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Reverse-engineering the cortical architecture for controlled semantic cognition.

ABSTRACT: We employ a reverse-engineering approach to illuminate the neurocomputational building blocks that combine to support controlled semantic cognition: the storage and context-appropriate use of conceptual knowledge. By systematically varying the structure of a computational model and assessing the functional consequences, we identified the architectural properties that best promote some core functions of the semantic system. Semantic cognition presents a challenging test case, as the brain must achieve two seemingly contradictory functions: abstracting context-invariant conceptual representations across time and modalities, while producing specific context-sensitive behaviours appropriate for the immediate task. These functions were best achieved in models possessing a single, deep multimodal hub with sparse connections from modality-specific regions, and control systems acting on peripheral rather than deep network layers. The reverse-engineered model provides a unifying account of core findings in the cognitive neuroscience of controlled semantic cognition, including evidence from anatomy, neuropsychology and functional brain imaging.

SUBMITTER: Jackson RL

PROVIDER: S-EPMC7611056 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Built upon a wealth of neuroimaging, neurostimulation, and neuropsychology data, a recent proposal set forth a framework termed controlled semantic cognition (CSC) to account for how the brain underpins the ability to flexibly use semantic knowledge (Lambon Ralph et al., 2017; Nature Reviews Neuroscience). In CSC, the 'semantic control' system, underpinned predominantly by the prefrontal cortex, dynamically monitors and modulates the 'semantic representation' system that consists of a 'hub' (anterior temporal lobe, ATL) and multiple 'spokes' (modality-specific areas). CSC predicts that unfamiliar and exacting semantic tasks should intensify communication between the 'control' and 'representation' systems, relative to familiar and less taxing tasks. In the present study, we used functional magnetic resonance imaging (fMRI) to test this hypothesis. Participants paired unrelated concepts by canonical colours (a less accustomed task - e.g., pairing ketchup with fire-extinguishers due to both being red) or paired well-related concepts by semantic relationship (a typical task - e.g., ketchup is related to mustard). We found the 'control' system was more engaged by atypical than typical pairing. While both tasks activated the ATL 'hub', colour pairing additionally involved occipitotemporal 'spoke' regions abutting areas of hue perception. Furthermore, we uncovered a gradient along the ventral temporal cortex, transitioning from the caudal 'spoke' zones preferring canonical colour processing to the rostral 'hub' zones preferring semantic relationship. Functional connectivity also differed between the tasks: Compared with semantic pairing, colour pairing relied more upon the inferior frontal gyrus, a key node of the control system, driving enhanced connectivity with occipitotemporal 'spoke'. Together, our findings characterise the interaction within the neural architecture of semantic cognition - the control system dynamically heightens its connectivity with relevant components of the representation system, in response to different semantic contents and difficulty levels.

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Reverse-engineering the cortical architecture for controlled semantic cognition.

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