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Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex

Nature Neuroscience volume 14, pages 1045–1052 (2011)Cite this article

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Abstract

Neuronal responses during sensory processing are influenced by both the organization of intracortical connections and the statistical features of sensory stimuli. How these intrinsic and extrinsic factors govern the activity of excitatory and inhibitory populations is unclear. Using two-photon calcium imaging in vivo and intracellular recordings in vitro, we investigated the dependencies between synaptic connectivity, feature selectivity and network activity in pyramidal cells and fast-spiking parvalbumin-expressing (PV) interneurons in mouse visual cortex. In pyramidal cell populations, patterns of neuronal correlations were largely stimulus-dependent, indicating that their responses were not strongly dominated by functionally biased recurrent connectivity. By contrast, visual stimulation only weakly modified co-activation patterns of fast-spiking PV cells, consistent with the observation that these broadly tuned interneurons received very dense and strong synaptic input from nearby pyramidal cells with diverse feature selectivities. Therefore, feedforward and recurrent network influences determine the activity of excitatory and inhibitory ensembles in fundamentally different ways.

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Figure 1: Calcium imaging and electrophysiological recordings of visually evoked responses in PV neurons.
Figure 2: Assessing synaptic connectivity in vitro between neurons functionally characterized in vivo.
Figure 3: Relationship between response similarity and pair-wise correlations during spontaneous activity.
Figure 4: Comparison of population activity patterns with and without visual stimulation.
Figure 5: Comparison between spontaneous and noise correlation patterns during visual stimulation.

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Acknowledgements

We thank T. Margrie, A. Arenz and E. Rancz for help with in vivo electrophysiology, J. Sjöström and K. Buchanan for help with in vitro electrophysiology, J. Rothman for NeuroMatic software, and M. Hübener and M. Sahani for comments on an earlier version of this manuscript. This work was supported by the Wellcome Trust (T.D.M.-F.), the European Research Council (T.D.M.-F.), the European Molecular Biology Organization (S.B.H.) and the Humboldt Foundation (S.B.H.). We also received funding from the European Community's Seventh Framework Programme (FP2007-2013) under grant agreement no. 223326 (T.D.M.-F.).

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Author notes

  1. Bruno Pichler

    Present address: Present address: National Institute for Medical Research, Mill Hill, London, UK.,

  2. Sonja B Hofer and Ho Ko: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Neuroscience, Physiology and Pharmacology, University College London, London, UK

    Sonja B Hofer, Ho Ko, Bruno Pichler, Hana Ros & Thomas D Mrsic-Flogel

  2. Johns Hopkins University, Baltimore, Maryland, USA

    Joshua Vogelstein

  3. Allen Institute for Brain Science, Seattle, Washington, USA

    Hongkui Zeng & Ed Lein

  4. Ear Institute, University College London, London, UK

    Nicholas A Lesica

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Contributions

S.B.H. and H.K. performed all in vivo and slice experiments. S.B.H., H.K., N.A.L. and T.D.M.-F. analyzed the data. H.R. carried out antibody labeling. B.P. developed software for visual stimulation, image acquisition and image analysis. J.V. developed spike inference algorithms. E.L. and H.Z. generated and supplied the mice. S.B.H., H.K., N.A.L. and T.D.M.-F. wrote the paper.

Corresponding author

Correspondence to Thomas D Mrsic-Flogel.

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The authors declare no competing financial interests.

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Hofer, S., Ko, H., Pichler, B. et al. Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex. Nat Neurosci 14, 1045–1052 (2011). https://doi.org/10.1038/nn.2876

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