No abstract

Association cortex is organized into large-scale distributed networks. One such network, the default network (DN), is linked to diverse forms of internal mentation, opening debate about whether shared or distinct anatomy supports multiple forms of cognition. Using within-individual analysis procedures that preserve idiosyncratic anatomical details, we probed whether multiple tasks from two domains, episodic projection and theory of mind (ToM), rely on the same or distinct networks. In an initial experiment (6 subjects, each scanned 4 times), we found evidence that episodic projection and ToM tasks activate separate regions distributed throughout the cortex, with adjacent regions in parietal, temporal, prefrontal, and midline zones. These distinctions were predicted by the hypothesis that the DN comprises two parallel, interdigitated networks. One network, linked to parahippocampal cortex (PHC), is preferentially recruited during episodic projection, including both remembering and imagining the future. A second juxtaposed network, which includes the temporoparietal junction (TPJ), is differentially engaged during multiple forms of ToM. In two prospectively acquired independent experiments, we replicated and triplicated the dissociation (each with 6 subjects scanned 4 times). Furthermore, the dissociation was found in all zones when analyzed independently, including robustly in midline regions previously described as hubs. The TPJ-linked network is interwoven with the PHC-linked network across the cortex, making clear why it is difficult to fully resolve the two networks in group-averaged or lower-resolution data. These results refine our understanding of the functional-anatomical organization of association cortex and raise fundamental questions about how specialization might arise in parallel, juxtaposed association networks. NEW & NOTEWORTHY Two distributed, interdigitated networks exist within the bounds of the canonical default network. Here we used repeated scanning of individuals, across three independent samples, to provide evidence that tasks requiring episodic projection or theory of mind differentially recruit the two networks across multiple cortical zones. The two distributed networks thus appear to preferentially subserve distinct functions.

Using procedures optimized to explore network organization within the individual, the topography of a candidate language network was characterized and situated within the broader context of adjacent networks. The candidate network was first identified using functional connectivity and replicated across individuals, datasets, acquisition tasks, and analytic methods. In addition to classical language regions near to perisylvian cortex and temporal pole, additional regions were observed in dorsal posterior cingulate, midcingulate, anterior superior frontal and inferior temporal cortex. The candidate network was selectively activated when processing meaningful (as contrast to non-word) sentences, while spatially adjacent networks showed minimal or even decreased activity. Examined in relation to adjacent networks, the topography of the language network was found to parallel the motif of other association networks including the transmodal association networks linked to theory of mind and episodic remembering (often collectively called the default network). The several networks contained juxtaposed regions in multiple association zones. Outside of these juxtaposed higher-order networks, we further noted a distinct frontotemporal network situated between language regions and a frontal orofacial motor region and a temporal auditory region. A possibility is that these functionally-related sensorimotor regions might anchor specialization of neighboring association regions that develop into the language network. What is most striking is that the canonical language network appears to be just one of multiple similarly organized, differentially specialized distributed networks that populate the evolutionarily expanded zones of human association cortex.

Using procedures optimized to explore network organization within the individual, the topography of a candidate language network was characterized and situated within the broader context of adjacent networks. The candidate network was first identified using functional connectivity and replicated across individuals, acquisition tasks, and analytic methods. In addition to classical language regions near to perisylvian cortex and temporal pole, regions were also observed in dorsal posterior cingulate, midcingulate, anterior superior frontal and inferior temporal cortex. The candidate network was selectively activated when processing meaningful (as contrasted to non-word) sentences, while spatially adjacent networks showed minimal or even decreased activity. Results were replicated and triplicated across two prospectively acquired cohorts. Examined in relation to adjacent networks, the topography of the language network was found to parallel the motif of other association networks including the transmodal association networks linked to theory of mind and episodic remembering (often collectively called the default network). The several networks contained juxtaposed regions in multiple association zones. Outside of these juxtaposed higher-order networks, we further noted a distinct frontotemporal network situated between language regions and a frontal orofacial motor region and a temporal auditory region. A possibility is that these functionally-related sensorimotor regions might anchor specialization of neighboring association regions that develop into a language network. What is most striking is that the canonical language network appears to be just one of multiple similarly organized, differentially specialized distributed networks that populate the evolutionarily expanded zones of human association cortex.

Association cortex is organized into large-scale distributed networks. One such network, the default network (DN), is linked to diverse forms of internal mentation, opening debate about whether shared anatomy supports multiple forms of cognition. Alternatively, subtle distinctions in cortical organization could remain to be resolved. Using within-individual analysis procedures that preserve idiosyncratic details of cortical anatomy, we probed whether multiple tasks from two domains -Episodic Projection and Theory of Mind (ToM) -rely upon the same or distinct networks. In an initial experiment (n=6, subjects scanned 4 times each), we found evidence that Episodic Projection and ToM tasks activate distinct functional regions distributed throughout cortex, with adjacent regions in parietal, temporal, prefrontal and midline zones. These distinctions were predicted by the hypothesis that the DN comprises two parallel, interdigitated networks. One network, linked to parahippocampal cortex (PHC), is preferentially recruited during Episodic Projection, including both remembering the past and imagining the future. A second juxtaposed network, which includes the temporoparietal junction (TPJ), is differentially engaged during multiple forms of ToM tasks. The TPJ-linked network is interwoven with the PHC-linked network in multiple zones, including the posterior and anterior midline, making clear why it is difficult to fully resolve the two networks in groupaveraged or lower-resolution data. We replicated all aspects of this network dissociation in a second, prospectively acquired dataset (n=6). These results refine our understanding of the functional-anatomical organization of association cortex as well as raise questions about how functional specialization might arise in parallel, juxtaposed association networks.