Neural networks for inhibitory function and error detection in younger and older adults for early detection of cognitive decline: a comparative study

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Abstract

Cognitive function can decline irreversibly with age, potentially progressing to dementia. Intervention during the preclinical stage is considered effective, but evaluation often requires large-scale equipment and tests. A decline in inhibitory function precedes and is involved in a general decline in higher-order brain functions, making its assessment a key target for early detection. We focused on error-related negativity (ERN) to capture the neural network of inhibitory function. While larger ERN amplitudes indicate higher error detection ability and correlate with inhibitory function, the causal relationship, mutual influences, and age-related effects in older adults remain unclear. This study measured brain activity during an inhibitory task in young and older adults to examine the neural networks related to error detection and inhibitory function. We used LORETA iCoh Full Vector Field analysis to verify directional connectivity. In the elderly group, during error responses, we observed significantly stronger beta-band directionality from the ventral anterior cingulate cortex (ACC) to the left frontal pole. Between the ventral and dorsal ACC, we also found significantly stronger directionality in the theta, alpha, and beta bands. During correct responses, they showed significantly stronger alpha and beta-band directionality from the left dorsolateral prefrontal cortex (DLPFC) to the right frontal pole. Compared to the elderly, the young group exhibited significantly stronger mutual directionality between the ventral and dorsal prefrontal cortices in the alpha and beta bands. They also showed widespread, significantly strong directionality among the ACC, bilateral DLPFC, and frontal poles. These results suggest that error detection ability is important for the normal functioning of inhibitory control in older adults. Furthermore, an age-related decline in metacognitive abilities may be associated with impaired inhibitory function. The insights from this study can contribute to developing risk prediction models for cognitive decline and establishing effective preventive strategies.
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Abstract Cognitive function can decline irreversibly with age, potentially progressing to dementia. Intervention during the preclinical stage is considered effective, but evaluation often requires large-scale equipment and tests. A decline in inhibitory function precedes and is involved in a general decline in higher-order brain functions, making its assessment a key target for early detection. We focused on error-related negativity (ERN) to capture the neural network of inhibitory function. While larger ERN amplitudes indicate higher error detection ability and correlate with inhibitory function, the causal relationship, mutual influences, and age-related effects in older adults remain unclear. This study measured brain activity during an inhibitory task in young and older adults to examine the neural networks related to error detection and inhibitory function. We used LORETA iCoh Full Vector Field analysis to verify directional connectivity. In the elderly group, during error responses, we observed significantly stronger beta-band directionality from the ventral anterior cingulate cortex (ACC) to the left frontal pole. Between the ventral and dorsal ACC, we also found significantly stronger directionality in the theta, alpha, and beta bands. During correct responses, they showed significantly stronger alpha and beta-band directionality from the left dorsolateral prefrontal cortex (DLPFC) to the right frontal pole. Compared to the elderly, the young group exhibited significantly stronger mutual directionality between the ventral and dorsal prefrontal cortices in the alpha and beta bands. They also showed widespread, significantly strong directionality among the ACC, bilateral DLPFC, and frontal poles. These results suggest that error detection ability is important for the normal functioning of inhibitory control in older adults. Furthermore, an age-related decline in metacognitive abilities may be associated with impaired inhibitory function. The insights from this study can contribute to developing risk prediction models for cognitive decline and establishing effective preventive strategies. Competing Interest Statement The authors have declared no competing interest. Funding Statement The author(s) received no specific funding for this work. Author Declarations I confirm all relevant ethical guidelines have been followed, and any necessary IRB and/or ethics committee approvals have been obtained. Yes The details of the IRB/oversight body that provided approval or exemption for the research described are given below: This study was conducted in accordance with the Declaration of Helsinki and was approved by the Research Ethics Committee of Kyoto Tachibana University (Approval No. 23-45). I confirm that all necessary patient/participant consent has been obtained and the appropriate institutional forms have been archived, and that any patient/participant/sample identifiers included were not known to anyone (e.g., hospital staff, patients or participants themselves) outside the research group so cannot be used to identify individuals. Yes I understand that all clinical trials and any other prospective interventional studies must be registered with an ICMJE-approved registry, such as ClinicalTrials.gov. I confirm that any such study reported in the manuscript has been registered and the trial registration ID is provided (note: if posting a prospective study registered retrospectively, please provide a statement in the trial ID field explaining why the study was not registered in advance). Yes I have followed all appropriate research reporting guidelines, such as any relevant EQUATOR Network research reporting checklist(s) and other pertinent material, if applicable. Yes Abbreviations - ACC - Anterior Cingulate Cortex - DLPFC - Dorsolateral Prefrontal Cortex - EEG - Electroencephalography - ERN - Error-Related Negativity - ERP - Event-Related Potentials - FPC - Frontal Polar Cortex - ICA - Independent Component Analysis - LORETA - Low-Resolution Electromagnetic Tomography - MCI - Mild Cognitive Impairment

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