Causal Evidence for the Multiple Demand Network in Change Detection: Auditory Mismatch Magnetoencephalography across Focal Neurodegenerative Diseases.

Autor:	Cope TE; Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0SZ, United Kingdom thomascope@gmail.com.; Cognition and Brain Sciences Unit, Medical Research Council, Cambridge CB2 7EF, United Kingdom.; Cambridge University Hospitals NHS Trust, Cambridge CB2 0SZ, United Kingdom., Hughes LE; Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0SZ, United Kingdom.; Cognition and Brain Sciences Unit, Medical Research Council, Cambridge CB2 7EF, United Kingdom., Phillips HN; Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0SZ, United Kingdom.; Cognition and Brain Sciences Unit, Medical Research Council, Cambridge CB2 7EF, United Kingdom.; Cambridge Centre for Ageing and Neuroscience (Cam-CAN), University of Cambridge, Cambridge CB2 7EF, United Kingdom., Adams NE; Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0SZ, United Kingdom., Jafarian A; Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0SZ, United Kingdom., Nesbitt D; Cognition and Brain Sciences Unit, Medical Research Council, Cambridge CB2 7EF, United Kingdom., Assem M; Cognition and Brain Sciences Unit, Medical Research Council, Cambridge CB2 7EF, United Kingdom., Woolgar A; Cognition and Brain Sciences Unit, Medical Research Council, Cambridge CB2 7EF, United Kingdom., Duncan J; Cognition and Brain Sciences Unit, Medical Research Council, Cambridge CB2 7EF, United Kingdom.; Cambridge Centre for Ageing and Neuroscience (Cam-CAN), University of Cambridge, Cambridge CB2 7EF, United Kingdom.; Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom., Rowe JB; Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0SZ, United Kingdom.; Cognition and Brain Sciences Unit, Medical Research Council, Cambridge CB2 7EF, United Kingdom.; Cambridge Centre for Ageing and Neuroscience (Cam-CAN), University of Cambridge, Cambridge CB2 7EF, United Kingdom.; Cambridge University Hospitals NHS Trust, Cambridge CB2 0SZ, United Kingdom.
Jazyk:	angličtina
Zdroj:	The Journal of neuroscience : the official journal of the Society for Neuroscience [J Neurosci] 2022 Apr 13; Vol. 42 (15), pp. 3197-3215. Date of Electronic Publication: 2022 Mar 08.
DOI:	10.1523/JNEUROSCI.1622-21.2022
Abstrakt:	The multiple demand (MD) system is a network of fronto-parietal brain regions active during the organization and control of diverse cognitive operations. It has been argued that this activation may be a nonspecific signal of task difficulty. However, here we provide convergent evidence for a causal role for the MD network in the "simple task" of automatic auditory change detection, through the impairment of top-down control mechanisms. We employ independent structure-function mapping, dynamic causal modeling (DCM), and frequency-resolved functional connectivity analyses of MRI and magnetoencephalography (MEG) from 75 mixed-sex human patients across four neurodegenerative syndromes [behavioral variant fronto-temporal dementia (bvFTD), nonfluent variant primary progressive aphasia (nfvPPA), posterior cortical atrophy (PCA), and Alzheimer's disease mild cognitive impairment with positive amyloid imaging (ADMCI)] and 48 age-matched controls. We show that atrophy of any MD node is sufficient to impair auditory neurophysiological response to change in frequency, location, intensity, continuity, or duration. There was no similar association with atrophy of the cingulo-opercular, salience or language networks, or with global atrophy. MD regions displayed increased functional but decreased effective connectivity as a function of neurodegeneration, suggesting partially effective compensation. Overall, we show that damage to any of the nodes of the MD network is sufficient to impair top-down control of sensation, providing a common mechanism for impaired change detection across dementia syndromes. SIGNIFICANCE STATEMENT Previous evidence for fronto-parietal networks controlling perception is largely associative and may be confounded by task difficulty. Here, we use a preattentive measure of automatic auditory change detection [mismatch negativity (MMN) magnetoencephalography (MEG)] to show that neurodegeneration in any frontal or parietal multiple demand (MD) node impairs primary auditory cortex (A1) neurophysiological response to change through top-down mechanisms. This explains why the impaired ability to respond to change is a core feature across dementias, and other conditions driven by brain network dysfunction, such as schizophrenia. It validates theoretical frameworks in which neurodegenerating networks upregulate connectivity as partially effective compensation. The significance extends beyond network science and dementia, in its construct validation of dynamic causal modeling (DCM), and human confirmation of frequency-resolved analyses of animal neurodegeneration models. (Copyright © 2022 Cope et al.)
Databáze:	MEDLINE
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