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Learning enhances the relative impact of top-down processing in the visual cortex

Nature Neuroscience volume 18, pages 11161122 (2015) | Download Citation

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Abstract

Theories have proposed that, in sensory cortices, learning can enhance top-down modulation by higher brain areas while reducing bottom-up sensory drives. To address circuit mechanisms underlying this process, we examined the activity of layer 2/3 (L2/3) excitatory neurons in the mouse primary visual cortex (V1) as well as L4 excitatory neurons, the main bottom-up source, and long-range top-down projections from the retrosplenial cortex (RSC) during associative learning over days using chronic two-photon calcium imaging. During learning, L4 responses gradually weakened, whereas RSC inputs became stronger. Furthermore, L2/3 acquired a ramp-up response temporal profile, potentially encoding the timing of the associated event, which coincided with a similar change in RSC inputs. Learning also reduced the activity of somatostatin-expressing inhibitory neurons (SOM-INs) in V1 that could potentially gate top-down inputs. Finally, RSC inactivation or SOM-IN activation was sufficient to partially reverse the learning-induced changes in L2/3. Together, these results reveal a learning-dependent dynamic shift in the balance between bottom-up and top-down information streams and uncover a role of SOM-INs in controlling this process.

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Change history

  • 16 July 2015

    In the version of this article initially published online, the Acknowledgments listed T.K. as a recipient of the Robertson Stem Cell Prize from the New York Stem Cell Foundation. This should have read a NYSCF-Robertson Investigator. The error has been corrected for the print, PDF and HTML versions of this article.

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Acknowledgements

We thank A. Kim and L. Xiao for technical assistance, L.L. Looger, J. Akerboom, D.S. Kim and the GENIE Project at Janelia Farm for making GCaMP available, S. Olsen, B. Liu, S. Ruediger-Lee and M. Scanziani for help with visual stimulation and circular treadmill, S. Shabel and R. Malinow for help with slice experiments, and M. Basso, R. Malinow, J. Serences and members of the Komiyama laboratory for comments and discussions. This work was supported by grants from the US National Institutes of Health (1R01NS091010-01, 1R01DC014690-01), Japan Science and Technology Agency (PRESTO), Pew Charitable Trusts, Alfred P. Sloan Foundation, David & Lucile Packard Foundation, Human Frontier Science Program, McKnight Foundation, and the New York Stem Cell Foundation (NYSCF) to T.K. H.M. was supported by the Uehara Memorial Foundation Research Fellowship and the JSPS postdoctoral fellowship for Research Abroad. T.K. is a NYSCF-Robertson Investigator.

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Affiliations

  1. Neurobiology Section, Center for Neural Circuits and Behavior, and Department of Neurosciences, University of California, San Diego, La Jolla, California, USA.

    • Hiroshi Makino
    •  & Takaki Komiyama
  2. JST, PRESTO, University of California, San Diego, La Jolla, California, USA.

    • Takaki Komiyama

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Contributions

H.M. and T.K. conceived the project. H.M. performed the experiments. H.M. and T.K. analyzed the data and wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Takaki Komiyama.

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DOI

https://doi.org/10.1038/nn.4061

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