Balanced synaptic impact via distance-dependent synapse distribution and complementary expression of AMPARs and NMDARs in hippocampal dendrites

Vilas Menon; Timothy F. Musial; Annie Liu; Yael Katz; William L. Kath; Nelson Spruston; Daniel A. Nicholson

doi:10.1016/j.neuron.2013.09.027

Balanced synaptic impact via distance-dependent synapse distribution and complementary expression of AMPARs and NMDARs in hippocampal dendrites

Vilas Menon, Timothy F. Musial, Annie Liu, Yael Katz, William L. Kath, Nelson Spruston^*, Daniel A. Nicholson

^*Corresponding author for this work

Engineering Sciences and Applied Mathematics

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

33 Scopus citations

Abstract

Neuronal computation involves the integration of synaptic inputs that are often distributed over expansive dendritic trees, suggesting the need for compensatory mechanisms that enable spatially disparate synapses to influence neuronal output. In hippocampal CA1 pyramidal neurons, such mechanisms have indeed been reported, which normalize either the ability of distributed synapses to drive action potential initiation in the axon or their ability to drive dendritic spiking locally. Here we report that these mechanisms can coexist, through an elegant combination of distance-dependent regulation of synapse number and synaptic expression of AMPA and NMDA receptors. Together, these complementary gradients allow individual dendrites in both the apical and basal dendritic trees of hippocampal neurons to operate as facile computational subunits capable of supporting both global integration in the soma/axon and local integration in the dendrite.

Original language	English (US)
Pages (from-to)	1451-1463
Number of pages	13
Journal	Neuron
Volume	80
Issue number	6
DOIs	https://doi.org/10.1016/j.neuron.2013.09.027
State	Published - Dec 18 2013

Funding

The authors thank Stephen Smith’s laboratory and John Morrison’s laboratory for help with array tomography and fluorescent dye loading, respectively, and members of the Nicholson and Spruston laboratories for helpful discussions. This work was supported by R01 AG017139, R00 AG031574, and the Charles and M.R. Shapiro Foundation (D.A.N.); T32 AG000269 (T.F.M); and R01 NS046064 (W.L.K. and N.S.), R01 NS077601 (W.L.K. and N.S.), R01 NS035180 (N.S.), and the Howard Hughes Medical Institute (N.S.).

ASJC Scopus subject areas

General Neuroscience

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10.1016/j.neuron.2013.09.027

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title = "Balanced synaptic impact via distance-dependent synapse distribution and complementary expression of AMPARs and NMDARs in hippocampal dendrites",

abstract = "Neuronal computation involves the integration of synaptic inputs that are often distributed over expansive dendritic trees, suggesting the need for compensatory mechanisms that enable spatially disparate synapses to influence neuronal output. In hippocampal CA1 pyramidal neurons, such mechanisms have indeed been reported, which normalize either the ability of distributed synapses to drive action potential initiation in the axon or their ability to drive dendritic spiking locally. Here we report that these mechanisms can coexist, through an elegant combination of distance-dependent regulation of synapse number and synaptic expression of AMPA and NMDA receptors. Together, these complementary gradients allow individual dendrites in both the apical and basal dendritic trees of hippocampal neurons to operate as facile computational subunits capable of supporting both global integration in the soma/axon and local integration in the dendrite.",

author = "Vilas Menon and Musial, {Timothy F.} and Annie Liu and Yael Katz and Kath, {William L.} and Nelson Spruston and Nicholson, {Daniel A.}",

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AU - Menon, Vilas

AU - Musial, Timothy F.

AU - Liu, Annie

AU - Katz, Yael

AU - Kath, William L.

AU - Spruston, Nelson

AU - Nicholson, Daniel A.

N1 - Funding Information: The authors thank Stephen Smith’s laboratory and John Morrison’s laboratory for help with array tomography and fluorescent dye loading, respectively, and members of the Nicholson and Spruston laboratories for helpful discussions. This work was supported by R01 AG017139, R00 AG031574, and the Charles and M.R. Shapiro Foundation (D.A.N.); T32 AG000269 (T.F.M); and R01 NS046064 (W.L.K. and N.S.), R01 NS077601 (W.L.K. and N.S.), R01 NS035180 (N.S.), and the Howard Hughes Medical Institute (N.S.).

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AB - Neuronal computation involves the integration of synaptic inputs that are often distributed over expansive dendritic trees, suggesting the need for compensatory mechanisms that enable spatially disparate synapses to influence neuronal output. In hippocampal CA1 pyramidal neurons, such mechanisms have indeed been reported, which normalize either the ability of distributed synapses to drive action potential initiation in the axon or their ability to drive dendritic spiking locally. Here we report that these mechanisms can coexist, through an elegant combination of distance-dependent regulation of synapse number and synaptic expression of AMPA and NMDA receptors. Together, these complementary gradients allow individual dendrites in both the apical and basal dendritic trees of hippocampal neurons to operate as facile computational subunits capable of supporting both global integration in the soma/axon and local integration in the dendrite.

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Balanced synaptic impact via distance-dependent synapse distribution and complementary expression of AMPARs and NMDARs in hippocampal dendrites

Abstract

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