Slow integration leads to persistent action potential firing in distal axons of coupled interneurons

Mark E.J. Sheffield; Tyler K. Best; Brett D. Mensh; William L. Kath; Nelson Spruston

doi:10.1038/nn.2728

Slow integration leads to persistent action potential firing in distal axons of coupled interneurons

Mark E.J. Sheffield, Tyler K. Best, Brett D. Mensh, William L. Kath, Nelson Spruston^*

^*Corresponding author for this work

Engineering Sciences and Applied Mathematics

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

103 Scopus citations

Abstract

The conventional view of neurons is that synaptic inputs are integrated on a timescale of milliseconds to seconds in the dendrites, with action potential initiation occurring in the axon initial segment. We found a much slower form of integration that leads to action potential initiation in the distal axon, well beyond the initial segment. In a subset of rodent hippocampal and neocortical interneurons, hundreds of spikes, evoked over minutes, resulted in persistent firing that lasted for a similar duration. Although axonal action potential firing was required to trigger persistent firing, somatic depolarization was not. In paired recordings, persistent firing was not restricted to the stimulated neuron; it could also be produced in the unstimulated cell. Thus, these interneurons can slowly integrate spiking, share the output across a coupled network of axons and respond with persistent firing even in the absence of input to the soma or dendrites.

Original language	English (US)
Pages (from-to)	200-209
Number of pages	10
Journal	Nature neuroscience
Volume	14
Issue number	2
DOIs	https://doi.org/10.1038/nn.2728
State	Published - Feb 2011

Funding

We thank T. Klausberger, S. Layton and M. Wilson for providing in vivo spiking data, and M. Benton, M. Nusbaum and members of the Spruston laboratory for helpful discussion and comments on the manuscript. We also thank E. Grodinsky for interneuron reconstructions. Grant support was provided by the US National Institutes of Health (NS-046064 to N.S. and W.L.K.) and the National Alliance for Research on Schizophrenia and Depression (N.S.). M.E.J.S. was supported by a Presidential Fellowship from Northwestern University.

ASJC Scopus subject areas

General Neuroscience

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title = "Slow integration leads to persistent action potential firing in distal axons of coupled interneurons",

abstract = "The conventional view of neurons is that synaptic inputs are integrated on a timescale of milliseconds to seconds in the dendrites, with action potential initiation occurring in the axon initial segment. We found a much slower form of integration that leads to action potential initiation in the distal axon, well beyond the initial segment. In a subset of rodent hippocampal and neocortical interneurons, hundreds of spikes, evoked over minutes, resulted in persistent firing that lasted for a similar duration. Although axonal action potential firing was required to trigger persistent firing, somatic depolarization was not. In paired recordings, persistent firing was not restricted to the stimulated neuron; it could also be produced in the unstimulated cell. Thus, these interneurons can slowly integrate spiking, share the output across a coupled network of axons and respond with persistent firing even in the absence of input to the soma or dendrites.",

author = "Sheffield, {Mark E.J.} and Best, {Tyler K.} and Mensh, {Brett D.} and Kath, {William L.} and Nelson Spruston",

note = "Funding Information: We thank T. Klausberger, S. Layton and M. Wilson for providing in vivo spiking data, and M. Benton, M. Nusbaum and members of the Spruston laboratory for helpful discussion and comments on the manuscript. We also thank E. Grodinsky for interneuron reconstructions. Grant support was provided by the US National Institutes of Health (NS-046064 to N.S. and W.L.K.) and the National Alliance for Research on Schizophrenia and Depression (N.S.). M.E.J.S. was supported by a Presidential Fellowship from Northwestern University.",

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AB - The conventional view of neurons is that synaptic inputs are integrated on a timescale of milliseconds to seconds in the dendrites, with action potential initiation occurring in the axon initial segment. We found a much slower form of integration that leads to action potential initiation in the distal axon, well beyond the initial segment. In a subset of rodent hippocampal and neocortical interneurons, hundreds of spikes, evoked over minutes, resulted in persistent firing that lasted for a similar duration. Although axonal action potential firing was required to trigger persistent firing, somatic depolarization was not. In paired recordings, persistent firing was not restricted to the stimulated neuron; it could also be produced in the unstimulated cell. Thus, these interneurons can slowly integrate spiking, share the output across a coupled network of axons and respond with persistent firing even in the absence of input to the soma or dendrites.

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Slow integration leads to persistent action potential firing in distal axons of coupled interneurons

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