Elsevier

NeuroImage

Volume 81, 1 November 2013, Pages 381-392
NeuroImage

Technical Note
Characterization of the temporo-parietal junction by combining data-driven parcellation, complementary connectivity analyses, and functional decoding

https://doi.org/10.1016/j.neuroimage.2013.05.046Get rights and content

Highlights

  • Multimodal connectivity-based parcellation identified two distinct cortical modules.

  • Parcellation results using resting-state and co-activations were nearly identical.

  • The derived cortical modules featured anti-correlated connectivity patterns.

  • The modules were functionally related to stimulus–response and social processes.

Abstract

The right temporo-parietal junction (RTPJ) is consistently implicated in two cognitive domains, attention and social cognitions. We conducted multi-modal connectivity-based parcellation to investigate potentially separate functional modules within RTPJ implementing this cognitive dualism. Both task-constrained meta-analytic coactivation mapping and task-free resting-state connectivity analysis independently identified two distinct clusters within RTPJ, subsequently characterized by network mapping and functional forward/reverse inference. Coactivation mapping and resting-state correlations revealed that the anterior cluster increased neural activity concomitantly with a midcingulate–motor–insular network, functionally associated with attention, and decreased neural activity concomitantly with a parietal network, functionally associated with social cognition and memory retrieval. The posterior cluster showed the exact opposite association pattern. Our data thus suggest that RTPJ links two antagonistic brain networks processing external versus internal information.

Introduction

The human right temporo-parietal junction (RTPJ) is a supramodal association area located at the border between the temporal and parietal lobes surrounding the posterior end of the Sylvian fissure. It is at times referred to as posterior inferior parietal lobule, angular gyrus, Brodmann area 39, or posterior superior temporal sulcus. The highly inconsistent neuroanatomical labeling epitomizes the lacking consensus on coordinates, micro- or macroanatomical landmarks that would topographically define RTPJ (cf. Brodmann, 1909, Déjerine, 1895, Mars et al., 2012). Put differently, “temporo-parietal junction” is a vaguely defined term that is frequently used within various cognitive disciplines to refer to a certain functional cortical module.

While the left TPJ is specifically related to processing language and semantics (Binder et al., 2009), an interesting discrepancy emerges when reviewing the literature on functions of the right TPJ: An extensive body of work implies selectivity of the RTPJ for low-level attentional processes, while a similarly extensive body of literature claims selectivity of the RTPJ for the higher-level processing of social information. More specifically, neuroimaging studies in cognitive neuroscience linked RTPJ activity to spatial reorienting (Corbetta et al., 2000), visuo-proprioceptive conflict (Balslev et al., 2005), and multi-modal detection of sensory changes (Downar et al., 2000). Congruently, direct electrical stimulation of the RTPJ during neurosurgery was associated with altered perception and stimulus awareness (Blanke et al., 2002). Finally, RTPJ lesions in humans are associated with hemi-neglect (Corbetta et al., 2000), i.e. failure to orient visual attention to the contra-lesional side.

On the other hand, neuroimaging research in social neuroscience suggests that the RTPJ encodes imagined goals of others' actions (Hamilton and Grafton, 2008) and contributes to social cognition by specifically representing others' mental states such as thoughts and intentions (i.e., theory of mind, Saxe and Wexler, 2005). Indeed, transient RTPJ disruption by transcranial magnetic stimulation significantly reduced relying on an agent's intentions when judging moral scenarios (Young et al., 2010) and resulted in impaired self–other distinction (Uddin et al., 2006). Taken together, one line of research provides converging evidence for a key role of the RTPJ in attentional processes, while another line of research associates this region with social-cognitive processes.

Conceivably, this apparent contradiction may be explained by an interaction of distinct parts of the RTPJ with different brain networks reflecting functional heterogeneity within this region. The combination of connectivity-based parcellation (CBP), mapping task-constrained/-unconstrained connectivity, and large-scale functional inference represents an ideally suited toolbox for this question. In particular, CBP exploits the unique set of input and output connections of any particular functional cortical module (Passingham et al., 2002, Saygin et al., 2012) to “blindly” infer functional parcellations from connectivity data (Johansen-Berg et al., 2004). To both accommodate lacking neuroanatomical consensus (cf. Mars et al., 2011) and acknowledge the diverse functions ascribed to the RTPJ, the volume of interest for CBP (Fig. 1A) was constructed by merging results of three meta-analyses of neuroimaging data on sustained attention (Langner and Eickhoff, in press), sensorimotor control (Jakobs et al., 2012), and theory of mind (Bzdok et al., 2012b).

First, we thus conducted CBP of the seed region, that is the volume of interest here formed by merging three independent, previously published quantitative meta-analyses. Importantly, the parcellation procedure was performed once for each of two distinct measures of functional connectivity, task-related meta-analytic connectivity modeling (MACM) and task-unrelated resting-state functional connectivity (RSFC). Second, the connectivity-derived sub-regions were characterized by determining their brain-wise connectivity profiles based on the complementary measures of functional connectivity (i.e., MACM and RSFC). Third, we delineated the sub-regions' functional profiles from above-chance taxonomic associations with meta-data archived in the BrainMap database.

Section snippets

Definition of the RTPJ seed region

We conducted connectivity-based parcellation (CBP) on a volume of interest (VOI) that was derived from three individual quantitative meta-analyses. Please note that we opted for a meta-analytic VOI definition because of the absence of commonly accepted neuroanatomical landmarks to define the location of this functional region (see introduction). Rather than deriving a VOI from single fMRI contrasts, we used quantitative meta-analysis results as they overcome several shortcomings of neuroimaging

Functional modules in the RTPJ

Whole-brain task-dependent (MACM; based on coactivation patterns across a large number of databased neuroimaging experiments (Robinson et al., 2010)) and task-independent (RSFC; based on correlations of slow [< 0.1 Hz] fluctuations of fMRI activity during task-free mind-wandering (Biswal et al., 1995)) connectivity analyses were computed for every single voxel within the seed region. For each of these two modalities, the connectivity profiles of all seed voxels were correlated with each other,

Discussion

The functional role of the RTPJ has long remained enigmatic given implication in very heterogeneous mental functions, especially lower-order attention-/action-related cognition and higher-order social cognition. To reflect this functional spectrum, a functional seed region was constructed by merging quantitative meta-analysis results on sustained attention, sensorimotor control, and theory of mind. We then employed connectivity-based-parcellation (CBP) techniques, bimodal network mapping, and

Acknowledgments

This study was supported by the Human Brain Project (R01-MH074457-01A1, PTF, ARL, SBE), the Helmholtz Initiative on Systems-Biology “The Human Brain Model” (KZ, SBE), and the German National Academic Foundation (DB).

Conflict of interest

The authors declare no conflict of interest.

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