Nonlinear dendritic integration of electrical and chemical synaptic inputs drives fine-scale correlations

Stuart Trenholm; Amanda J. McLaughlin; David J. Schwab; Maxwell H. Turner; Robert G. Smith; Fred Rieke; Gautam B. Awatramani

doi:10.1038/nn.3851

Nonlinear dendritic integration of electrical and chemical synaptic inputs drives fine-scale correlations

Stuart Trenholm, Amanda J. McLaughlin, David J. Schwab, Maxwell H. Turner, Robert G. Smith, Fred Rieke, Gautam B. Awatramani^*

^*Corresponding author for this work

Physics and Astronomy

Research output: Contribution to journal › Article › peer-review

60 Scopus citations

Abstract

Throughout the CNS, gap junction-mediated electrical signals synchronize neural activity on millisecond timescales via cooperative interactions with chemical synapses. However, gap junction-mediated synchrony has rarely been studied in the context of varying spatiotemporal patterns of electrical and chemical synaptic activity. Thus, the mechanism underlying fine-scale synchrony and its relationship to neural coding remain unclear. We examined spike synchrony in pairs of genetically identified, electrically coupled ganglion cells in mouse retina. We found that coincident electrical and chemical synaptic inputs, but not electrical inputs alone, elicited synchronized dendritic spikes in subregions of coupled dendritic trees. The resulting nonlinear integration produced fine-scale synchrony in the cells' spike output, specifically for light stimuli driving input to the regions of dendritic overlap. In addition, the strength of synchrony varied inversely with spike rate. Together, these features may allow synchronized activity to encode information about the spatial distribution of light that is ambiguous on the basis of spike rate alone.

Original language	English (US)
Pages (from-to)	1759-1766
Number of pages	8
Journal	Nature neuroscience
Volume	17
Issue number	12
DOIs	https://doi.org/10.1038/nn.3851
State	Published - Jan 1 2014

Funding

We thank K. Delaney, A. Pereda and S. Sethuramanujam for their helpful comments on this manuscript, D. Paul for kindly providing the Cx36−/− mice, J. Boyd (University of British Columbia) for his help in writing software for two-photon imaging, and A. Sullivan for maintaining mouse colonies. This work was supported by US National Institutes of Health grants R01-EY022070 (R.G.S.) and R01-EY11850 (F.R.), National Eye Institute grant EY07031 (M.H.T.), the Howard Hughes Medical Institute (F.R.), and by the Canadian Institutes of Health Research (130268-2013, G.B.A.) and Foundation for Fighting Blindness (Canada, G.B.A.).

ASJC Scopus subject areas

General Neuroscience

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10.1038/nn.3851

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abstract = "Throughout the CNS, gap junction-mediated electrical signals synchronize neural activity on millisecond timescales via cooperative interactions with chemical synapses. However, gap junction-mediated synchrony has rarely been studied in the context of varying spatiotemporal patterns of electrical and chemical synaptic activity. Thus, the mechanism underlying fine-scale synchrony and its relationship to neural coding remain unclear. We examined spike synchrony in pairs of genetically identified, electrically coupled ganglion cells in mouse retina. We found that coincident electrical and chemical synaptic inputs, but not electrical inputs alone, elicited synchronized dendritic spikes in subregions of coupled dendritic trees. The resulting nonlinear integration produced fine-scale synchrony in the cells' spike output, specifically for light stimuli driving input to the regions of dendritic overlap. In addition, the strength of synchrony varied inversely with spike rate. Together, these features may allow synchronized activity to encode information about the spatial distribution of light that is ambiguous on the basis of spike rate alone.",

author = "Stuart Trenholm and McLaughlin, {Amanda J.} and Schwab, {David J.} and Turner, {Maxwell H.} and Smith, {Robert G.} and Fred Rieke and Awatramani, {Gautam B.}",

note = "Funding Information: We thank K. Delaney, A. Pereda and S. Sethuramanujam for their helpful comments on this manuscript, D. Paul for kindly providing the Cx36−/− mice, J. Boyd (University of British Columbia) for his help in writing software for two-photon imaging, and A. Sullivan for maintaining mouse colonies. This work was supported by US National Institutes of Health grants R01-EY022070 (R.G.S.) and R01-EY11850 (F.R.), National Eye Institute grant EY07031 (M.H.T.), the Howard Hughes Medical Institute (F.R.), and by the Canadian Institutes of Health Research (130268-2013, G.B.A.) and Foundation for Fighting Blindness (Canada, G.B.A.). Publisher Copyright: {\textcopyright} 2014 Nature America, Inc. All rights reserved.",

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N2 - Throughout the CNS, gap junction-mediated electrical signals synchronize neural activity on millisecond timescales via cooperative interactions with chemical synapses. However, gap junction-mediated synchrony has rarely been studied in the context of varying spatiotemporal patterns of electrical and chemical synaptic activity. Thus, the mechanism underlying fine-scale synchrony and its relationship to neural coding remain unclear. We examined spike synchrony in pairs of genetically identified, electrically coupled ganglion cells in mouse retina. We found that coincident electrical and chemical synaptic inputs, but not electrical inputs alone, elicited synchronized dendritic spikes in subregions of coupled dendritic trees. The resulting nonlinear integration produced fine-scale synchrony in the cells' spike output, specifically for light stimuli driving input to the regions of dendritic overlap. In addition, the strength of synchrony varied inversely with spike rate. Together, these features may allow synchronized activity to encode information about the spatial distribution of light that is ambiguous on the basis of spike rate alone.

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Nonlinear dendritic integration of electrical and chemical synaptic inputs drives fine-scale correlations

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