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Interdigitated Columnar Representation of Personal Space and Visual Space in Human Parietal Cortex

Personal space (PS) is the space around the body that people prefer to maintain between themselves and unfamiliar others. Intrusion into personal space evokes discomfort and an urge to move away. Physiologic studies in nonhuman primates suggest that defensive responses to intruding stimuli involve t...

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Autores principales: Tootell, Roger B.H., Nasiriavanaki, Zahra, Babadi, Baktash, Greve, Douglas N., Nasr, Shahin, Holt, Daphne J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9732835/
https://www.ncbi.nlm.nih.gov/pubmed/36198501
http://dx.doi.org/10.1523/JNEUROSCI.0516-22.2022
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author Tootell, Roger B.H.
Nasiriavanaki, Zahra
Babadi, Baktash
Greve, Douglas N.
Nasr, Shahin
Holt, Daphne J.
author_facet Tootell, Roger B.H.
Nasiriavanaki, Zahra
Babadi, Baktash
Greve, Douglas N.
Nasr, Shahin
Holt, Daphne J.
author_sort Tootell, Roger B.H.
collection PubMed
description Personal space (PS) is the space around the body that people prefer to maintain between themselves and unfamiliar others. Intrusion into personal space evokes discomfort and an urge to move away. Physiologic studies in nonhuman primates suggest that defensive responses to intruding stimuli involve the parietal cortex. We hypothesized that the spatial encoding of interpersonal distance is initially transformed from purely sensory to more egocentric mapping within human parietal cortex. This hypothesis was tested using 7 Tesla (7T) fMRI at high spatial resolution (1.1 mm isotropic), in seven subjects (four females, three males). In response to visual stimuli presented at a range of virtual distances, we found two categories of distance encoding in two corresponding radially-extending columns of activity within parietal cortex. One set of columns (P columns) responded selectively to moving and stationary face images presented at virtual distances that were nearer (but not farther) than each subject's behaviorally-defined personal space boundary. In most P columns, BOLD response amplitudes increased monotonically and nonlinearly with increasing virtual face proximity. In the remaining P columns, BOLD responses decreased with increasing proximity. A second set of parietal columns (D columns) responded selectively to disparity-based distance cues (near or far) in random dot stimuli, similar to disparity-selective columns described previously in occipital cortex. Critically, in parietal cortex, P columns were topographically interdigitated (nonoverlapping) with D columns. These results suggest that visual spatial information is transformed from visual to body-centered (or person-centered) dimensions in multiple local sites within human parietal cortex. SIGNIFICANCE STATEMENT Recent COVID-related social distancing practices highlight the need to better understand brain mechanisms which regulate “personal space” (PS), which is defined by the closest interpersonal distance that is comfortable for an individual. Using high spatial resolution brain imaging, we tested whether a map of external space is transformed from purely visual (3D-based) information to a more egocentric map (related to personal space) in human parietal cortex. We confirmed this transformation and further showed that it was mediated by two mutually segregated sets of columns: one which encoded interpersonal distance and another that encoded visual distance. These results suggest that the cortical transformation of sensory-centered to person-centered encoding of space near the body involves short-range communication across interdigitated columns within parietal cortex.
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spelling pubmed-97328352022-12-09 Interdigitated Columnar Representation of Personal Space and Visual Space in Human Parietal Cortex Tootell, Roger B.H. Nasiriavanaki, Zahra Babadi, Baktash Greve, Douglas N. Nasr, Shahin Holt, Daphne J. J Neurosci Research Articles Personal space (PS) is the space around the body that people prefer to maintain between themselves and unfamiliar others. Intrusion into personal space evokes discomfort and an urge to move away. Physiologic studies in nonhuman primates suggest that defensive responses to intruding stimuli involve the parietal cortex. We hypothesized that the spatial encoding of interpersonal distance is initially transformed from purely sensory to more egocentric mapping within human parietal cortex. This hypothesis was tested using 7 Tesla (7T) fMRI at high spatial resolution (1.1 mm isotropic), in seven subjects (four females, three males). In response to visual stimuli presented at a range of virtual distances, we found two categories of distance encoding in two corresponding radially-extending columns of activity within parietal cortex. One set of columns (P columns) responded selectively to moving and stationary face images presented at virtual distances that were nearer (but not farther) than each subject's behaviorally-defined personal space boundary. In most P columns, BOLD response amplitudes increased monotonically and nonlinearly with increasing virtual face proximity. In the remaining P columns, BOLD responses decreased with increasing proximity. A second set of parietal columns (D columns) responded selectively to disparity-based distance cues (near or far) in random dot stimuli, similar to disparity-selective columns described previously in occipital cortex. Critically, in parietal cortex, P columns were topographically interdigitated (nonoverlapping) with D columns. These results suggest that visual spatial information is transformed from visual to body-centered (or person-centered) dimensions in multiple local sites within human parietal cortex. SIGNIFICANCE STATEMENT Recent COVID-related social distancing practices highlight the need to better understand brain mechanisms which regulate “personal space” (PS), which is defined by the closest interpersonal distance that is comfortable for an individual. Using high spatial resolution brain imaging, we tested whether a map of external space is transformed from purely visual (3D-based) information to a more egocentric map (related to personal space) in human parietal cortex. We confirmed this transformation and further showed that it was mediated by two mutually segregated sets of columns: one which encoded interpersonal distance and another that encoded visual distance. These results suggest that the cortical transformation of sensory-centered to person-centered encoding of space near the body involves short-range communication across interdigitated columns within parietal cortex. Society for Neuroscience 2022-11-30 /pmc/articles/PMC9732835/ /pubmed/36198501 http://dx.doi.org/10.1523/JNEUROSCI.0516-22.2022 Text en Copyright © 2022 Tootell, Nasiriavanaki et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Tootell, Roger B.H.
Nasiriavanaki, Zahra
Babadi, Baktash
Greve, Douglas N.
Nasr, Shahin
Holt, Daphne J.
Interdigitated Columnar Representation of Personal Space and Visual Space in Human Parietal Cortex
title Interdigitated Columnar Representation of Personal Space and Visual Space in Human Parietal Cortex
title_full Interdigitated Columnar Representation of Personal Space and Visual Space in Human Parietal Cortex
title_fullStr Interdigitated Columnar Representation of Personal Space and Visual Space in Human Parietal Cortex
title_full_unstemmed Interdigitated Columnar Representation of Personal Space and Visual Space in Human Parietal Cortex
title_short Interdigitated Columnar Representation of Personal Space and Visual Space in Human Parietal Cortex
title_sort interdigitated columnar representation of personal space and visual space in human parietal cortex
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9732835/
https://www.ncbi.nlm.nih.gov/pubmed/36198501
http://dx.doi.org/10.1523/JNEUROSCI.0516-22.2022
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