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Research Article

Axonal plasticity associated with perceptual learning in adult macaque primary visual cortex

Timo van Kerkoerle, View ORCID ProfileSally A. Marik, Stephan Meyer zum Alten Borgloh, and Charles D. Gilbert
  1. aLaboratory of Neurobiology, The Rockefeller University, New York, NY 10065;
  2. bCognitive Neuroimaging Unit, Commissariat à l’Énergie Atomique et aux Énergies Alternatives, Direction des Sciences du Vivant/Institut d’Imagerie Biomédicale, INSERM, NeuroSpin Center, Université Paris-Sud, Université Paris-Saclay, 91191 Gif-sur-Yvette, France;
  3. cDepartment of Biology, Pace University, Pleasantville, NY 10570

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PNAS October 9, 2018 115 (41) 10464-10469; first published September 27, 2018; https://doi.org/10.1073/pnas.1812932115
Timo van Kerkoerle
aLaboratory of Neurobiology, The Rockefeller University, New York, NY 10065;
bCognitive Neuroimaging Unit, Commissariat à l’Énergie Atomique et aux Énergies Alternatives, Direction des Sciences du Vivant/Institut d’Imagerie Biomédicale, INSERM, NeuroSpin Center, Université Paris-Sud, Université Paris-Saclay, 91191 Gif-sur-Yvette, France;
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Sally A. Marik
cDepartment of Biology, Pace University, Pleasantville, NY 10570
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  • ORCID record for Sally A. Marik
Stephan Meyer zum Alten Borgloh
aLaboratory of Neurobiology, The Rockefeller University, New York, NY 10065;
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Charles D. Gilbert
aLaboratory of Neurobiology, The Rockefeller University, New York, NY 10065;
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  • For correspondence: gilbert@rockefeller.edu
  1. Contributed by Charles Gilbert, August 24, 2018 (sent for review July 26, 2018; reviewed by Ulf T. Eysel and Takeo Watanabe)

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Significance

Perceptual learning is a form of memory involving improvement in the ability to detect or discriminate between sensory stimuli. Encoding learned information requires plasticity of cortical circuits. Physiological studies have suggested that even the earliest stages in sensory cortical processing show functional changes associated with perceptual improvements. Previously, we have shown experience-dependent change in cortical circuits associated with retinal lesions that can account for functional adaptation to CNS lesions. Here, we have studied whether these changes are also associated with normal visual experience, specifically with perceptual learning. We found that during the course of perceptual learning axon collaterals in primary visual cortex (V1) undergo sprouting and pruning, suggesting how V1 is engaged in encoding learned information.

Abstract

Perceptual learning is associated with changes in the functional properties of neurons even in primary sensory areas. In macaque monkeys trained to perform a contour detection task, we have observed changes in contour-related facilitation of neuronal responses in primary visual cortex that track their improvement in performance on a contour detection task. We have previously explored the anatomical substrate of experience-dependent changes in the visual cortex based on a retinal lesion model, where we find sprouting and pruning of the axon collaterals in the cortical lesion projection zone. Here, we attempted to determine whether similar changes occur under normal visual experience, such as that associated with perceptual learning. We labeled the long-range horizontal connections in visual cortex by virally mediated transfer of genes expressing fluorescent probes, which enabled us to do longitudinal two-photon imaging of axonal arbors over the period during which animals improve in contour detection performance. We found that there are substantial changes in the axonal arbors of neurons in cortical regions representing the trained part of the visual field, with sprouting of new axon collaterals and pruning of preexisting axon collaterals. Our findings indicate that changes in the structure of axonal arbors are part of the circuit-level mechanism of perceptual learning, and further support the idea that the learned information is encoded at least in part in primary visual cortex.

  • cortical plasticity
  • adult plasticity
  • horizontal connections
  • axon sprouting
  • axon pruning

Footnotes

  • ↵1T.v.K. and S.A.M. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: gilbert{at}rockefeller.edu.
  • Author contributions: T.v.K., S.A.M., S.M.z.A.B., and C.D.G. designed research; T.v.K., S.A.M., S.M.z.A.B., and C.D.G. performed research; T.v.K., S.A.M., and C.D.G. analyzed data; and T.v.K., S.A.M., and C.D.G. wrote the paper.

  • Reviewers: U.T.E., Ruhr-Universität Bochum; and T.W., Brown University.

  • The authors declare no conflict of interest.

Published under the PNAS license.

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Axonal plasticity associated with perceptual learning in adult macaque primary visual cortex
Timo van Kerkoerle, Sally A. Marik, Stephan Meyer zum Alten Borgloh, Charles D. Gilbert
Proceedings of the National Academy of Sciences Oct 2018, 115 (41) 10464-10469; DOI: 10.1073/pnas.1812932115

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Axonal plasticity associated with perceptual learning in adult macaque primary visual cortex
Timo van Kerkoerle, Sally A. Marik, Stephan Meyer zum Alten Borgloh, Charles D. Gilbert
Proceedings of the National Academy of Sciences Oct 2018, 115 (41) 10464-10469; DOI: 10.1073/pnas.1812932115
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Proceedings of the National Academy of Sciences: 115 (41)
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