Intrinsic dynamic shapes responses to external stimulation in the human brain

Sensory stimulation of the brain reverberates in its recurrent neural networks. However, current computational models of brain activity do not separate immediate sensory responses from this intrinsic dynamic. We apply a vector-autoregressive model with external input (VARX), combining the concepts o...

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Main Authors: Maximilian Nentwich, Marcin Leszczynski, Charles E Schroeder, Stephan Bickel, Lucas C Parra
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2025-07-01
Series:eLife
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Online Access:https://elifesciences.org/articles/104996
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author Maximilian Nentwich
Marcin Leszczynski
Charles E Schroeder
Stephan Bickel
Lucas C Parra
author_facet Maximilian Nentwich
Marcin Leszczynski
Charles E Schroeder
Stephan Bickel
Lucas C Parra
author_sort Maximilian Nentwich
collection DOAJ
description Sensory stimulation of the brain reverberates in its recurrent neural networks. However, current computational models of brain activity do not separate immediate sensory responses from this intrinsic dynamic. We apply a vector-autoregressive model with external input (VARX), combining the concepts of ‘functional connectivity’ and ‘encoding models’, to intracranial recordings in humans. This model captures the extrinsic effect of the stimulus and separates that from the intrinsic effect of the recurrent brain dynamic. We find that the intrinsic dynamic enhances and prolongs the neural responses to scene cuts, eye movements, and sounds. Failing to account for these extrinsic inputs leads to spurious recurrent connections that govern the intrinsic dynamic. We also find that the recurrent connectivity during rest is reduced during movie watching. The model shows that an external stimulus can reduce intrinsic noise. It also shows that sensory areas have mostly outward, whereas higher-order brain areas have mostly incoming connections. We conclude that the response to an external audiovisual stimulus can largely be attributed to the intrinsic dynamic of the brain, already observed during rest.
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spelling doaj-art-fa1bd305e7b34823b0d619269e9f3ab22025-08-20T03:15:27ZengeLife Sciences Publications LtdeLife2050-084X2025-07-011410.7554/eLife.104996Intrinsic dynamic shapes responses to external stimulation in the human brainMaximilian Nentwich0https://orcid.org/0000-0002-9306-7591Marcin Leszczynski1https://orcid.org/0000-0003-3172-4661Charles E Schroeder2Stephan Bickel3Lucas C Parra4https://orcid.org/0000-0003-4667-816XThe Feinstein Institutes for Medical Research, Northwell Health, Manhasset, United StatesDepartments of Psychiatry and Neurology, Columbia University College of Physicians and Surgeons, New York, United States; Translational Neuroscience Lab Division, Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute, Orangeburg, United States; Cognitive Science Department, Institute of Philosophy, Jagiellonian University, Kraków, PolandDepartments of Psychiatry and Neurology, Columbia University College of Physicians and Surgeons, New York, United States; Translational Neuroscience Lab Division, Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute, Orangeburg, United StatesThe Feinstein Institutes for Medical Research, Northwell Health, Manhasset, United States; Translational Neuroscience Lab Division, Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute, Orangeburg, United States; Departments of Neurology and Neurosurgery, Zucker School of Medicine at Hofstra/Northwell, Hempstead, United StatesDepartment of Biomedical Engineering, The City College of New York, New York, United StatesSensory stimulation of the brain reverberates in its recurrent neural networks. However, current computational models of brain activity do not separate immediate sensory responses from this intrinsic dynamic. We apply a vector-autoregressive model with external input (VARX), combining the concepts of ‘functional connectivity’ and ‘encoding models’, to intracranial recordings in humans. This model captures the extrinsic effect of the stimulus and separates that from the intrinsic effect of the recurrent brain dynamic. We find that the intrinsic dynamic enhances and prolongs the neural responses to scene cuts, eye movements, and sounds. Failing to account for these extrinsic inputs leads to spurious recurrent connections that govern the intrinsic dynamic. We also find that the recurrent connectivity during rest is reduced during movie watching. The model shows that an external stimulus can reduce intrinsic noise. It also shows that sensory areas have mostly outward, whereas higher-order brain areas have mostly incoming connections. We conclude that the response to an external audiovisual stimulus can largely be attributed to the intrinsic dynamic of the brain, already observed during rest.https://elifesciences.org/articles/104996connectivitygranger analysisencoding modelsrecurrent networksintracranial EEGnaturalistic
spellingShingle Maximilian Nentwich
Marcin Leszczynski
Charles E Schroeder
Stephan Bickel
Lucas C Parra
Intrinsic dynamic shapes responses to external stimulation in the human brain
eLife
connectivity
granger analysis
encoding models
recurrent networks
intracranial EEG
naturalistic
title Intrinsic dynamic shapes responses to external stimulation in the human brain
title_full Intrinsic dynamic shapes responses to external stimulation in the human brain
title_fullStr Intrinsic dynamic shapes responses to external stimulation in the human brain
title_full_unstemmed Intrinsic dynamic shapes responses to external stimulation in the human brain
title_short Intrinsic dynamic shapes responses to external stimulation in the human brain
title_sort intrinsic dynamic shapes responses to external stimulation in the human brain
topic connectivity
granger analysis
encoding models
recurrent networks
intracranial EEG
naturalistic
url https://elifesciences.org/articles/104996
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AT marcinleszczynski intrinsicdynamicshapesresponsestoexternalstimulationinthehumanbrain
AT charleseschroeder intrinsicdynamicshapesresponsestoexternalstimulationinthehumanbrain
AT stephanbickel intrinsicdynamicshapesresponsestoexternalstimulationinthehumanbrain
AT lucascparra intrinsicdynamicshapesresponsestoexternalstimulationinthehumanbrain