Cited by 143Spatial Cognition and NavigationMemory and Neural MechanismsTactile and Sensory Interactions

Modality-independent coding of spatial layout in the human brain

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Wolbers, Thomas, Klatzky, Roberta L., Loomis, Jack M., Wutte, Magdalena G., Giudice, Nicholas A.·2011·Current Biology

Abstract

In many nonhuman species, neural computations of navigational information such as position and orientation are not tied to a specific sensory modality [1, 2]. Rather, spatial signals are integrated from multiple input sources, likely leading to abstract representations of space. In contrast, the potential for abstract spatial representations in humans is not known, because most neuroscientific experiments on human navigation have focused exclusively on visual cues. Here, we tested the modality independence hypothesis with two functional magnetic resonance imaging (fMRI) experiments that characterized computations in regions implicated in processing spatial layout [3]. According to the hypothesis, such regions should be recruited for spatial computation of 3D geometric configuration, independent of a specific sensory modality. In support of this view, sighted participants showed strong activation of the parahippocampal place area (PPA) and the retrosplenial cortex (RSC) for visual and haptic exploration of information-matched scenes but not objects. Functional connectivity analyses suggested that these effects were not related to visual recoding, which was further supported by a similar preference for haptic scenes found with blind participants. Taken together, these findings establish the PPA/RSC network as critical in modality-independent spatial computations and provide important evidence for a theory of high-level abstract spatial information processing in the human brain.

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  1. [1]Jeffery KJ 2007 Self-localization and the entorhinal-hippocampal system Curr Opin Neurobiol 17 684 691 18249109
  2. [2]Taube JS 2007 The head direction signal: origins and sensory-motor integration Annu Rev Neurosci 30 181 207 17341158
  3. [3]Epstein RA 2008 Parahippocampal and retrosplenial contributions to human spatial navigation Trends Cogn Sci 12 388 396 18760955 PMC2858632
  4. [4]Epstein R Harris A Stanley D Kanwisher N 1999 The parahippocampal place area: Recognition, navigation, or encoding? Neuron 23 115 125 10402198
  5. [5]Newell FN Woods AT Mernagh M Bulthoff HH 2005 Visual, haptic and crossmodal recognition of scenes Experimental Brain Research 161 233 242 15490135
  6. [6]O’Craven KM Kanwisher N 2000 Mental imagery of faces and places activates corresponding stimulus-specific brain regions J Cogn Neurosci 12 1013 1023 11177421
  7. [7]Gattas R Sousa AP Mishkin M Ungerleider LG 1997 Cortical projections of area V2 in the macaque Cerebral Cortex 7 110 129 9087820
  8. [8]Ungerleider LG Galkin TW Desimone R Gattass R 2008 Cortical connections of area V4 in the macaque Cerebral Cortex 18 477 499 17548798
  9. [10]Mahon BZ Anzellotti S Schwarzbach J Zampini M Caramazza A 2009 Category-specific organization in the human brain does not require visual experience Neuron 63 397 405 19679078 PMC2743253
  10. [11]Scheperjans F Hermann K Eickhoff SB Amunts K Schleicher A Zilles K 2008 Observer-independent cytoarchitectonic mapping of the human superior parietal cortex Cerebral Cortex 18 846 867 17644831
  11. [12]Nichols T Brett M Andersson J Wager T Poline JB 2005 Valid conjunction inference with the minimum statistic Neuroimage 25 653 660 15808966
  12. [13]Amedi A Jacobson G Hendler T Malach R Zohary E 2002 Convergence of visual and tactile shape processing in the human lateral occipital complex Cerebral Cortex 12 1202 1212 12379608
  13. [14]Pietrini P Furey ML Ricciardi E Gobbini MI Wu WH Cohen L Guazzelli M Haxby JV 2004 Beyond sensory images: Object-based representation in the human ventral pathway Proc Natl Acad Sci U S A 101 5658 5663 15064396 PMC397466
  14. [15]Hamilton RH Pascual-Leone A 1998 Cortical plasticity associated with Braille learning Trends in Cognitive Sciences 2 168 174 21227151
  15. [16]Buchel C Price C Frackowiak RSJ Friston K 1998 Different activation patterns in the visual cortex of late and congenitally blind subjects Brain 121 409 419 9549517
  16. [17]Kilgour AR Kitada R Servos P James TW Lederman SJ 2005 Haptic face identification activates ventral occipital and temporal areas: an fMRI study Brain and Cognition 59 246 257 16157435
  17. [18]Kitada R Johnsrude IS Kochiyama T Lederman SJ 2009 Functional specialization and convergence in the occipito-temporal cortex supporting haptic and visual identification of human faces and body parts: an fMRI study Journal of Cognitive Neuroscience 21 2027 2045 18823255
  18. [19]James TW Humphrey GK Gati JS Servos P Menon RS Goodale MA 2002 Haptic study of three-dimensional objects activates extrastriate visual areas Neuropsychologia 40 1706 1714 11992658
  19. [20]Wolbers T Hegarty M 2010 What determines our navigational abilities? Trends Cogn Sci 14 138 146 20138795
  20. [21]Loomis JM Klatzky RL Golledge RG Cincinelli JG Pellegrino JW Fry PA 1993 Nonvisual navigation by blind and sighted: Assessment of path integration ability Journal of Experimental Psychology: General 122 73 91 8440978
  21. [22]Tcheang L Bulthoff HH Burgess N 2011 Visual influence on path integration in darkness indicates a multimodal representation of large-scale space Proc Natl Acad Sci U S A 108 1152 1157 21199934 PMC3024704
  22. [23]Nardini M Jones P Bedford R Braddick O 2008 Development of cue integration in human navigation Curr Biol 18 689 693 18450447
  23. [24]Presson CC Montello DR 1994 Updating after rotational and translational body movements: Coordinate structure of perspective space Perception 23 1447 1455 7792134
  24. [26]Loomis JM Lippa Y Golledge RG Klatzky RL 2002 Spatial updating of locations specified by 3-d sound and spatial language Journal of Experimental Psychology: Learning, Memory, and Cognition 28 335 345 11911388
  25. [28]Byrne P Becker S 2004 Modeling mental navigation in scenes with multiple objects Neural Comput 16 1851 1872 15265325
  26. [29]Henderson JM Larson CL Zhu DC 2008 Full scenes produce more activation than close-up scenes and scene-diagnostic objects in parahippocampal and retrosplenial cortex: an fMRI study Brain Cogn 66 40 49 17606317
  27. [30]Park S Chun MM 2009 Different roles of the parahippocampal place area (PPA) and retrosplenial cortex (RSC) in panoramic scene perception Neuroimage 47 1747 1756 19398014 PMC2753672
  28. [31]Kobayashi Y Amaral DG 2003 Macaque monkey retrosplenial cortex: II. Cortical afferents J Comp Neurol 466 48 79 14515240
  29. [32]Loomis JM Lederman SJ Boff K Kaufman L Thomas J 1986 Tactual perception Handbook of Perception and Human Performance 2 New York Wiley
  30. [34]Epstein RA 2008 Parahippocampal and retrosplenial contributions to human spatial navigation Trends in Cognitive Sciences 12 388 396 18760955 PMC2858632
  31. [35]Oldfield RC 1971 The assessment and analysis of handedness: the Edinburgh inventory Neuropsychologia 9 97 113 5146491
  32. [36]Evans AC Collins DL Mills DR Brown ED Kelly RL Peters TM 1993 3D statistical neuroanatomical models from 305 MRI volumes Proc. IEEE-Nuclear Science Symposium and Medical Imaging 1–3 1813 1817

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Authors
Wolbers, T., Klatzky, R. L., Loomis, J. M., Wutte, M. G., & Giudice, N. A.
Affiliations
  • University of Edinburgh (GB)
  • Carnegie Mellon University (US)
  • University of California, Santa Barbara (US)
  • Ludwig-Maximilians-Universität München (DE)
  • University of Maine (US)
Corresponding author
  • Wolbers, Thomas
  • Giudice, Nicholas A.
Venue
Current Biology
Publisher
Elsevier BV
Published
2011-06
Volume
21
Issue
11
Pages
984-989
ISSN
0960-9822 (ISSN-L)
OpenAlex
W2150225858
Cited by
143
References
4
Citations by year
2026: 7 · 2025: 6 · 2024: 10 · 2023: 11 · 2022: 16 · 2021: 6 · 2020: 15 · 2019: 7 · 2018: 6 · 2017: 12 · 2016: 11 · 2015: 8 · 2014: 10 · 2013: 10 · 2012: 5
FWCI
18.34
Type
journal article
Language
en
Open access
Locations
  • Current Biology (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
  • Figshare (submittedVersion, cc-by)
  • KiltHub Repository
Funders
  • National Science Foundation (0745328)
  • National Institutes of Health
  • University of California, Santa Barbara
  • National Eye Institute (R01EY016817)
Topics
  • Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
Keywords
modality independence, spatial configuration, parahippocampal place area, retrosplenial cortex, haptic exploration, visual exploration, functional connectivity, spatial navigation, multisensory integration
MeSH terms
Adult, Aged, Blindness, Brain Mapping, Cerebral Cortex, Cues, Female, Form Perception, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Photic Stimulation, Space Perception, Visual Perception, Visually Impaired Persons, Persons with Visual Disabilities, Feedback, Sensory

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