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Neuron. 2016 Dec 7;92(5):1106-1121. doi: 10.1016/j.neuron.2016.10.027. Epub 2016 Nov 17.

The Impact of Structural Heterogeneity on Excitation-Inhibition Balance in Cortical Networks.

Author information

1
Neurophysics Laboratory, The Edmond and Lily Safra Center for Brain Sciences, Hebrew University, Jerusalem 91904, Israel; Max Planck-Hebrew University Center for Neuroscience, Jerusalem 91904, Israel.
2
Max Planck-Hebrew University Center for Neuroscience, Jerusalem 91904, Israel; Computational Neuroanatomy Group, Max Planck Institute for Biological Cybernetics, Tübingen 72076, Germany.
3
Max Planck-Hebrew University Center for Neuroscience, Jerusalem 91904, Israel; Department of Visual Data Analysis, Zuse Institute Berlin, Berlin 14195, Germany.
4
Max Planck-Hebrew University Center for Neuroscience, Jerusalem 91904, Israel; Computational Neuroanatomy Group, Max Planck Institute for Biological Cybernetics, Tübingen 72076, Germany; Max Planck Group "In Silico Brain Sciences," Center of Advanced European Studies and Research, Bonn 53175, Germany.
5
Neurophysics Laboratory, The Edmond and Lily Safra Center for Brain Sciences, Hebrew University, Jerusalem 91904, Israel; Max Planck-Hebrew University Center for Neuroscience, Jerusalem 91904, Israel; Center for Brain Science, Harvard University, Cambridge, MA 02138, USA. Electronic address: haim@fiz.huji.ac.il.

Abstract

Models of cortical dynamics often assume a homogeneous connectivity structure. However, we show that heterogeneous input connectivity can prevent the dynamic balance between excitation and inhibition, a hallmark of cortical dynamics, and yield unrealistically sparse and temporally regular firing. Anatomically based estimates of the connectivity of layer 4 (L4) rat barrel cortex and numerical simulations of this circuit indicate that the local network possesses substantial heterogeneity in input connectivity, sufficient to disrupt excitation-inhibition balance. We show that homeostatic plasticity in inhibitory synapses can align the functional connectivity to compensate for structural heterogeneity. Alternatively, spike-frequency adaptation can give rise to a novel state in which local firing rates adjust dynamically so that adaptation currents and synaptic inputs are balanced. This theory is supported by simulations of L4 barrel cortex during spontaneous and stimulus-evoked conditions. Our study shows how synaptic and cellular mechanisms yield fluctuation-driven dynamics despite structural heterogeneity in cortical circuits.

KEYWORDS:

adaptation; balance; cortical networks; dynamics; homeostatic plasticity; inhibition

PMID:
27866797
PMCID:
PMC5158120
DOI:
10.1016/j.neuron.2016.10.027
[Indexed for MEDLINE]
Free PMC Article

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