Activity in ventral premotor cortex is modulated by vision of own hand in action

Parietal and premotor cortices of the macaque monkey contain distinct populations of neurons which, in addition to their motor discharge, are also activated by visual stimulation. Among these visuomotor neurons, a population of grasping neurons located in the anterior intraparietal area (AIP) shows...

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Main Authors: Luciano Fadiga, Luana Caselli, Laila Craighero, Benno Gesierich, Andriy Oliynyk, Banty Tia, Riccardo Viaro
Format: Article
Language:English
Published: PeerJ Inc. 2013-07-01
Series:PeerJ
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Online Access:https://peerj.com/articles/88.pdf
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author Luciano Fadiga
Luana Caselli
Laila Craighero
Benno Gesierich
Andriy Oliynyk
Banty Tia
Riccardo Viaro
author_facet Luciano Fadiga
Luana Caselli
Laila Craighero
Benno Gesierich
Andriy Oliynyk
Banty Tia
Riccardo Viaro
author_sort Luciano Fadiga
collection DOAJ
description Parietal and premotor cortices of the macaque monkey contain distinct populations of neurons which, in addition to their motor discharge, are also activated by visual stimulation. Among these visuomotor neurons, a population of grasping neurons located in the anterior intraparietal area (AIP) shows discharge modulation when the own hand is visible during object grasping. Given the dense connections between AIP and inferior frontal regions, we aimed at investigating whether two hand-related frontal areas, ventral premotor area F5 and primary motor cortex (area F1), contain neurons with similar properties. Two macaques were involved in a grasping task executed in various light/dark conditions in which the to-be-grasped object was kept visible by a dim retro-illumination. Approximately 62% of F5 and 55% of F1 motor neurons showed light/dark modulations. To better isolate the effect of hand-related visual input, we introduced two further conditions characterized by kinematic features similar to the dark condition. The scene was briefly illuminated (i) during hand preshaping (pre-touch flash, PT-flash) and (ii) at hand-object contact (touch flash, T-flash). Approximately 48% of F5 and 44% of F1 motor neurons showed a flash-related modulation. Considering flash-modulated neurons in the two flash conditions, ∼40% from F5 and ∼52% from F1 showed stronger activity in PT- than T-flash (PT-flash-dominant), whereas ∼60% from F5 and ∼48% from F1 showed stronger activity in T- than PT-flash (T-flash-dominant). Furthermore, F5, but not F1, flash-dominant neurons were characterized by a higher peak and mean discharge in the preferred flash condition as compared to light and dark conditions. Still considering F5, the distribution of the time of peak discharge was similar in light and preferred flash conditions. This study shows that the frontal cortex contains neurons, previously classified as motor neurons, which are sensitive to the observation of meaningful phases of the own grasping action. We conclude by discussing the possible functional role of these populations.
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spelling doaj.art-3c1e3444584e4b789ae0f15343a5bfea2023-12-03T10:55:34ZengPeerJ Inc.PeerJ2167-83592013-07-011e8810.7717/peerj.8888Activity in ventral premotor cortex is modulated by vision of own hand in actionLuciano Fadiga0Luana Caselli1Laila Craighero2Benno Gesierich3Andriy Oliynyk4Banty Tia5Riccardo Viaro6Department of Biomedical and Specialty Surgical Sciences, Section of Human Physiology, University of Ferrara, Ferrara, ItalyDepartment of Biomedical and Specialty Surgical Sciences, Section of Human Physiology, University of Ferrara, Ferrara, ItalyDepartment of Biomedical and Specialty Surgical Sciences, Section of Human Physiology, University of Ferrara, Ferrara, ItalyDepartment of Biomedical and Specialty Surgical Sciences, Section of Human Physiology, University of Ferrara, Ferrara, ItalyDepartment of Biomedical and Specialty Surgical Sciences, Section of Human Physiology, University of Ferrara, Ferrara, ItalyDepartment of Robotics, Brain and Cognitive Sciences, Italian Institute of Technology, Genova, ItalyDepartment of Robotics, Brain and Cognitive Sciences, Italian Institute of Technology, Genova, ItalyParietal and premotor cortices of the macaque monkey contain distinct populations of neurons which, in addition to their motor discharge, are also activated by visual stimulation. Among these visuomotor neurons, a population of grasping neurons located in the anterior intraparietal area (AIP) shows discharge modulation when the own hand is visible during object grasping. Given the dense connections between AIP and inferior frontal regions, we aimed at investigating whether two hand-related frontal areas, ventral premotor area F5 and primary motor cortex (area F1), contain neurons with similar properties. Two macaques were involved in a grasping task executed in various light/dark conditions in which the to-be-grasped object was kept visible by a dim retro-illumination. Approximately 62% of F5 and 55% of F1 motor neurons showed light/dark modulations. To better isolate the effect of hand-related visual input, we introduced two further conditions characterized by kinematic features similar to the dark condition. The scene was briefly illuminated (i) during hand preshaping (pre-touch flash, PT-flash) and (ii) at hand-object contact (touch flash, T-flash). Approximately 48% of F5 and 44% of F1 motor neurons showed a flash-related modulation. Considering flash-modulated neurons in the two flash conditions, ∼40% from F5 and ∼52% from F1 showed stronger activity in PT- than T-flash (PT-flash-dominant), whereas ∼60% from F5 and ∼48% from F1 showed stronger activity in T- than PT-flash (T-flash-dominant). Furthermore, F5, but not F1, flash-dominant neurons were characterized by a higher peak and mean discharge in the preferred flash condition as compared to light and dark conditions. Still considering F5, the distribution of the time of peak discharge was similar in light and preferred flash conditions. This study shows that the frontal cortex contains neurons, previously classified as motor neurons, which are sensitive to the observation of meaningful phases of the own grasping action. We conclude by discussing the possible functional role of these populations.https://peerj.com/articles/88.pdfSingle-neuron recordingGraspingVisuomotorFrontal cortex
spellingShingle Luciano Fadiga
Luana Caselli
Laila Craighero
Benno Gesierich
Andriy Oliynyk
Banty Tia
Riccardo Viaro
Activity in ventral premotor cortex is modulated by vision of own hand in action
PeerJ
Single-neuron recording
Grasping
Visuomotor
Frontal cortex
title Activity in ventral premotor cortex is modulated by vision of own hand in action
title_full Activity in ventral premotor cortex is modulated by vision of own hand in action
title_fullStr Activity in ventral premotor cortex is modulated by vision of own hand in action
title_full_unstemmed Activity in ventral premotor cortex is modulated by vision of own hand in action
title_short Activity in ventral premotor cortex is modulated by vision of own hand in action
title_sort activity in ventral premotor cortex is modulated by vision of own hand in action
topic Single-neuron recording
Grasping
Visuomotor
Frontal cortex
url https://peerj.com/articles/88.pdf
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