Spatial and Temporal Distribution of Information Processing in the Human Dorsal Anterior Cingulate Cortex
The dorsal anterior cingulate cortex (dACC) is a key node in the human salience network. It has been ascribed motor, pain-processing and affective functions. However, the dynamics of information flow in this complex region and how it responds to inputs remain unclear and are difficult to study using...
Main Authors: | , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2022-03-01
|
Series: | Frontiers in Human Neuroscience |
Subjects: | |
Online Access: | https://www.frontiersin.org/articles/10.3389/fnhum.2022.780047/full |
_version_ | 1818156088188469248 |
---|---|
author | Conor Keogh Alceste Deli Amir Puyan Divanbeighi Zand Mark Jernej Zorman Sandra G. Boccard-Binet Matthew Parrott Charalampos Sigalas Alexander R. Weiss John Frederick Stein James J. FitzGerald Tipu Z. Aziz Alexander L. Green Martin John Gillies |
author_facet | Conor Keogh Alceste Deli Amir Puyan Divanbeighi Zand Mark Jernej Zorman Sandra G. Boccard-Binet Matthew Parrott Charalampos Sigalas Alexander R. Weiss John Frederick Stein James J. FitzGerald Tipu Z. Aziz Alexander L. Green Martin John Gillies |
author_sort | Conor Keogh |
collection | DOAJ |
description | The dorsal anterior cingulate cortex (dACC) is a key node in the human salience network. It has been ascribed motor, pain-processing and affective functions. However, the dynamics of information flow in this complex region and how it responds to inputs remain unclear and are difficult to study using non-invasive electrophysiology. The area is targeted by neurosurgery to treat neuropathic pain. During deep brain stimulation surgery, we recorded local field potentials from this region in humans during a decision-making task requiring motor output. We investigated the spatial and temporal distribution of information flow within the dACC. We demonstrate the existence of a distributed network within the anterior cingulate cortex where discrete nodes demonstrate directed communication following inputs. We show that this network anticipates and responds to the valence of feedback to actions. We further show that these network dynamics adapt following learning. Our results provide evidence for the integration of learning and the response to feedback in a key cognitive region. |
first_indexed | 2024-12-11T14:52:44Z |
format | Article |
id | doaj.art-7a7b7b60d2fc40f7971ca41a8b9b79fb |
institution | Directory Open Access Journal |
issn | 1662-5161 |
language | English |
last_indexed | 2024-12-11T14:52:44Z |
publishDate | 2022-03-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Human Neuroscience |
spelling | doaj.art-7a7b7b60d2fc40f7971ca41a8b9b79fb2022-12-22T01:01:25ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612022-03-011610.3389/fnhum.2022.780047780047Spatial and Temporal Distribution of Information Processing in the Human Dorsal Anterior Cingulate CortexConor Keogh0Alceste Deli1Amir Puyan Divanbeighi Zand2Mark Jernej Zorman3Sandra G. Boccard-Binet4Matthew Parrott5Charalampos Sigalas6Alexander R. Weiss7John Frederick Stein8James J. FitzGerald9Tipu Z. Aziz10Alexander L. Green11Martin John Gillies12Nuffield Department of Surgical Sciences, University of Oxford, Oxford, United KingdomNuffield Department of Surgical Sciences, University of Oxford, Oxford, United KingdomNuffield Department of Surgical Sciences, University of Oxford, Oxford, United KingdomNuffield Department of Surgical Sciences, University of Oxford, Oxford, United KingdomNuffield Department of Surgical Sciences, University of Oxford, Oxford, United KingdomSt Hilda’s College, University of Oxford, Oxford, United KingdomDepartment of Pharmacology, University of Oxford, Oxford, United KingdomDepartment of Neurology, Johns Hopkins University, Baltimore, MD, United StatesDepartment of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United KingdomNuffield Department of Surgical Sciences, University of Oxford, Oxford, United KingdomNuffield Department of Surgical Sciences, University of Oxford, Oxford, United KingdomNuffield Department of Surgical Sciences, University of Oxford, Oxford, United KingdomNuffield Department of Surgical Sciences, University of Oxford, Oxford, United KingdomThe dorsal anterior cingulate cortex (dACC) is a key node in the human salience network. It has been ascribed motor, pain-processing and affective functions. However, the dynamics of information flow in this complex region and how it responds to inputs remain unclear and are difficult to study using non-invasive electrophysiology. The area is targeted by neurosurgery to treat neuropathic pain. During deep brain stimulation surgery, we recorded local field potentials from this region in humans during a decision-making task requiring motor output. We investigated the spatial and temporal distribution of information flow within the dACC. We demonstrate the existence of a distributed network within the anterior cingulate cortex where discrete nodes demonstrate directed communication following inputs. We show that this network anticipates and responds to the valence of feedback to actions. We further show that these network dynamics adapt following learning. Our results provide evidence for the integration of learning and the response to feedback in a key cognitive region.https://www.frontiersin.org/articles/10.3389/fnhum.2022.780047/fullhuman cortexelectrophysiologydecision makinginformation theoryerror |
spellingShingle | Conor Keogh Alceste Deli Amir Puyan Divanbeighi Zand Mark Jernej Zorman Sandra G. Boccard-Binet Matthew Parrott Charalampos Sigalas Alexander R. Weiss John Frederick Stein James J. FitzGerald Tipu Z. Aziz Alexander L. Green Martin John Gillies Spatial and Temporal Distribution of Information Processing in the Human Dorsal Anterior Cingulate Cortex Frontiers in Human Neuroscience human cortex electrophysiology decision making information theory error |
title | Spatial and Temporal Distribution of Information Processing in the Human Dorsal Anterior Cingulate Cortex |
title_full | Spatial and Temporal Distribution of Information Processing in the Human Dorsal Anterior Cingulate Cortex |
title_fullStr | Spatial and Temporal Distribution of Information Processing in the Human Dorsal Anterior Cingulate Cortex |
title_full_unstemmed | Spatial and Temporal Distribution of Information Processing in the Human Dorsal Anterior Cingulate Cortex |
title_short | Spatial and Temporal Distribution of Information Processing in the Human Dorsal Anterior Cingulate Cortex |
title_sort | spatial and temporal distribution of information processing in the human dorsal anterior cingulate cortex |
topic | human cortex electrophysiology decision making information theory error |
url | https://www.frontiersin.org/articles/10.3389/fnhum.2022.780047/full |
work_keys_str_mv | AT conorkeogh spatialandtemporaldistributionofinformationprocessinginthehumandorsalanteriorcingulatecortex AT alcestedeli spatialandtemporaldistributionofinformationprocessinginthehumandorsalanteriorcingulatecortex AT amirpuyandivanbeighizand spatialandtemporaldistributionofinformationprocessinginthehumandorsalanteriorcingulatecortex AT markjernejzorman spatialandtemporaldistributionofinformationprocessinginthehumandorsalanteriorcingulatecortex AT sandragboccardbinet spatialandtemporaldistributionofinformationprocessinginthehumandorsalanteriorcingulatecortex AT matthewparrott spatialandtemporaldistributionofinformationprocessinginthehumandorsalanteriorcingulatecortex AT charalampossigalas spatialandtemporaldistributionofinformationprocessinginthehumandorsalanteriorcingulatecortex AT alexanderrweiss spatialandtemporaldistributionofinformationprocessinginthehumandorsalanteriorcingulatecortex AT johnfrederickstein spatialandtemporaldistributionofinformationprocessinginthehumandorsalanteriorcingulatecortex AT jamesjfitzgerald spatialandtemporaldistributionofinformationprocessinginthehumandorsalanteriorcingulatecortex AT tipuzaziz spatialandtemporaldistributionofinformationprocessinginthehumandorsalanteriorcingulatecortex AT alexanderlgreen spatialandtemporaldistributionofinformationprocessinginthehumandorsalanteriorcingulatecortex AT martinjohngillies spatialandtemporaldistributionofinformationprocessinginthehumandorsalanteriorcingulatecortex |