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Journal ArticleDOI

Rethinking the role of the rTPJ in attention and social cognition in light of the opposing domains hypothesis: findings from an ALE-based meta-analysis and resting-state functional connectivity

TL;DR: An alternative account is proposed, according to which the capacity for social cognition depends on a network which is both distinct from and in tension with brain areas involved in focused attention and target detection: the default mode network (DMN).
Abstract: The right temporo-parietal junction (rTPJ) has been associated with two apparently disparate functional roles: in attention and in social cognition. According to one account, the rTPJ initiates a “circuit-breaking” signal that interrupts ongoing attentional processes, effectively reorienting attention. It is argued this primary function of the rTPJ has been extended beyond attention, through a process of evolutionarily cooption, to play a role in social cognition. We propose an alternative account, according to which the capacity for social cognition depends on a network which is both distinct from and in tension with brain areas involved in focused attention and target detection: the default mode network (DMN). Theory characterizing the rTPJ based on the area's purported role in reorienting may be falsely guided by the co-occurrence of two distinct effects in contiguous regions: activation of the supramarginal gyrus (SMG), associated with its functional role in target detection; and the transient release, during spatial reorienting, of suppression of the angular gyrus (AG) associated with focused attention. Findings based on meta-analysis and resting functional connectivity are presented which support this alternative account. We find distinct regions, possessing anti-correlated patterns of resting connectivity, associated with social reasoning (AG) and target detection (SMG) at the rTPJ. The locus for reorienting was spatially intermediate between the AG and SMG and showed a pattern of connectivity with similarities to social reasoning and target detection seeds. These findings highlight a general methodological concern for brain imaging. Given evidence that certain tasks not only activate some areas but also suppress activity in other areas, it is suggested that researchers need to distinguish two distinct putative mechanisms, either of which may produce an increase in activity in a brain area: functional engagement in the task vs. release of suppression.

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Citations
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Journal ArticleDOI
TL;DR: TPJ function in many domains is well described by contextual updating by using data from cognitive neuroscience to critically evaluate the function of the temporo-parietal junction.

308 citations


Cites background from "Rethinking the role of the rTPJ in ..."

  • ...Although these differences can be seemingly small from study-to-study, they have played a critical role in the debate regarding functional specialization (Decety and Lamm, 2007a; Mitchell, 2008; Scholz et al., 2009; Kubit and Jack, 2013)....

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Journal ArticleDOI
TL;DR: While posterior rTPJ seems exclusively involved in the social domain, anterior rTPj is involved in both, attention and ToM, conceivably indicating an attentional shifting role of this region.
Abstract: The right temporoparietal junction (rTPJ) is frequently associated with different capacities that to shift attention to unexpected stimuli (reorienting of attention) and to understand others’ (false) mental state [theory of mind (ToM), typically represented by false belief tasks]. Competing hypotheses either suggest the rTPJ representing a unitary region involved in separate cognitive functions or consisting of subregions subserving distinct processes. We conducted activation likelihood estimation (ALE) meta-analyses to test these hypotheses. A conjunction analysis across ALE meta-analyses delineating regions consistently recruited by reorienting of attention and false belief studies revealed the anterior rTPJ, suggesting an overarching role of this specific region. Moreover, the anatomical difference analysis unravelled the posterior rTPJ as higher converging in false belief compared with reorienting of attention tasks. This supports the concept of an exclusive role of the posterior rTPJ in the social domain. These results were complemented by meta-analytic connectivity mapping (MACM) and resting-state functional connectivity (RSFC) analysis to investigate whole-brain connectivity patterns in task-constrained and task-free brain states. This allowed for detailing the functional separation of the anterior and posterior rTPJ. The combination of MACM and RSFC mapping showed that the posterior rTPJ has connectivity patterns with typical ToM regions, whereas the anterior part of rTPJ co-activates with the attentional network. Taken together, our data suggest that rTPJ contains two functionally fractionated subregions: while posterior rTPJ seems exclusively involved in the social domain, anterior rTPJ is involved in both, attention and ToM, conceivably indicating an attentional shifting role of this region.

260 citations


Cites background from "Rethinking the role of the rTPJ in ..."

  • ...Recent ALE meta-analyses have already reviewed the role of the rTPJ from different perspectives (Bzdok et al. 2012; Decety and Lamm 2007; Geng and Vossel 2013; Kubit and Jack 2013)....

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  • ...Basically, it has been suggested that the function of the posterior rTPJ network is particularly related to a more internally oriented network, also relating to the default mode network reflecting stimulus-independent mental processes (Bzdok et al. 2013a; Kubit and Jack 2013; Mars et al. 2012a)....

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Journal ArticleDOI
TL;DR: An integrative review and novel insights regarding human research with classic psychedelics (classic hallucinogens), which are serotonin 2A receptor (5‐HT2AR) agonists such as lysergic acid diethylamide (LSD), mescaline, and psilocybin, are offered.

243 citations


Cites background from "Rethinking the role of the rTPJ in ..."

  • ..., 2012), and the LPChas been implicated in a number of processes, including empathy (Kubit and Jack, 2013) and coding a sense of self in spatial cognition (Amorapanth et al....

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  • ...…(Svoboda et al., 2006), self-related judgements and theory of mind processes (Gilbert et al., 2006; Denny et al., 2012), and the LPChas been implicated in a number of processes, including empathy (Kubit and Jack, 2013) and coding a sense of self in spatial cognition (Amorapanth et al., 2010)....

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Journal ArticleDOI
TL;DR: This review aimed to synthesize findings from anatomical and functional studies of the IPL/TPJ that used neuroimaging at rest and during a wide range of tasks to discuss how network nodes within the IPJ are organized and how they participate in human perception and cognition.

234 citations


Cites background or result from "Rethinking the role of the rTPJ in ..."

  • ...…in within-subject studies and metaanalyses, but separation has also been reported, with a more posterior location for theory-of-mind activity (Bzdok et al., 2013; Carter and Huettel, 2013; Decety and Lamm, 2007; Krall et al., 2015; Kubit and Jack, 2013; Lee and McCarthy, 2016; Mitchell, 2008)....

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  • ...The location of the IPL/TPJ activation is often more anterior than the region recruited by invalidly cued targets in Posner tasks, and is more consistent with the TPJa as defined in our studies (Igelström et al., 2015, 2016a; Kim, 2014; Kubit and Jack, 2013)....

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  • ...Some overlap of social and attentional processes have been found in within-subject studies and metaanalyses, but separation has also been reported, with a more posterior location for theory-of-mind activity (Bzdok et al., 2013; Carter and Huettel, 2013; Decety and Lamm, 2007; Krall et al., 2015; Kubit and Jack, 2013; Lee and McCarthy, 2016; Mitchell, 2008)....

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Journal ArticleDOI
TL;DR: Neuroscience has the potential to address accounts of theory-of-mind acquisition and future research directions include microgenetic and training fMRI studies.

158 citations

References
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Journal ArticleDOI
TL;DR: Evidence for partially segregated networks of brain areas that carry out different attentional functions is reviewed, finding that one system is involved in preparing and applying goal-directed selection for stimuli and responses, and the other is specialized for the detection of behaviourally relevant stimuli.
Abstract: We review evidence for partially segregated networks of brain areas that carry out different attentional functions. One system, which includes parts of the intraparietal cortex and superior frontal cortex, is involved in preparing and applying goal-directed (top-down) selection for stimuli and responses. This system is also modulated by the detection of stimuli. The other system, which includes the temporoparietal cortex and inferior frontal cortex, and is largely lateralized to the right hemisphere, is not involved in top-down selection. Instead, this system is specialized for the detection of behaviourally relevant stimuli, particularly when they are salient or unexpected. This ventral frontoparietal network works as a 'circuit breaker' for the dorsal system, directing attention to salient events. Both attentional systems interact during normal vision, and both are disrupted in unilateral spatial neglect.

10,985 citations


"Rethinking the role of the rTPJ in ..." refers background in this paper

  • ...These findings present three challenges to current theory concerning the VAN (Corbetta and Shulman, 2002; Corbetta et al., 2008)....

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  • ...First, contra Corbetta and Shulman (2002), our findings indicate that target detection has a distinct locus from reorienting....

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  • ...…neuroscience has implicated cortical regions near the right temporo-parietal junction (rTPJ) in a broad variety of tasks ranging from social interactions (Saxe and Powell, 2006) to attentional interactions with inanimate, visuo-spatial stimuli (Corbetta and Shulman, 2002; Corbetta et al., 2008)....

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  • ...In that case, our challenge to VAN theory would be restricted to noting the need to differentiate between regions involved in reorienting, target detection (Corbetta and Shulman, 2002) and ToM (Corbetta et al., 2008)....

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  • ...In summary, the number of attention networks has increased and evolved into a more complex account than simply the DAN and VAN (Corbetta and Shulman, 2002)....

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Journal ArticleDOI
TL;DR: Past observations are synthesized to provide strong evidence that the default network is a specific, anatomically defined brain system preferentially active when individuals are not focused on the external environment, and for understanding mental disorders including autism, schizophrenia, and Alzheimer's disease.
Abstract: Thirty years of brain imaging research has converged to define the brain’s default network—a novel and only recently appreciated brain system that participates in internal modes of cognition Here we synthesize past observations to provide strong evidence that the default network is a specific, anatomically defined brain system preferentially active when individuals are not focused on the external environment Analysis of connectional anatomy in the monkey supports the presence of an interconnected brain system Providing insight into function, the default network is active when individuals are engaged in internally focused tasks including autobiographical memory retrieval, envisioning the future, and conceiving the perspectives of others Probing the functional anatomy of the network in detail reveals that it is best understood as multiple interacting subsystems The medial temporal lobe subsystem provides information from prior experiences in the form of memories and associations that are the building blocks of mental simulation The medial prefrontal subsystem facilitates the flexible use of this information during the construction of self-relevant mental simulations These two subsystems converge on important nodes of integration including the posterior cingulate cortex The implications of these functional and anatomical observations are discussed in relation to possible adaptive roles of the default network for using past experiences to plan for the future, navigate social interactions, and maximize the utility of moments when we are not otherwise engaged by the external world We conclude by discussing the relevance of the default network for understanding mental disorders including autism, schizophrenia, and Alzheimer’s disease

8,448 citations


"Rethinking the role of the rTPJ in ..." refers background in this paper

  • ...…of the default network can, in some cases, be best accounted for by the suppressive effect of task demands which are positively associated with functions instantiated in entirely distinct cortical networks (McKiernan et al., 2003; Mason et al., 2007; Buckner et al., 2008; Andrews-Hanna, 2011)....

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Journal ArticleDOI
TL;DR: It is suggested that both task-driven neuronal responses and behavior are reflections of this dynamic, ongoing, functional organization of the brain, featuring the presence of anticorrelated networks in the absence of overt task performance.
Abstract: During performance of attention-demanding cognitive tasks, certain regions of the brain routinely increase activity, whereas others routinely decrease activity. In this study, we investigate the extent to which this task-related dichotomy is represented intrinsically in the resting human brain through examination of spontaneous fluctuations in the functional MRI blood oxygen level-dependent signal. We identify two diametrically opposed, widely distributed brain networks on the basis of both spontaneous correlations within each network and anticorrelations between networks. One network consists of regions routinely exhibiting task-related activations and the other of regions routinely exhibiting task-related deactivations. This intrinsic organization, featuring the presence of anticorrelated networks in the absence of overt task performance, provides a critical context in which to understand brain function. We suggest that both task-driven neuronal responses and behavior are reflections of this dynamic, ongoing, functional organization of the brain.

7,741 citations


"Rethinking the role of the rTPJ in ..." refers background or methods or result in this paper

  • ...…and that these regions are part of two distinct networks which can be differentiated using rs-fcMRI (Fox et al., 2005; Cohen et al., 2008; Mars et al., 2012a) and by virtue of their differential engagement in attention demanding social and non-social tasks (Fox et al., 2005; Jack et al., 2012)....

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  • ...…of true anti-correlations, and that findings using a global regressor appear more accurate when compared to independent evidence: The methods of Fox et al. (2005) using global normalization, which we also use here, demonstrate good correspondence with regions that are consistently deactivated…...

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  • ...The TPN also includes a region near the rTPJ, the SMG (Fox et al., 2005; Jack et al., 2012)....

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  • ...…2008; Scholz et al., 2009; Mars et al., 2012a), and that these regions are part of two distinct networks which can be differentiated using rs-fcMRI (Fox et al., 2005; Cohen et al., 2008; Mars et al., 2012a) and by virtue of their differential engagement in attention demanding social and non-social…...

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  • ...…with the DMN, regions anti-correlated with the target detection seed show an excellent correspondence with the DMN as identified in prior publications (Fox et al., 2005), including rTPJ, MP/PCC, and dMPFC regions specifically associated with mentalizing (Van Overwalle, 2009; Denny et al., 2012)....

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Journal ArticleDOI
TL;DR: The data allow us to reject alternative accounts of the function of the fusiform face area (area “FF”) that appeal to visual attention, subordinate-level classification, or general processing of any animate or human forms, demonstrating that this region is selectively involved in the perception of faces.
Abstract: Using functional magnetic resonance imaging (fMRI), we found an area in the fusiform gyrus in 12 of the 15 subjects tested that was significantly more active when the subjects viewed faces than when they viewed assorted common objects. This face activation was used to define a specific region of interest individually for each subject, within which several new tests of face specificity were run. In each of five subjects tested, the predefined candidate “face area” also responded significantly more strongly to passive viewing of (1) intact than scrambled two-tone faces, (2) full front-view face photos than front-view photos of houses, and (in a different set of five subjects) (3) three-quarter-view face photos (with hair concealed) than photos of human hands; it also responded more strongly during (4) a consecutive matching task performed on three-quarter-view faces versus hands. Our technique of running multiple tests applied to the same region defined functionally within individual subjects provides a solution to two common problems in functional imaging: (1) the requirement to correct for multiple statistical comparisons and (2) the inevitable ambiguity in the interpretation of any study in which only two or three conditions are compared. Our data allow us to reject alternative accounts of the function of the fusiform face area (area “FF”) that appeal to visual attention, subordinate-level classification, or general processing of any animate or human forms, demonstrating that this region is selectively involved in the perception of faces.

7,059 citations


"Rethinking the role of the rTPJ in ..." refers background in this paper

  • ...Instead, the right AG lies near to a right lateralized system of occipital and temporal regions involved in the sensory processing of socially relevant information (Kanwisher et al., 1997; Peelen, 2004; Pelphrey, 2005)....

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Journal ArticleDOI
TL;DR: In this paper, the organization of networks in the human cerebrum was explored using resting-state functional connectivity MRI data from 1,000 subjects and a clustering approach was employed to identify and replicate networks of functionally coupled regions across the cerebral cortex.
Abstract: Information processing in the cerebral cortex involves interactions among distributed areas. Anatomical connectivity suggests that certain areas form local hierarchical relations such as within the visual system. Other connectivity patterns, particularly among association areas, suggest the presence of large-scale circuits without clear hierarchical relations. In this study the organization of networks in the human cerebrum was explored using resting-state functional connectivity MRI. Data from 1,000 subjects were registered using surface-based alignment. A clustering approach was employed to identify and replicate networks of functionally coupled regions across the cerebral cortex. The results revealed local networks confined to sensory and motor cortices as well as distributed networks of association regions. Within the sensory and motor cortices, functional connectivity followed topographic representations across adjacent areas. In association cortex, the connectivity patterns often showed abrupt transitions between network boundaries. Focused analyses were performed to better understand properties of network connectivity. A canonical sensory-motor pathway involving primary visual area, putative middle temporal area complex (MT+), lateral intraparietal area, and frontal eye field was analyzed to explore how interactions might arise within and between networks. Results showed that adjacent regions of the MT+ complex demonstrate differential connectivity consistent with a hierarchical pathway that spans networks. The functional connectivity of parietal and prefrontal association cortices was next explored. Distinct connectivity profiles of neighboring regions suggest they participate in distributed networks that, while showing evidence for interactions, are embedded within largely parallel, interdigitated circuits. We conclude by discussing the organization of these large-scale cerebral networks in relation to monkey anatomy and their potential evolutionary expansion in humans to support cognition.

6,284 citations