiments have coupled two scanner sites over the Internet, a setup called hyperscanning, enabling subjects to observe higher-level behavioral responses such as choices made to accept or reject an offer in real time while in the scanners (10, 11). In the current study, we aimed to combine the advantages of these experimental approaches by enabling two humans to see (and possibly hear) each other in a hyperscanning framework, enabling an immersive social interaction while both participant's brains are imaged. To do so, we implemented a setup with delay-free data transmission and precisely synchronized data acquisitio...

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Section: Discussionmentioning

confidence: 82%

Information flow between interacting human brains: Identification, validation, and relationship to social expertise

Bilek¹,

Ruf

Schäfer³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

144

131

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“…Evidence in the literature to date seems to suggest that tasks that induce certain types of internal processing activate this resting network. Examples of such tasks are self-and other-person judgments (4,6,7,(19)(20)(21)(22)(38)(39)(40)(41)(42)(43)(44)(45), person familiarity judgments (24,25), emotion processing (15-17, 46), perspective-taking (22,47), passive observation of social interactions vs. nonsocial interactions (18), relaxation based on interoceptive biofeedback (48,49), conceptual judgments (based on internal knowledge stores) vs. perceptual judgments (50), and episodic memory tasks (51), among others [moral decision making (52), joint attention experience (23), and pleasantness judgments (53)]. Therefore, the activity in these regions at rest might simply reflect the extent to which these types of internally directed thoughts are engaged at rest.…”

Section: Discussionmentioning

confidence: 99%

“…First, the functions it subserves [including emotional processing (15)(16)(17), perception of social interactions (18), theory of mind (19)(20)(21)(22), experience of joint attention (23), and person familiarity (24,25)] overlap remarkably well with the social and emotional deficits that characterize autism. Second, in anterior regions of this network, researchers have documented volumetric, metabolic, cellular, and developmental growth abnormalities in this disorder (reviewed in ref.…”

mentioning

confidence: 99%

Failing to deactivate: Resting functional abnormalities in autism

Kennedy

Redcay²,

Courchesne³

2006

Proc. Natl. Acad. Sci. U.S.A.

508

394

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Several regions of the brain (including medial prefrontal cortex, rostral anterior cingulate, posterior cingulate, and precuneus) are known to have high metabolic activity during rest, which is suppressed during cognitively demanding tasks. With functional magnetic resonance imaging (fMRI), this suppression of activity is observed as ''deactivations,'' which are thought to be indicative of an interruption of the mental activity that persists during rest. Thus, measuring deactivation provides a means by which restassociated functional activity can be quantitatively examined. Applying this approach to autism, we found that the autism group failed to demonstrate this deactivation effect. Furthermore, there was a strong correlation between a clinical measure of social impairment and functional activity within the ventral medial prefrontal cortex. We speculate that the lack of deactivation in the autism group is indicative of abnormal internally directed processes at rest, which may be an important contribution to the social and emotional deficits of autism.default mode ͉ functional MRI ͉ introspection ͉ medial prefrontal cortex ͉ precuneus I nternally directed processes, such as self-reflective thought and most higher-order social and emotional processes, consistently activate a medial cortical network involving several brain regions, namely, the medial prefrontal cortex (MPFC) and adjacent rostral anterior cingulate cortex (rACC), posterior cingulate cortex (PCC), and precuneus (PrC) (1-4). Interestingly, this network is active when normal subjects are passively resting (5), leading many to speculate that these internally directed thoughts dominate the resting state (6-9). Self-reports from subjects while at rest further support this interpretation, wherein they typically describe ''autobiographical reminiscences, either recent or ancient, consisting of familiar faces, scenes, dialogues, stories, and melodies'' (8). Conversely, activity in this midline ''resting network'' is reduced when subjects perform externally directed, attention-demanding, goal-oriented tasks (such as the Stroop task or math calculations), and the resulting ''deactivation'' of this network is thought to be an indicator of an interruption of ongoing internally directed thought processes (5, 6, 9-11). In this context, the term deactivation simply refers to activity that is greater during rest than during task performance (i.e., the opposite of the more typically reported activations). Thus, an objective method for testing the functioning of this midline resting network is to measure whether there is deactivation in these regions during externally directed tasks as compared with passive rest. Similar approaches of examining this ''deactivation effect'' have been used in studies of patients with fragile X (12), a developmental disorder with some characteristics that overlap with autism, and in patients with dementia of the Alzheimer type (13) and Alzheimer's disease (14).There are several lines of evidence that suggest that this resting network m...

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“…Regions within inferior parietal cortex have shown robust activity upon presentation of another's hand or body movements (Grafton et al 1996;Iacoboni et al 1999;Rizzolatti et al 1996) that have led researchers to posit involvement of these regions in the internal representation of basic motor movements (Decety and Chaminade 2003;Iacoboni et al 1999;Jeannerod and Frak 1999). Similarly, regions within anterorostral and ventral ACC (r/vACC) as well as within surrounding ventromedial prefrontal cortex, have in turn shown activation during self-judgments (Ochsner et al 2005), social cooperation (Rilling et al 2006), observation of movie clips displaying human actors (Iacoboni et al 2004), joint attention experience (Williams et al 2005), the observation of hand and foot movements (Jackson et al 2004), the observation of videos depicting persons versus videos depicting objects (Mitchell et al 2002), and during judgments of strangers, versus judgments about one's self (Ochsner et al 2005). In the present study, we found substantive activity within both inferior parietal and r/vACC that was unique to the observation of another's errors.…”

Section: Discussionmentioning

confidence: 99%

Neural correlates of the processing of another’s mistakes: A possible underpinning for social and observational learning

et al. 2008

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Recent work suggests that a generalized error-monitoring circuit, which shows heightened activation when one commits an error in goal-directed behavior, may exhibit synonymous activity when one watches another person commit a similar goal-directed error. In the present study, fMRI was utilized to compare and contrast those regions that show sensitivity to the performance, and to the observation, of committed errors. Participants performed a speeded go/nogo task, and also observed a video of another person performing the same task. Dorsal anterior cingulate, orbitofrontal cortex, and supplementary motor regions were commonly activated to both performed and observed errors, providing evidence for common neural circuitry underlying the processing of one's own, and another's mistakes. In addition, several regions, including inferior parietal cortex and anterorostral and ventral cinguli, did not show activation during performed errors, but were instead uniquely activated by the observation of another's mistakes. The unique nature of these 'observer-related' activations suggests that these regions, while of potential import towards recognition of another's errors, are not core to circuitry underlying error-monitoring. Rather, we suggest that these regions may represent components of a distributed network important for the representation and interpretation of complex social actions.

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An fMRI study of joint attention experience

Cited by 158 publications

References 41 publications

Information flow between interacting human brains: Identification, validation, and relationship to social expertise

Information flow between interacting human brains: Identification, validation, and relationship to social expertise

Failing to deactivate: Resting functional abnormalities in autism

Neural correlates of the processing of another’s mistakes: A possible underpinning for social and observational learning

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