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Sensory and decision-related activity propagate in a cortical feedback loop during touch perception

Nature Neuroscience volume 19, pages 12431249 (2016) | Download Citation

Abstract

The brain transforms physical sensory stimuli into meaningful perceptions. In animals making choices about sensory stimuli, neuronal activity in successive cortical stages reflects a progression from sensation to decision. Feedforward and feedback pathways connecting cortical areas are critical for this transformation. However, the computational functions of these pathways are poorly understood because pathway-specific activity has rarely been monitored during a perceptual task. Using cellular-resolution, pathway-specific imaging, we measured neuronal activity across primary (S1) and secondary (S2) somatosensory cortices of mice performing a tactile detection task. S1 encoded the stimulus better than S2, while S2 activity more strongly reflected perceptual choice. S1 neurons projecting to S2 fed forward activity that predicted choice. Activity encoding touch and choice propagated in an S1–S2 loop along feedforward and feedback axons. Our results suggest that sensory inputs converge into a perceptual outcome as feedforward computations are reinforced in a feedback loop.

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Acknowledgements

We thank V. Jayaraman, R. Kerr, D. Kim, L. Looger, K. Svoboda and the HHMI Janelia Farm GENIE Project for GCaMP6. We thank S. Peron for MATLAB software, T. Shelley for instrument fabrication, and K. Severson and E. Finkel for mouse husbandry. We thank E. Finkel, D. Xu, K. Severson, B. Bari, M. Chevee, K. Svoboda, S. Brown, J. Cohen and S. Mysore for comments on the manuscript. This work was supported by the Whitehall Foundation, Klingenstein Fund, the Johns Hopkins Science of Learning Institute, NIH grant R01NS089652 (D.H.O.) and NIH core grant P30NS050274. G.M. was supported by a JSPS Postdoctoral Fellowship for Research Abroad.

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Affiliations

  1. The Solomon H. Snyder Department of Neuroscience, Kavli Neuroscience Discovery Institute, Brain Science Institute, The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

    • Sung Eun Kwon
    • , Hongdian Yang
    • , Genki Minamisawa
    •  & Daniel H O'Connor

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Contributions

S.E.K. and D.H.O. planned the project. S.E.K. performed imaging, behavioral, and optogenetics experiments. H.Y. performed electrophysiology and optogenetics experiments. S.E.K. and D.H.O. analyzed data. G.M. established S2 targeting methods. S.E.K. and D.H.O. wrote the paper with comments from H.Y. and G.M.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Daniel H O'Connor.

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https://doi.org/10.1038/nn.4356

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