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Development of natural scene representation in primary visual cortex requires early postnatal experience

Nina Kowalewski, Janne Kauttonen, Patricia L. Stan, Brian B. Jeon, Thomas Fuchs, Steven M. Chase, Tai Sing Lee, View ORCID ProfileSandra J. Kuhlman
doi: https://doi.org/10.1101/2020.10.14.338897
Nina Kowalewski
1Department of Biological Sciences, Carnegie Mellon University, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
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Janne Kauttonen
1Department of Biological Sciences, Carnegie Mellon University, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
2Center for the Neural Basis of Cognition, 1400 Locust Street, Pittsburgh, PA 15219, USA
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Patricia L. Stan
2Center for the Neural Basis of Cognition, 1400 Locust Street, Pittsburgh, PA 15219, USA
3University of Pittsburgh Center for Neuroscience, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
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Brian B. Jeon
4Department of Biomedical Engineering, Carnegie Mellon University, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
5Neuroscience Institute, Carnegie Mellon University, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
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Thomas Fuchs
1Department of Biological Sciences, Carnegie Mellon University, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
2Center for the Neural Basis of Cognition, 1400 Locust Street, Pittsburgh, PA 15219, USA
5Neuroscience Institute, Carnegie Mellon University, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
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Steven M. Chase
2Center for the Neural Basis of Cognition, 1400 Locust Street, Pittsburgh, PA 15219, USA
4Department of Biomedical Engineering, Carnegie Mellon University, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
5Neuroscience Institute, Carnegie Mellon University, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
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Tai Sing Lee
2Center for the Neural Basis of Cognition, 1400 Locust Street, Pittsburgh, PA 15219, USA
5Neuroscience Institute, Carnegie Mellon University, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
6Department of Computer Science, Carnegie Mellon University, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
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Sandra J. Kuhlman
1Department of Biological Sciences, Carnegie Mellon University, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
2Center for the Neural Basis of Cognition, 1400 Locust Street, Pittsburgh, PA 15219, USA
3University of Pittsburgh Center for Neuroscience, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
4Department of Biomedical Engineering, Carnegie Mellon University, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
5Neuroscience Institute, Carnegie Mellon University, 4400 Fifth Ave, Pittsburgh, PA 15213, USA
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  • ORCID record for Sandra J. Kuhlman
  • For correspondence: skuhlman@cmu.edu
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Summary

The development of the visual system is known to be shaped by early-life experience. To identify response properties that contribute to enhanced natural scene representation, we performed calcium imaging of excitatory neurons in the primary visual cortex (V1) of awake mice raised in three different conditions (standard-reared, dark-reared, and delayed-visual experience) and compared neuronal responses to natural scene features relative to simpler grating stimuli that varied in orientation and spatial frequency. We assessed population selectivity in V1 using decoding methods and found that natural scene discriminability increased by 75% between the ages of 4 to 6 weeks. Both natural scene and grating discriminability were higher in standard-reared animals compared to those raised in the dark. This increase in discriminability was accompanied by a reduction in the number of neurons that responded to low-spatial frequency gratings. At the same time there was an increase in neuronal preference for natural scenes. Light exposure restricted to a 2-4 week window during adulthood did not induce improvements in natural scene nor in grating stimulus discriminability. Our results demonstrate that experience reduces the number of neurons required to effectively encode grating stimuli and that early visual experience enhances natural scene discriminability by directly increasing responsiveness to natural scene features.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵* co-first authors

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted October 15, 2020.
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Development of natural scene representation in primary visual cortex requires early postnatal experience
Nina Kowalewski, Janne Kauttonen, Patricia L. Stan, Brian B. Jeon, Thomas Fuchs, Steven M. Chase, Tai Sing Lee, Sandra J. Kuhlman
bioRxiv 2020.10.14.338897; doi: https://doi.org/10.1101/2020.10.14.338897
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Development of natural scene representation in primary visual cortex requires early postnatal experience
Nina Kowalewski, Janne Kauttonen, Patricia L. Stan, Brian B. Jeon, Thomas Fuchs, Steven M. Chase, Tai Sing Lee, Sandra J. Kuhlman
bioRxiv 2020.10.14.338897; doi: https://doi.org/10.1101/2020.10.14.338897

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