Cargando…

Frontal cortex tracks surprise separately for different sensory modalities but engages a common inhibitory control mechanism

The brain constantly generates predictions about the environment to guide action. Unexpected events lead to surprise and can necessitate the modification of ongoing behavior. Surprise can occur for any sensory domain, but it is not clear how these separate surprise signals are integrated to affect m...

Descripción completa

Detalles Bibliográficos
Autores principales: Wessel, Jan R., Huber, David E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6687204/
https://www.ncbi.nlm.nih.gov/pubmed/31356593
http://dx.doi.org/10.1371/journal.pcbi.1006927
_version_ 1783442699964121088
author Wessel, Jan R.
Huber, David E.
author_facet Wessel, Jan R.
Huber, David E.
author_sort Wessel, Jan R.
collection PubMed
description The brain constantly generates predictions about the environment to guide action. Unexpected events lead to surprise and can necessitate the modification of ongoing behavior. Surprise can occur for any sensory domain, but it is not clear how these separate surprise signals are integrated to affect motor output. By applying a trial-to-trial Bayesian surprise model to human electroencephalography data recorded during a cross-modal oddball task, we tested whether there are separate predictive models for different sensory modalities (visual, auditory), or whether expectations are integrated across modalities such that surprise in one modality decreases surprise for a subsequent unexpected event in the other modality. We found that while surprise was represented in a common frontal signature across sensory modalities (the fronto-central P3 event-related potential), the single-trial amplitudes of this signature more closely conformed to a model with separate surprise terms for each sensory domain. We then investigated whether surprise-related fronto-central P3 activity indexes the rapid inhibitory control of ongoing behavior after surprise, as suggested by recent theories. Confirming this prediction, the fronto-central P3 amplitude after both auditory and visual unexpected events was highly correlated with the fronto-central P3 found after stop-signals (measured in a separate stop-signal task). Moreover, surprise-related and stopping-related activity loaded onto the same component in a cross-task independent components analysis. Together, these findings suggest that medial frontal cortex maintains separate predictive models for different sensory domains, but engages a common mechanism for inhibitory control of behavior regardless of the source of surprise.
format Online
Article
Text
id pubmed-6687204
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-66872042019-08-15 Frontal cortex tracks surprise separately for different sensory modalities but engages a common inhibitory control mechanism Wessel, Jan R. Huber, David E. PLoS Comput Biol Research Article The brain constantly generates predictions about the environment to guide action. Unexpected events lead to surprise and can necessitate the modification of ongoing behavior. Surprise can occur for any sensory domain, but it is not clear how these separate surprise signals are integrated to affect motor output. By applying a trial-to-trial Bayesian surprise model to human electroencephalography data recorded during a cross-modal oddball task, we tested whether there are separate predictive models for different sensory modalities (visual, auditory), or whether expectations are integrated across modalities such that surprise in one modality decreases surprise for a subsequent unexpected event in the other modality. We found that while surprise was represented in a common frontal signature across sensory modalities (the fronto-central P3 event-related potential), the single-trial amplitudes of this signature more closely conformed to a model with separate surprise terms for each sensory domain. We then investigated whether surprise-related fronto-central P3 activity indexes the rapid inhibitory control of ongoing behavior after surprise, as suggested by recent theories. Confirming this prediction, the fronto-central P3 amplitude after both auditory and visual unexpected events was highly correlated with the fronto-central P3 found after stop-signals (measured in a separate stop-signal task). Moreover, surprise-related and stopping-related activity loaded onto the same component in a cross-task independent components analysis. Together, these findings suggest that medial frontal cortex maintains separate predictive models for different sensory domains, but engages a common mechanism for inhibitory control of behavior regardless of the source of surprise. Public Library of Science 2019-07-29 /pmc/articles/PMC6687204/ /pubmed/31356593 http://dx.doi.org/10.1371/journal.pcbi.1006927 Text en © 2019 Wessel, Huber http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Wessel, Jan R.
Huber, David E.
Frontal cortex tracks surprise separately for different sensory modalities but engages a common inhibitory control mechanism
title Frontal cortex tracks surprise separately for different sensory modalities but engages a common inhibitory control mechanism
title_full Frontal cortex tracks surprise separately for different sensory modalities but engages a common inhibitory control mechanism
title_fullStr Frontal cortex tracks surprise separately for different sensory modalities but engages a common inhibitory control mechanism
title_full_unstemmed Frontal cortex tracks surprise separately for different sensory modalities but engages a common inhibitory control mechanism
title_short Frontal cortex tracks surprise separately for different sensory modalities but engages a common inhibitory control mechanism
title_sort frontal cortex tracks surprise separately for different sensory modalities but engages a common inhibitory control mechanism
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6687204/
https://www.ncbi.nlm.nih.gov/pubmed/31356593
http://dx.doi.org/10.1371/journal.pcbi.1006927
work_keys_str_mv AT wesseljanr frontalcortextrackssurpriseseparatelyfordifferentsensorymodalitiesbutengagesacommoninhibitorycontrolmechanism
AT huberdavide frontalcortextrackssurpriseseparatelyfordifferentsensorymodalitiesbutengagesacommoninhibitorycontrolmechanism