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Stable readout of observed actions from format-dependent activity of monkey’s anterior intraparietal neurons

Humans accurately identify observed actions despite large dynamic changes in their retinal images and a variety of visual presentation formats. A large network of brain regions in primates participates in the processing of others’ actions, with the anterior intraparietal area (AIP) playing a major r...

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Autores principales: Lanzilotto, Marco, Maranesi, Monica, Livi, Alessandro, Ferroni, Carolina Giulia, Orban, Guy A., Bonini, Luca
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7369316/
https://www.ncbi.nlm.nih.gov/pubmed/32581128
http://dx.doi.org/10.1073/pnas.2007018117
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author Lanzilotto, Marco
Maranesi, Monica
Livi, Alessandro
Ferroni, Carolina Giulia
Orban, Guy A.
Bonini, Luca
author_facet Lanzilotto, Marco
Maranesi, Monica
Livi, Alessandro
Ferroni, Carolina Giulia
Orban, Guy A.
Bonini, Luca
author_sort Lanzilotto, Marco
collection PubMed
description Humans accurately identify observed actions despite large dynamic changes in their retinal images and a variety of visual presentation formats. A large network of brain regions in primates participates in the processing of others’ actions, with the anterior intraparietal area (AIP) playing a major role in routing information about observed manipulative actions (OMAs) to the other nodes of the network. This study investigated whether the AIP also contributes to invariant coding of OMAs across different visual formats. We recorded AIP neuronal activity from two macaques while they observed videos portraying seven manipulative actions (drag, drop, grasp, push, roll, rotate, squeeze) in four visual formats. Each format resulted from the combination of two actor’s body postures (standing, sitting) and two viewpoints (lateral, frontal). Out of 297 recorded units, 38% were OMA-selective in at least one format. Robust population code for viewpoint and actor’s body posture emerged shortly after stimulus presentation, followed by OMA selectivity. Although we found no fully invariant OMA-selective neuron, we discovered a population code that allowed us to classify action exemplars irrespective of the visual format. This code depends on a multiplicative mixing of signals about OMA identity and visual format, particularly evidenced by a set of units maintaining a relatively stable OMA selectivity across formats despite considerable rescaling of their firing rate depending on the visual specificities of each format. These findings suggest that the AIP integrates format-dependent information and the visual features of others’ actions, leading to a stable readout of observed manipulative action identity.
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spelling pubmed-73693162020-07-29 Stable readout of observed actions from format-dependent activity of monkey’s anterior intraparietal neurons Lanzilotto, Marco Maranesi, Monica Livi, Alessandro Ferroni, Carolina Giulia Orban, Guy A. Bonini, Luca Proc Natl Acad Sci U S A Biological Sciences Humans accurately identify observed actions despite large dynamic changes in their retinal images and a variety of visual presentation formats. A large network of brain regions in primates participates in the processing of others’ actions, with the anterior intraparietal area (AIP) playing a major role in routing information about observed manipulative actions (OMAs) to the other nodes of the network. This study investigated whether the AIP also contributes to invariant coding of OMAs across different visual formats. We recorded AIP neuronal activity from two macaques while they observed videos portraying seven manipulative actions (drag, drop, grasp, push, roll, rotate, squeeze) in four visual formats. Each format resulted from the combination of two actor’s body postures (standing, sitting) and two viewpoints (lateral, frontal). Out of 297 recorded units, 38% were OMA-selective in at least one format. Robust population code for viewpoint and actor’s body posture emerged shortly after stimulus presentation, followed by OMA selectivity. Although we found no fully invariant OMA-selective neuron, we discovered a population code that allowed us to classify action exemplars irrespective of the visual format. This code depends on a multiplicative mixing of signals about OMA identity and visual format, particularly evidenced by a set of units maintaining a relatively stable OMA selectivity across formats despite considerable rescaling of their firing rate depending on the visual specificities of each format. These findings suggest that the AIP integrates format-dependent information and the visual features of others’ actions, leading to a stable readout of observed manipulative action identity. National Academy of Sciences 2020-07-14 2020-06-24 /pmc/articles/PMC7369316/ /pubmed/32581128 http://dx.doi.org/10.1073/pnas.2007018117 Text en Copyright © 2020 the Author(s). Published by PNAS. http://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Lanzilotto, Marco
Maranesi, Monica
Livi, Alessandro
Ferroni, Carolina Giulia
Orban, Guy A.
Bonini, Luca
Stable readout of observed actions from format-dependent activity of monkey’s anterior intraparietal neurons
title Stable readout of observed actions from format-dependent activity of monkey’s anterior intraparietal neurons
title_full Stable readout of observed actions from format-dependent activity of monkey’s anterior intraparietal neurons
title_fullStr Stable readout of observed actions from format-dependent activity of monkey’s anterior intraparietal neurons
title_full_unstemmed Stable readout of observed actions from format-dependent activity of monkey’s anterior intraparietal neurons
title_short Stable readout of observed actions from format-dependent activity of monkey’s anterior intraparietal neurons
title_sort stable readout of observed actions from format-dependent activity of monkey’s anterior intraparietal neurons
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7369316/
https://www.ncbi.nlm.nih.gov/pubmed/32581128
http://dx.doi.org/10.1073/pnas.2007018117
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