Neural codes for one’s own position and direction in a real-world “vista” environment

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Humans, like animals, rely on an accurate knowledge of one’s spatial position and facing direction to keep orientated in the surrounding space. Although previous neuroimaging studies demonstrated that scene-selective regions (the parahippocampal place area or PPA, the occipital place area or OPA and the retrosplenial complex or RSC), and the hippocampus (HC) are implicated in coding position and facing direction within small-(room-sized) and large-scale navigational environments, little is known about how these regions represent these spatial quantities in a large open-field environment. Here, we used functional magnetic resonance imaging (fMRI) in humans to explore the neural codes of these navigationally-relevant information while participants viewed images which varied for position and facing direction within a familiar, real-world circular square. We observed neural adaptation for repeated directions in the HC, even if no navigational task was required. Further, we found that the amount of knowledge of the environment interacts with the PPA selectivity in encoding positions: individuals who needed more time to memorize positions in the square during a preliminary training task showed less neural attenuation in this scene-selective region. We also observed adaptation effects, which reflect the real distances between consecutive positions, in scene-selective regions but not in the HC. When examining the multi-voxel patterns of activity we observed that scene-responsive regions and the HC encoded both spatial information and that the RSC classification accuracy for positions was higher in individuals scoring higher to a self-reported questionnaire of spatial abilities. Our findings provide new insight into how the human brain represents a real, large-scale “vista” space, demonstrating the presence of neural codes for position and direction in both scene-selective and hippocampal regions, and revealing the existence, in the former regions, of a map-like spatial representation reflecting real-world distance between consecutive positions.

Original languageEnglish
Article number167
JournalFrontiers in Human Neuroscience
Volume12
DOIs
Publication statusPublished - Apr 30 2018

Fingerprint

Hippocampus
Neuroimaging
Magnetic Resonance Imaging
Direction compound
Brain

Keywords

  • FMRI adaptation
  • Hippocampus
  • Individual differences
  • Multi-voxel pattern analysis
  • Occipital place area
  • Parahippocampal place area
  • Retrosplenial complex
  • Spatial representation

ASJC Scopus subject areas

  • Neuropsychology and Physiological Psychology
  • Neurology
  • Psychiatry and Mental health
  • Biological Psychiatry
  • Behavioral Neuroscience

Cite this

@article{4be53f97bd344a5ea66df0564f2db9a8,
title = "Neural codes for one’s own position and direction in a real-world “vista” environment",
abstract = "Humans, like animals, rely on an accurate knowledge of one’s spatial position and facing direction to keep orientated in the surrounding space. Although previous neuroimaging studies demonstrated that scene-selective regions (the parahippocampal place area or PPA, the occipital place area or OPA and the retrosplenial complex or RSC), and the hippocampus (HC) are implicated in coding position and facing direction within small-(room-sized) and large-scale navigational environments, little is known about how these regions represent these spatial quantities in a large open-field environment. Here, we used functional magnetic resonance imaging (fMRI) in humans to explore the neural codes of these navigationally-relevant information while participants viewed images which varied for position and facing direction within a familiar, real-world circular square. We observed neural adaptation for repeated directions in the HC, even if no navigational task was required. Further, we found that the amount of knowledge of the environment interacts with the PPA selectivity in encoding positions: individuals who needed more time to memorize positions in the square during a preliminary training task showed less neural attenuation in this scene-selective region. We also observed adaptation effects, which reflect the real distances between consecutive positions, in scene-selective regions but not in the HC. When examining the multi-voxel patterns of activity we observed that scene-responsive regions and the HC encoded both spatial information and that the RSC classification accuracy for positions was higher in individuals scoring higher to a self-reported questionnaire of spatial abilities. Our findings provide new insight into how the human brain represents a real, large-scale “vista” space, demonstrating the presence of neural codes for position and direction in both scene-selective and hippocampal regions, and revealing the existence, in the former regions, of a map-like spatial representation reflecting real-world distance between consecutive positions.",
keywords = "FMRI adaptation, Hippocampus, Individual differences, Multi-voxel pattern analysis, Occipital place area, Parahippocampal place area, Retrosplenial complex, Spatial representation",
author = "Valentina Sulpizio and Maddalena Boccia and Cecilia Guariglia and Gaspare Galati",
year = "2018",
month = "4",
day = "30",
doi = "10.3389/fnhum.2018.00167",
language = "English",
volume = "12",
journal = "Frontiers in Human Neuroscience",
issn = "1662-5161",
publisher = "Frontiers Media S. A.",

}

TY - JOUR

T1 - Neural codes for one’s own position and direction in a real-world “vista” environment

AU - Sulpizio, Valentina

AU - Boccia, Maddalena

AU - Guariglia, Cecilia

AU - Galati, Gaspare

PY - 2018/4/30

Y1 - 2018/4/30

N2 - Humans, like animals, rely on an accurate knowledge of one’s spatial position and facing direction to keep orientated in the surrounding space. Although previous neuroimaging studies demonstrated that scene-selective regions (the parahippocampal place area or PPA, the occipital place area or OPA and the retrosplenial complex or RSC), and the hippocampus (HC) are implicated in coding position and facing direction within small-(room-sized) and large-scale navigational environments, little is known about how these regions represent these spatial quantities in a large open-field environment. Here, we used functional magnetic resonance imaging (fMRI) in humans to explore the neural codes of these navigationally-relevant information while participants viewed images which varied for position and facing direction within a familiar, real-world circular square. We observed neural adaptation for repeated directions in the HC, even if no navigational task was required. Further, we found that the amount of knowledge of the environment interacts with the PPA selectivity in encoding positions: individuals who needed more time to memorize positions in the square during a preliminary training task showed less neural attenuation in this scene-selective region. We also observed adaptation effects, which reflect the real distances between consecutive positions, in scene-selective regions but not in the HC. When examining the multi-voxel patterns of activity we observed that scene-responsive regions and the HC encoded both spatial information and that the RSC classification accuracy for positions was higher in individuals scoring higher to a self-reported questionnaire of spatial abilities. Our findings provide new insight into how the human brain represents a real, large-scale “vista” space, demonstrating the presence of neural codes for position and direction in both scene-selective and hippocampal regions, and revealing the existence, in the former regions, of a map-like spatial representation reflecting real-world distance between consecutive positions.

AB - Humans, like animals, rely on an accurate knowledge of one’s spatial position and facing direction to keep orientated in the surrounding space. Although previous neuroimaging studies demonstrated that scene-selective regions (the parahippocampal place area or PPA, the occipital place area or OPA and the retrosplenial complex or RSC), and the hippocampus (HC) are implicated in coding position and facing direction within small-(room-sized) and large-scale navigational environments, little is known about how these regions represent these spatial quantities in a large open-field environment. Here, we used functional magnetic resonance imaging (fMRI) in humans to explore the neural codes of these navigationally-relevant information while participants viewed images which varied for position and facing direction within a familiar, real-world circular square. We observed neural adaptation for repeated directions in the HC, even if no navigational task was required. Further, we found that the amount of knowledge of the environment interacts with the PPA selectivity in encoding positions: individuals who needed more time to memorize positions in the square during a preliminary training task showed less neural attenuation in this scene-selective region. We also observed adaptation effects, which reflect the real distances between consecutive positions, in scene-selective regions but not in the HC. When examining the multi-voxel patterns of activity we observed that scene-responsive regions and the HC encoded both spatial information and that the RSC classification accuracy for positions was higher in individuals scoring higher to a self-reported questionnaire of spatial abilities. Our findings provide new insight into how the human brain represents a real, large-scale “vista” space, demonstrating the presence of neural codes for position and direction in both scene-selective and hippocampal regions, and revealing the existence, in the former regions, of a map-like spatial representation reflecting real-world distance between consecutive positions.

KW - FMRI adaptation

KW - Hippocampus

KW - Individual differences

KW - Multi-voxel pattern analysis

KW - Occipital place area

KW - Parahippocampal place area

KW - Retrosplenial complex

KW - Spatial representation

UR - http://www.scopus.com/inward/record.url?scp=85046888080&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85046888080&partnerID=8YFLogxK

U2 - 10.3389/fnhum.2018.00167

DO - 10.3389/fnhum.2018.00167

M3 - Article

AN - SCOPUS:85046888080

VL - 12

JO - Frontiers in Human Neuroscience

JF - Frontiers in Human Neuroscience

SN - 1662-5161

M1 - 167

ER -