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Reorganization of cortical population activity imaged throughout long-term sensory deprivation

Nature Neuroscience volume 15, pages 1539–1546 (2012)Cite this article

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Abstract

Sensory maps are reshaped by experience. It is unknown how map plasticity occurs in vivo in functionally diverse neuronal populations because activity of the same cells has not been tracked over long time periods. Here we used repeated two-photon imaging of a genetic calcium indicator to measure whisker-evoked responsiveness of the same layer 2/3 neurons in adult mouse barrel cortex over weeks, first with whiskers intact, then during continued trimming of all but one whisker. Across the baseline period, neurons displayed heterogeneous yet stable responsiveness. During sensory deprivation, responses to trimmed whisker stimulation globally decreased, whereas responses to spared whisker stimulation increased for the least active neurons and decreased for the most active neurons. These findings suggest that recruitment of inactive, 'silent' neurons is part of a convergent redistribution of population activity underlying sensory map plasticity. Sensory-driven responsiveness is a key property controlling experience-dependent activity changes in individual neurons.

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Figure 1: Long-term imaging of neuronal population activity in mouse barrel cortex.
Figure 2: Long-term functionality of YC3.60.
Figure 3: Stable response probabilities of cortical neurons under baseline conditions.
Figure 4: Flexible tuning properties over baseline days and weeks.
Figure 5: Map plasticity induced by whisker trimming.
Figure 6: Retuning of neuronal selectivity.
Figure 7: Differential changes in population activity depend on cell class.

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Acknowledgements

We thank H. Kasper, S. Giger and D. Göckeritz for technical assistance and A. Holtmaat, B. Gähwiler, M. Schwab, M. Thallmair and V. Planchamp for comments on an earlier version of the manuscript. This work was supported by an AMBIZIONE grant from the Swiss National Science Foundation (SNSF) to D.J.M.; a postdoctoral fellowship from the German Academic Exchange Service (DAAD) to H.L.; an SNSF grant to F. Helmchen (3100A0-114624); the EU-FP7 program (PLASTICISE project 223524 to F. Helmchen, and BRAIN-I-NETS project 243914 to F. Helmchen and F. Haiss); a grant from the Swiss SystemsX.ch initiative (project 2008/2011-Neurochoice) to F. Helmchen and B.W.; and the Max Planck Society and the Fritz Thyssen Stiftung (M.T.H.).

Author information

Author notes

  1. Mazahir T Hasan

    Present address: Present address: Charité – Universitätsmedizin, NeuroCure Cluster of Excellence, Berlin, Germany.,

  2. David J Margolis and Henry Lütcke: These authors contributed equally to this work.

Authors and Affiliations

  1. Brain Research Institute, University of Zurich, Zurich, Switzerland

    David J Margolis, Henry Lütcke, Kristina Schulz & Fritjof Helmchen

  2. Neuroscience Center Zurich, University of Zurich and Swiss Federal Institute of Technology (ETH), Zurich, Switzerland

    David J Margolis, Kristina Schulz, Bruno Weber & Fritjof Helmchen

  3. Institute of Pharmacology and Toxicology, University of Zurich, Switzerland

    Florent Haiss & Bruno Weber

  4. Department of Neurology, Center for Molecular Physiology of the Brain, University Medicine Göttingen, Göttingen, Germany

    Sebastian Kügler

  5. Max Planck Institute for Medical Research, Heidelberg, Germany

    Mazahir T Hasan

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Contributions

Conceived/designed the study: D.J.M., H.L., F. Helmchen; performed viral injections: D.J.M., H.L.; performed cranial window surgeries: D.J.M., F. Haiss (laboratory of B.W.); performed imaging experiments: D.J.M., H.L., K.S.; performed electrophysiology experiments: H.L., D.J.M.; produced constructs and viruses: M.T.H., S.K.; developed analysis routines: H.L.; performed analysis: H.L., D.J.M., F. Helmchen; wrote the manuscript: D.J.M., H.L., F. Helmchen.

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Correspondence to Fritjof Helmchen.

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Margolis, D., Lütcke, H., Schulz, K. et al. Reorganization of cortical population activity imaged throughout long-term sensory deprivation. Nat Neurosci 15, 1539–1546 (2012). https://doi.org/10.1038/nn.3240

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