The brain in (Willed) action

A meta-analytical comparison of imaging studies on motor intentionality and sense of agency

Silvia Seghezzi, Eleonora Zirone, Eraldo Paulesu, Laura Zapparoli

Research output: Contribution to journalArticle

Abstract

Voluntary actions can be fractionated in different phenomena: from the emergence of intentions and the ensuing motor plans and actions, to the anticipation and monitoring of their outcomes, to the appreciation of their congruency with intentions and to the eventual emergence of a sense of agency. It follows that motor intention and the sense of agency should occur at different stages in the normal generation of willed actions. Both these processes have been associated with a fronto-parietal motor network, but no study has investigated to what extent the two experiences can be dissociated for the brain regions involved. To this end, we assessed the PET/fMRI literature on agency and intentionality using a meta-analytic technique based on a hierarchical clustering algorithm. Beside a shared brain network involving the meso-frontal and prefrontal regions, the middle insula and subcortical structures, we found that motor intention and the sense of agency are functionally underpinned by separable sets of brain regions: an "intentionality network," involving the rostral area of the mesial frontal cortex (middle cingulum and pre-supplementary motor area), the anterior insula and the parietal lobules, and a "self-agency network," which involves the posterior areas of the mesial frontal cortex (the SMA proper), the posterior insula, the occipital lobe and the cerebellum. We were then able to confirm this functional organization by a subsequent seed-based fMRI resting-state functional connectivity analysis, with seeds derived from the intentionality/sense of agency specific clusters of the medial wall of the frontal lobe. Our results suggest the existence of a rostro-caudal gradient within the mesial frontal cortex, with the more anterior regions linked to the concept of motor intentionality and the brain areas located more posteriorly associated with the direct monitoring between the action and its outcome. This suggestion is reinforced by the association between the sense of agency and the activation of the occipital lobes, to suggest a direct comparison between the movement and its external (e.g., visual) consequences. The shared network may be important for the integration of intentionality and agency in a coherent appreciation of self-generated actions.

Original languageEnglish
Article number804
JournalFrontiers in Psychology
Volume10
DOIs
Publication statusPublished - Jan 1 2019

Fingerprint

Frontal Lobe
Occipital Lobe
Brain
Seeds
Magnetic Resonance Imaging
Parietal Lobe
Motor Cortex
Cerebellum
Cluster Analysis

Keywords

  • Action awareness
  • fMRI
  • Meta-analysis
  • Motor intention
  • PET
  • Sense of agency

ASJC Scopus subject areas

  • Psychology(all)

Cite this

The brain in (Willed) action : A meta-analytical comparison of imaging studies on motor intentionality and sense of agency. / Seghezzi, Silvia; Zirone, Eleonora; Paulesu, Eraldo; Zapparoli, Laura.

In: Frontiers in Psychology, Vol. 10, 804, 01.01.2019.

Research output: Contribution to journalArticle

@article{bc4032f57bed416cbddce04ee5563375,
title = "The brain in (Willed) action: A meta-analytical comparison of imaging studies on motor intentionality and sense of agency",
abstract = "Voluntary actions can be fractionated in different phenomena: from the emergence of intentions and the ensuing motor plans and actions, to the anticipation and monitoring of their outcomes, to the appreciation of their congruency with intentions and to the eventual emergence of a sense of agency. It follows that motor intention and the sense of agency should occur at different stages in the normal generation of willed actions. Both these processes have been associated with a fronto-parietal motor network, but no study has investigated to what extent the two experiences can be dissociated for the brain regions involved. To this end, we assessed the PET/fMRI literature on agency and intentionality using a meta-analytic technique based on a hierarchical clustering algorithm. Beside a shared brain network involving the meso-frontal and prefrontal regions, the middle insula and subcortical structures, we found that motor intention and the sense of agency are functionally underpinned by separable sets of brain regions: an {"}intentionality network,{"} involving the rostral area of the mesial frontal cortex (middle cingulum and pre-supplementary motor area), the anterior insula and the parietal lobules, and a {"}self-agency network,{"} which involves the posterior areas of the mesial frontal cortex (the SMA proper), the posterior insula, the occipital lobe and the cerebellum. We were then able to confirm this functional organization by a subsequent seed-based fMRI resting-state functional connectivity analysis, with seeds derived from the intentionality/sense of agency specific clusters of the medial wall of the frontal lobe. Our results suggest the existence of a rostro-caudal gradient within the mesial frontal cortex, with the more anterior regions linked to the concept of motor intentionality and the brain areas located more posteriorly associated with the direct monitoring between the action and its outcome. This suggestion is reinforced by the association between the sense of agency and the activation of the occipital lobes, to suggest a direct comparison between the movement and its external (e.g., visual) consequences. The shared network may be important for the integration of intentionality and agency in a coherent appreciation of self-generated actions.",
keywords = "Action awareness, fMRI, Meta-analysis, Motor intention, PET, Sense of agency",
author = "Silvia Seghezzi and Eleonora Zirone and Eraldo Paulesu and Laura Zapparoli",
year = "2019",
month = "1",
day = "1",
doi = "10.3389/fpsyg.2019.00804",
language = "English",
volume = "10",
journal = "Frontiers in Psychology",
issn = "1664-1078",
publisher = "Frontiers Media S.A.",

}

TY - JOUR

T1 - The brain in (Willed) action

T2 - A meta-analytical comparison of imaging studies on motor intentionality and sense of agency

AU - Seghezzi, Silvia

AU - Zirone, Eleonora

AU - Paulesu, Eraldo

AU - Zapparoli, Laura

PY - 2019/1/1

Y1 - 2019/1/1

N2 - Voluntary actions can be fractionated in different phenomena: from the emergence of intentions and the ensuing motor plans and actions, to the anticipation and monitoring of their outcomes, to the appreciation of their congruency with intentions and to the eventual emergence of a sense of agency. It follows that motor intention and the sense of agency should occur at different stages in the normal generation of willed actions. Both these processes have been associated with a fronto-parietal motor network, but no study has investigated to what extent the two experiences can be dissociated for the brain regions involved. To this end, we assessed the PET/fMRI literature on agency and intentionality using a meta-analytic technique based on a hierarchical clustering algorithm. Beside a shared brain network involving the meso-frontal and prefrontal regions, the middle insula and subcortical structures, we found that motor intention and the sense of agency are functionally underpinned by separable sets of brain regions: an "intentionality network," involving the rostral area of the mesial frontal cortex (middle cingulum and pre-supplementary motor area), the anterior insula and the parietal lobules, and a "self-agency network," which involves the posterior areas of the mesial frontal cortex (the SMA proper), the posterior insula, the occipital lobe and the cerebellum. We were then able to confirm this functional organization by a subsequent seed-based fMRI resting-state functional connectivity analysis, with seeds derived from the intentionality/sense of agency specific clusters of the medial wall of the frontal lobe. Our results suggest the existence of a rostro-caudal gradient within the mesial frontal cortex, with the more anterior regions linked to the concept of motor intentionality and the brain areas located more posteriorly associated with the direct monitoring between the action and its outcome. This suggestion is reinforced by the association between the sense of agency and the activation of the occipital lobes, to suggest a direct comparison between the movement and its external (e.g., visual) consequences. The shared network may be important for the integration of intentionality and agency in a coherent appreciation of self-generated actions.

AB - Voluntary actions can be fractionated in different phenomena: from the emergence of intentions and the ensuing motor plans and actions, to the anticipation and monitoring of their outcomes, to the appreciation of their congruency with intentions and to the eventual emergence of a sense of agency. It follows that motor intention and the sense of agency should occur at different stages in the normal generation of willed actions. Both these processes have been associated with a fronto-parietal motor network, but no study has investigated to what extent the two experiences can be dissociated for the brain regions involved. To this end, we assessed the PET/fMRI literature on agency and intentionality using a meta-analytic technique based on a hierarchical clustering algorithm. Beside a shared brain network involving the meso-frontal and prefrontal regions, the middle insula and subcortical structures, we found that motor intention and the sense of agency are functionally underpinned by separable sets of brain regions: an "intentionality network," involving the rostral area of the mesial frontal cortex (middle cingulum and pre-supplementary motor area), the anterior insula and the parietal lobules, and a "self-agency network," which involves the posterior areas of the mesial frontal cortex (the SMA proper), the posterior insula, the occipital lobe and the cerebellum. We were then able to confirm this functional organization by a subsequent seed-based fMRI resting-state functional connectivity analysis, with seeds derived from the intentionality/sense of agency specific clusters of the medial wall of the frontal lobe. Our results suggest the existence of a rostro-caudal gradient within the mesial frontal cortex, with the more anterior regions linked to the concept of motor intentionality and the brain areas located more posteriorly associated with the direct monitoring between the action and its outcome. This suggestion is reinforced by the association between the sense of agency and the activation of the occipital lobes, to suggest a direct comparison between the movement and its external (e.g., visual) consequences. The shared network may be important for the integration of intentionality and agency in a coherent appreciation of self-generated actions.

KW - Action awareness

KW - fMRI

KW - Meta-analysis

KW - Motor intention

KW - PET

KW - Sense of agency

UR - http://www.scopus.com/inward/record.url?scp=85064496785&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85064496785&partnerID=8YFLogxK

U2 - 10.3389/fpsyg.2019.00804

DO - 10.3389/fpsyg.2019.00804

M3 - Article

VL - 10

JO - Frontiers in Psychology

JF - Frontiers in Psychology

SN - 1664-1078

M1 - 804

ER -