A Network of Topographic Maps in Human Association Cortex Hierarchically Transforms Visual Timing-Selective Responses

Ben M. Harvey*, Serge O. Dumoulin, Alessio Fracasso, Jacob M. Paul

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Accurately timing sub-second sensory events is crucial when perceiving our dynamic world. This ability allows complex human behaviors that require timing-dependent multisensory integration and action planning. Such behaviors include perception and performance of speech, music, driving, and many sports. How are responses to sensory event timing processed for multisensory integration and action planning? We measured responses to viewing systematically changing visual event timing using ultra-high-field fMRI. We analyzed these responses with neural population response models selective for event duration and frequency, following behavioral, computational, and macaque action planning results and comparisons to alternative models. We found systematic local changes in timing preferences (recently described in supplementary motor area) in an extensive network of topographic timing maps, mirroring sensory cortices and other quantity processing networks. These timing maps were partially left lateralized and widely spread, from occipital visual areas through parietal multisensory areas to frontal action planning areas. Responses to event duration and frequency were closely linked. As in sensory cortical maps, response precision varied systematically with timing preferences, and timing selectivity systematically varied between maps. Progressing from posterior to anterior maps, responses to multiple events were increasingly integrated, response selectivity narrowed, and responses focused increasingly on the middle of the presented timing range. These timing maps largely overlap with numerosity and visual field map networks. In both visual timing map and visual field map networks, selective responses and topographic map organization may facilitate hierarchical transformations by allowing neural populations to interact over minimal distances.

Original languageEnglish
Pages (from-to)1424-1434.e6
JournalCurrent Biology
Volume30
Issue number8
DOIs
Publication statusPublished - 20 Apr 2020

Bibliographical note

Funding Information:
This work was supported by the Netherlands Organization for Scientific Research (452.17.012 to B.M.H.; 016.Vici.185.050 to S.O.D.); the Portuguese Foundation for Science and Technology (IF/01405/2014 to B.M.H.); the Royal Netherlands Academy of Arts and Sciences (Ammodo award to S.O.D.); and the Biotechnology and Biological Sciences Research Council (BB/S006605/1 to A.F.). Conceptualization, B.M.H. and S.O.D.; Methodology, B.M.H.; Software, B.M.H.; Validation, B.M.H.; Formal Analysis, B.M.H. and J.M.P.; Investigation, B.M.H. A.F. and J.M.P.; Data Curation, B.M.H. A.F. and J.M.P.; Writing ? Original Draft, B.M.H.; Writing ? Review & Editing, B.M.H. S.O.D. A.F. and J.M.P.; Visualization, B.M.H.; Supervision, B.M.H. and S.O.D.; Project Administration, B.M.H.; Funding Acquisition, B.M.H. and S.O.D. The authors declare no competing interests.

Funding Information:
This work was supported by the Netherlands Organization for Scientific Research ( 452.17.012 to B.M.H.; 016.Vici.185.050 to S.O.D.); the Portuguese Foundation for Science and Technology ( IF/01405/2014 to B.M.H.); the Royal Netherlands Academy of Arts and Sciences (Ammodo award to S.O.D.); and the Biotechnology and Biological Sciences Research Council ( BB/S006605/1 to A.F.).

Publisher Copyright:
© 2020 The Author(s)

Funding

This work was supported by the Netherlands Organization for Scientific Research (452.17.012 to B.M.H.; 016.Vici.185.050 to S.O.D.); the Portuguese Foundation for Science and Technology (IF/01405/2014 to B.M.H.); the Royal Netherlands Academy of Arts and Sciences (Ammodo award to S.O.D.); and the Biotechnology and Biological Sciences Research Council (BB/S006605/1 to A.F.). Conceptualization, B.M.H. and S.O.D.; Methodology, B.M.H.; Software, B.M.H.; Validation, B.M.H.; Formal Analysis, B.M.H. and J.M.P.; Investigation, B.M.H. A.F. and J.M.P.; Data Curation, B.M.H. A.F. and J.M.P.; Writing ? Original Draft, B.M.H.; Writing ? Review & Editing, B.M.H. S.O.D. A.F. and J.M.P.; Visualization, B.M.H.; Supervision, B.M.H. and S.O.D.; Project Administration, B.M.H.; Funding Acquisition, B.M.H. and S.O.D. The authors declare no competing interests. This work was supported by the Netherlands Organization for Scientific Research ( 452.17.012 to B.M.H.; 016.Vici.185.050 to S.O.D.); the Portuguese Foundation for Science and Technology ( IF/01405/2014 to B.M.H.); the Royal Netherlands Academy of Arts and Sciences (Ammodo award to S.O.D.); and the Biotechnology and Biological Sciences Research Council ( BB/S006605/1 to A.F.).

Keywords

  • brain
  • fMRI
  • functional magnetic resonance imaging
  • hierarchy
  • human
  • numerosity
  • population receptive field
  • pRF
  • timing
  • topographic maps
  • vision

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