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Neurocognitive modeling of latent memory processes reveals reorganization of hippocampal-cortical circuits underlying learning and efficient strategies.

ABSTRACT: Efficient memory-based problem-solving strategies are a cardinal feature of expertise across a wide range of cognitive domains in childhood. However, little is known about the neurocognitive mechanisms that underlie the acquisition of efficient memory-based problem-solving strategies. Here we develop, to the best of our knowledge, a novel neurocognitive process model of latent memory processes to investigate how cognitive training designed to improve children's problem-solving skills alters brain network organization and leads to increased use and efficiency of memory retrieval-based strategies. We found that training increased both the use and efficiency of memory retrieval. Functional brain network analysis revealed training-induced changes in modular network organization, characterized by increase in network modules and reorganization of hippocampal-cortical circuits. Critically, training-related changes in modular network organization predicted performance gains, with emergent hippocampal, rather than parietal cortex, circuitry driving gains in efficiency of memory retrieval. Our findings elucidate a neurocognitive process model of brain network mechanisms that drive learning and gains in children's efficient problem-solving strategies.

SUBMITTER: Supekar K

PROVIDER: S-EPMC7994581 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The distribution of pathology in frontotemporal dementia is anatomically selective, to distinct cortical regions and with differential neurodegeneration across the cortical layers. The cytoarchitecture and connectivity of cortical laminae preferentially supports frequency-specific oscillations and hierarchical information transfer between brain regions. We therefore predicted that in frontotemporal dementia, core functional deficits such as disinhibition would be associated with differences in the frequency spectrum and altered cross-frequency coupling between frontal cortical regions. We examined this hypothesis using a 'Go-NoGo' response inhibition paradigm with 18 patients with behavioural variant frontotemporal dementia and 20 healthy aged-matched controls during magnetoencephalography. During Go and NoGo trials, beta desynchronization was severely attenuated in patients. Beta power was associated with increased impulsivity, as measured by the Cambridge Behavioural Inventory, a carer-based questionnaire of changes in everyday behaviour. To quantify the changes in cross-frequency coupling in the frontal lobe, we used dynamic causal modelling to test a family of hierarchical casual models, which included the inferior frontal gyrus, pre-supplementary motor area (preSMA) and primary motor cortex. This analysis revealed evidence for cross-frequency coupling in a fully connected network in both groups. However, in the patient group, we identified a significant loss of reciprocal connectivity of the inferior frontal gyrus, particularly for interactions in the gamma band and for theta to alpha coupling. Importantly, although prefrontal coupling was diminished, gamma connectivity between preSMA and motor cortex was enhanced in patients. We propose that the disruption of behavioural control arises from reduced frequency-specific connectivity of the prefrontal cortex, together with a hyper-synchronous reorganization of connectivity among preSMA and motor regions. These results are supported by preclinical evidence of the selectivity of frontotemporal lobar degeneration on oscillatory dynamics, and provide a clinically relevant yet precise neurophysiological signature of behavioural control as a potential pharmacological target for early phase experimental medicines studies.

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Neurocognitive modeling of latent memory processes reveals reorganization of hippocampal-cortical circuits underlying learning and efficient strategies.

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