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Published April 28, 2022 | Published + Submitted + Supplemental Material
Journal Article Open

A theory of cortical map formation in the visual brain

Abstract

The cerebral cortex receives multiple afferents from the thalamus that segregate by stimulus modality forming cortical maps for each sense. In vision, the primary visual cortex maps the multiple dimensions of the visual stimulus in patterns that vary across species for reasons unknown. Here we introduce a general theory of cortical map formation, which proposes that map diversity emerges from species variations in the thalamic afferent density sampling sensory space. In the theory, increasing afferent sampling density enlarges the cortical domains representing the same visual point, allowing the segregation of afferents and cortical targets by multiple stimulus dimensions. We illustrate the theory with an afferent-density model that accurately replicates the maps of different species through afferent segregation followed by thalamocortical convergence pruned by visual experience. Because thalamocortical pathways use similar mechanisms for axon segregation and pruning, the theory may extend to other sensory areas of the mammalian brain.

Additional Information

© The Author(s) 2022. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 14 May 2021; Accepted 16 March 2022; Published 28 April 2022. This work was supported by RO1 EY005253 and RO1 EY027361 from NIH/NEI (J.M.A.) and by DFG Emmy-Noether grant KR 4062/4–1 (J.K.). Data availability: All the electrophysiological measurements and computer simulations from this study are available from source data provided with this paper, from a repository in Zenodo40, and upon request from the correspondence author (jalonso@sunyopt.edu). Code availability: Code to run customized simulations and generate the figures and tables reported in this study are available from a repository in Zenodo40, and upon request from the correspondence author (jalonso@sunyopt.edu). These authors contributed equally: Sohrab Najafian, Erin Koch. Contributions: S.N., E.K. and J.M.A. developed the computational model. J.J., E.K., S.N., H.R., J.K., and J.M.A. performed the electrophysiological measurements. S.N., E.K., K.L.T., J.J., H.R., Q.Z., J.K., and J.M.A. performed analysis of electrophysiological measurements and/or model simulations. The paper was written by S.N. and J.M.A. and edited by all the authors. The authors declare no competing interests. Peer review information: Nature Communications thanks Dario Ringach and the other anonymous reviewer(s) for their contribution to the peer review of this work. Peer review reports are available.

Attached Files

Published - s41467-022-29433-y.pdf

Submitted - 2022.01.10.475662v2.full.pdf

Supplemental Material - 41467_2022_29433_MOESM1_ESM.pdf

Supplemental Material - 41467_2022_29433_MOESM2_ESM.pdf

Supplemental Material - 41467_2022_29433_MOESM3_ESM.pdf

Supplemental Material - 41467_2022_29433_MOESM4_ESM.zip

Supplemental Material - 41467_2022_29433_MOESM5_ESM.mp4

Supplemental Material - 41467_2022_29433_MOESM6_ESM.mp4

Supplemental Material - 41467_2022_29433_MOESM7_ESM.mp4

Supplemental Material - 41467_2022_29433_MOESM8_ESM.mp4

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Additional details

Created:
August 22, 2023
Modified:
November 16, 2023