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Journal Articles Nature Neuroscience Year : 2018

Generalizable representations of pain, cognitive control, and negative emotion in medial frontal cortex

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A central aim of cognitive neuroscience is to identify how different mental processes are represented in brain activity. The medial frontal cortex (MFC), which includes multiple functionally distinct cortical areas in the superior frontal and cingulate gyri 1 , is one brain region that has been linked to diverse psychological domains, i.e., sets of related psychological states with different adaptive functions 2. Clearly, different areas within MFC encode different functions, but there is a striking convergence of overlapping functions across domains in several 'hub' areas, particularly the anterior midcingulate cortex (aMCC 3). Research across species has linked activity in aMCC with multiple functions, including cognitive control 4,5 , reward-based learning and decision making 6-9 , somatic pain 10,11 , and processing of emotional 12,13 and social information 14,15. In fact, this area responds to such a variety of tasks, and so many underlying functions have been proposed to explain its responses, that it has been described as a "Rorschach test" and understanding it a "holy grail for many cognitive neuroscientists. " 16 Theories of aMCC function often explain the numerous signals in this area as components of an underlying process that operates across domains. Candidate processes have included conflict monitoring 4 , adaptive control (i.e., control processes broadly engaged by negative affect and nociception 17), cognitive effort 18 , valuation of actions 19 and control 20 , and detecting threats to survival 21 , among others. These models have value because they offer integrative explanations for aMCC engagement across multiple domains. However, measuring brain activity across domains with functional MRI (fMRI) glosses over a potential multiplicity of different local neural circuits with distinct functions 22,23. Electrophysiological and optogenetic studies of likely homologs of human aMCC provide evidence for distinct subpopulations of neurons with different functional properties 6,8,24. Recent evidence suggests that multivariate patterns of fMRI activity can, in some cases, identify representations distributed across subpopulations of cells, including identifying functionally dissociable patterns within aMCC associated with different tasks 25,26. Thus, unified accounts of aMCC function make predictions about the similarity of multivariate brain representations across domains that have not been adequately tested. If a set of domains activate representations of a single underlying process, then engaging these representations by tasks from these domain sets should produce similar patterns of brain activity in aMCC and other MFC areas. Conversely, if different domains engage an underlying pattern that is specific to each domain and not shared by other domains, this would provide evidence against a common underlying process. Here we test these predictions using a construct-validation approach grounded in psychometric theory. We investigated three constructs that engage MFC: pain, cognitive control, and negative emotion (see Methods). We sampled human fMRI data from 18 The medial frontal cortex, including anterior midcingulate cortex, has been linked to multiple psychological domains, including cognitive control, pain, and emotion. However, it is unclear whether this region encodes representations of these domains that are generalizable across studies and subdomains. Additionally, if there are generalizable representations, do they reflect a single underlying process shared across domains or multiple domain-specific processes? We decomposed multivariate patterns of functional MRI activity from 270 participants across 18 studies into study-specific, subdomain-specific, and domain-specific components and identified latent multivariate representations that generalized across subdomains but were specific to each domain. Pain representations were localized to anterior midcingulate cortex, negative emotion representations to ventromedial prefrontal cortex, and cognitive control representations to portions of the dorsal midcingulate. These findings provide evidence for medial frontal cortex representations that generalize across studies and subdomains but are specific to distinct psychological domains rather than reducible to a single underlying process.
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inserm-02472527 , version 1 (10-02-2020)



Philip A Kragel, Michiko Kano, Lukas Van Oudenhove, Giao Huynh, Patrick Dupont, et al.. Generalizable representations of pain, cognitive control, and negative emotion in medial frontal cortex. Nature Neuroscience, 2018, 21 (2), pp.283-289. ⟨10.1038/s41593-017-0051-7⟩. ⟨inserm-02472527⟩


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