Letter | Published:

Functional organization of excitatory synaptic strength in primary visual cortex

Nature volume 518, pages 399403 (19 February 2015) | Download Citation

Abstract

The strength of synaptic connections fundamentally determines how neurons influence each other’s firing. Excitatory connection amplitudes between pairs of cortical neurons vary over two orders of magnitude, comprising only very few strong connections among many weaker ones1,2,3,4,5,6,7,8,9. Although this highly skewed distribution of connection strengths is observed in diverse cortical areas1,2,3,4,5,6,7,8,9, its functional significance remains unknown: it is not clear how connection strength relates to neuronal response properties, nor how strong and weak inputs contribute to information processing in local microcircuits. Here we reveal that the strength of connections between layer 2/3 (L2/3) pyramidal neurons in mouse primary visual cortex (V1) obeys a simple rule—the few strong connections occur between neurons with most correlated responses, while only weak connections link neurons with uncorrelated responses. Moreover, we show that strong and reciprocal connections occur between cells with similar spatial receptive field structure. Although weak connections far outnumber strong connections, each neuron receives the majority of its local excitation from a small number of strong inputs provided by the few neurons with similar responses to visual features. By dominating recurrent excitation, these infrequent yet powerful inputs disproportionately contribute to feature preference and selectivity. Therefore, our results show that the apparently complex organization of excitatory connection strength reflects the similarity of neuronal responses, and suggest that rare, strong connections mediate stimulus-specific response amplification in cortical microcircuits.

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Acknowledgements

We thank K. Harris, G. Keller, T. Margrie, J. Sjöström, P. Znamenskiy and our laboratory members for discussions and comments, and T. Margrie, E. Rancz and J. Poulet for advice on in vivo whole-cell recordings. This work was supported by the Wellcome Trust (grant no. 095074) and the European Research council. L.C. was funded by the 4-year PhD programme in Neuroscience at UCL. M.F.I. was funded by a UCL International PhD fellowship. D.R.M. was supported by the University of Basel Young Researchers fund.

Author information

Author notes

    • Lee Cossell
    •  & Maria Florencia Iacaruso

    These authors contributed equally to this work.

Affiliations

  1. Department of Neuroscience, Physiology and Pharmacology, University College London, 21 University Street, London WC1E 6DE, UK

    • Lee Cossell
    • , Maria Florencia Iacaruso
    • , Rachael Houlton
    • , Elie N. Sader
    • , Ho Ko
    • , Sonja B. Hofer
    •  & Thomas D. Mrsic-Flogel
  2. Biozentrum, University of Basel, Klingelbergstrasse 50/70, CH - 4056 Basel, Switzerland

    • Lee Cossell
    • , Maria Florencia Iacaruso
    • , Dylan R. Muir
    • , Sonja B. Hofer
    •  & Thomas D. Mrsic-Flogel
  3. Lui Che Woo Institute of Innovative Medicine and Chow Yuk Ho Technology Center for Innovative Medicine, Faculty of Medicine, the Chinese University of Hong Kong, Shatin, New Territories, Hong Kong

    • Ho Ko

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Contributions

L.C., M.F.I., S.B.H. and T.D.M.-F. designed the experiments. L.C. and M.F.I. performed the in vivo and in vitro experiments. R.H. and E.N.S. performed the in vivo whole-cell recordings. H.K. and S.B.H. contributed to the transition during in vivo and in vitro experiments. H. K. and L.C. wrote the software for whole-cell recordings in vivo and in vitro. L.C., M.F.I. and D.R.M. analysed the data. L.C., M.F.I., D.R.M. and T.D.M.-F. wrote the manuscript. All authors discussed the data and commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Thomas D. Mrsic-Flogel.

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DOI

https://doi.org/10.1038/nature14182

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