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Causal explanation of individual differences in human sensorimotor memory formation

View ORCID ProfilePierre Petitet, Jill X. O’Reilly, Ana M. Gonçalves, Piergiorgio Salvan, Shigeru Kitazawa, Heidi Johansen-Berg, View ORCID ProfileJacinta O’Shea
doi: https://doi.org/10.1101/255091
Pierre Petitet
1Wellcome Centre for Integrative Neuroimaging (WIN), Oxford Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences (NDCN), University of Oxford, John Radcliffe Hospital, Headington, Oxford, U.K.
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Jill X. O’Reilly
1Wellcome Centre for Integrative Neuroimaging (WIN), Oxford Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences (NDCN), University of Oxford, John Radcliffe Hospital, Headington, Oxford, U.K.
2Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, Netherlands
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Ana M. Gonçalves
1Wellcome Centre for Integrative Neuroimaging (WIN), Oxford Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences (NDCN), University of Oxford, John Radcliffe Hospital, Headington, Oxford, U.K.
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Piergiorgio Salvan
1Wellcome Centre for Integrative Neuroimaging (WIN), Oxford Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences (NDCN), University of Oxford, John Radcliffe Hospital, Headington, Oxford, U.K.
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Shigeru Kitazawa
3Dynamic Brain Network Laboratory, Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan
4Department of Brain Physiology, Graduate School of Medicine, Osaka University, Osaka, Japan
5Center for Information and Neural Networks, Osaka University, Osaka, Japan
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Heidi Johansen-Berg
1Wellcome Centre for Integrative Neuroimaging (WIN), Oxford Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences (NDCN), University of Oxford, John Radcliffe Hospital, Headington, Oxford, U.K.
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Jacinta O’Shea
1Wellcome Centre for Integrative Neuroimaging (WIN), Oxford Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences (NDCN), University of Oxford, John Radcliffe Hospital, Headington, Oxford, U.K.
2Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, Netherlands
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Abstract

Sensorimotor cortex mediates the formation of adaptation memory. Individuals differ in the rate at which they acquire, retain, and generalize adaptation. We present a mechanistic explanation of the neurochemical and computational causes of this variation in humans. Neuroimaging identified structural, functional and neurochemical covariates of a computational parameter that determines memory persistence. To establish causality, we increased sensorimotor cortex excitability during adaptation, using transcranial direct current stimulation. As predicted, this increased retention. Inter-individual variance in the stimulation-induced E:I increase predicted the computational change, which predicted the memory gain. These relations did not hold, and memory was unchanged, with stimulation applied before adaptation. This cognitive state dependent effect was modulated by the BDNF val66met genetic polymorphism. Memory was enhanced by stimulation in Val/Val carriers only, implicating a mechanistic role for activity-dependent BDNF secretion. Sensorimotor cortex E:I causally determines the time constant of memory persistence, explaining phenotypic variation in adaptation decay.

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Posted January 29, 2018.
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Causal explanation of individual differences in human sensorimotor memory formation
Pierre Petitet, Jill X. O’Reilly, Ana M. Gonçalves, Piergiorgio Salvan, Shigeru Kitazawa, Heidi Johansen-Berg, Jacinta O’Shea
bioRxiv 255091; doi: https://doi.org/10.1101/255091
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Causal explanation of individual differences in human sensorimotor memory formation
Pierre Petitet, Jill X. O’Reilly, Ana M. Gonçalves, Piergiorgio Salvan, Shigeru Kitazawa, Heidi Johansen-Berg, Jacinta O’Shea
bioRxiv 255091; doi: https://doi.org/10.1101/255091

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