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Invariant computations in local cortical networks with balanced excitation and inhibition

Nature Neuroscience volume 8, pages 194–201 (2005)Cite this article

Abstract

Cortical computations critically involve local neuronal circuits. The computations are often invariant across a cortical area yet are carried out by networks that can vary widely within an area according to its functional architecture. Here we demonstrate a mechanism by which orientation selectivity is computed invariantly in cat primary visual cortex across an orientation preference map that provides a wide diversity of local circuits. Visually evoked excitatory and inhibitory synaptic conductances are balanced exquisitely in cortical neurons and thus keep the spike response sharply tuned at all map locations. This functional balance derives from spatially isotropic local connectivity of both excitatory and inhibitory cells. Modeling results demonstrate that such covariation is a signature of recurrent rather than purely feed-forward processing and that the observed isotropic local circuit is sufficient to generate invariant spike tuning.

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Figure 1: Orientation tuning of synaptic conductances for a cell in an orientation domain (a–d) and at a pinwheel center (e–h).
Figure 2: Additional examples of conductance tuning of cells in orientation domains and pinwheel centers.
Figure 3: Average tuning differences between cells at pinwheels and orientation domains.
Figure 5: Model predictions for synaptic conductances, membrane potentials and spike responses underlying orientation selectivity across the orientation map.
Figure 4: Anatomical analysis of local excitatory and inhibitory projections to pinwheel centers and orientation domains.

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Acknowledgements

This work was supported by Ministerio de Educación y Ciencia, Spain (J.M.), Howard Hughes Medical Institute (J.S.), Deutsche Forschungsgemeinschaft Sonderforschungsbereiche 618, Germany (L.S., O.B., K.O.), Wellcome Trust (P.W., K.O.) and National Institutes of Health (D.C.L., M.S.).

Author information

Author notes

  1. Jorge Mariño

    Present address: Department of Medicine, Neuroscience and Motor Control Group (Neurocom), Univ. A Coruña, Fac. CC. da Saúde, Campus de Oza, 15006, A Coruña, Spain

  2. David C Lyon

    Present address: The Salk Institute, SNL-C, 10010 North Torrey Pines Road, La Jolla, California, 92037, USA

Authors and Affiliations

  1. Department of Brain and Cognitive Sciences and Picower Center for Learning and Memory, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Jorge Mariño, James Schummers, David C Lyon & Mriganka Sur

  2. Department of Computer Science and Electrical Engineering, Berlin University of Technology, FR2-1, Franklinstrasse 28/29, Berlin, 10587, Germany

    Lars Schwabe, Oliver Beck, Peter Wiesing & Klaus Obermayer

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Correspondence to Mriganka Sur.

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Supplementary information

Supplementary Fig. 1

Examples of data used to measure synaptic conductances and passive neuronal properties. (PDF 282 kb)

Supplementary Fig. 2

Analysis of accuracy of pinwheel targeting. (PDF 126 kb)

Supplementary Fig. 3

Results from the single-cell model, demonstrating that inhibition balances excitation and produces sharp tuning across the orientation map. (PDF 26 kb)

Supplementary Fig. 4

Results from the network model, demonstrating tuned conductances and sharp spike tuning at pinwheels and orientation domains. (PDF 34 kb)

Supplementary Fig. 5

Results from the network model, demonstrating that balanced recurrent excitation and inhibition are required for location invariant orientation tuning. (PDF 17 kb)

Supplementary Notes (PDF 193 kb)

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Mariño, J., Schummers, J., Lyon, D. et al. Invariant computations in local cortical networks with balanced excitation and inhibition. Nat Neurosci 8, 194–201 (2005). https://doi.org/10.1038/nn1391

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