Theta frequency background tunes transmission but not summation of spiking responses.

Hippocampal neurons are known to fire as a function of frequency and phase of spontaneous network rhythms, associated with the animal's behaviour. This dependence is believed to give rise to precise rate and temporal codes. However, it is not well understood how these periodic membrane potentia...

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Main Authors: Dhanya Parameshwaran, Upinder S Bhalla
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3561309?pdf=render
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spelling doaj-05785df3dd0d4e92b016ed386f33b9bc2020-11-25T01:57:15ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0181e5560710.1371/journal.pone.0055607Theta frequency background tunes transmission but not summation of spiking responses.Dhanya ParameshwaranUpinder S BhallaHippocampal neurons are known to fire as a function of frequency and phase of spontaneous network rhythms, associated with the animal's behaviour. This dependence is believed to give rise to precise rate and temporal codes. However, it is not well understood how these periodic membrane potential fluctuations affect the integration of synaptic inputs. Here we used sinusoidal current injection to the soma of CA1 pyramidal neurons in the rat brain slice to simulate background oscillations in the physiologically relevant theta and gamma frequency range. We used a detailed compartmental model to show that somatic current injection gave comparable results to more physiological synaptically driven theta rhythms incorporating excitatory input in the dendrites, and inhibitory input near the soma. We systematically varied the phase of synaptic inputs with respect to this background, and recorded changes in response and summation properties of CA1 neurons using whole-cell patch recordings. The response of the cell was dependent on both the phase of synaptic inputs and frequency of the background input. The probability of the cell spiking for a given synaptic input was up to 40% greater during the depolarized phases between 30-135 degrees of theta frequency current injection. Summation gain on the other hand, was not affected either by the background frequency or the phasic afferent inputs. This flat summation gain, coupled with the enhanced spiking probability during depolarized phases of the theta cycle, resulted in enhanced transmission of summed inputs during the same phase window of 30-135 degrees. Overall, our study suggests that although oscillations provide windows of opportunity to selectively boost transmission and EPSP size, summation of synaptic inputs remains unaffected during membrane oscillations.http://europepmc.org/articles/PMC3561309?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Dhanya Parameshwaran
Upinder S Bhalla
spellingShingle Dhanya Parameshwaran
Upinder S Bhalla
Theta frequency background tunes transmission but not summation of spiking responses.
PLoS ONE
author_facet Dhanya Parameshwaran
Upinder S Bhalla
author_sort Dhanya Parameshwaran
title Theta frequency background tunes transmission but not summation of spiking responses.
title_short Theta frequency background tunes transmission but not summation of spiking responses.
title_full Theta frequency background tunes transmission but not summation of spiking responses.
title_fullStr Theta frequency background tunes transmission but not summation of spiking responses.
title_full_unstemmed Theta frequency background tunes transmission but not summation of spiking responses.
title_sort theta frequency background tunes transmission but not summation of spiking responses.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2013-01-01
description Hippocampal neurons are known to fire as a function of frequency and phase of spontaneous network rhythms, associated with the animal's behaviour. This dependence is believed to give rise to precise rate and temporal codes. However, it is not well understood how these periodic membrane potential fluctuations affect the integration of synaptic inputs. Here we used sinusoidal current injection to the soma of CA1 pyramidal neurons in the rat brain slice to simulate background oscillations in the physiologically relevant theta and gamma frequency range. We used a detailed compartmental model to show that somatic current injection gave comparable results to more physiological synaptically driven theta rhythms incorporating excitatory input in the dendrites, and inhibitory input near the soma. We systematically varied the phase of synaptic inputs with respect to this background, and recorded changes in response and summation properties of CA1 neurons using whole-cell patch recordings. The response of the cell was dependent on both the phase of synaptic inputs and frequency of the background input. The probability of the cell spiking for a given synaptic input was up to 40% greater during the depolarized phases between 30-135 degrees of theta frequency current injection. Summation gain on the other hand, was not affected either by the background frequency or the phasic afferent inputs. This flat summation gain, coupled with the enhanced spiking probability during depolarized phases of the theta cycle, resulted in enhanced transmission of summed inputs during the same phase window of 30-135 degrees. Overall, our study suggests that although oscillations provide windows of opportunity to selectively boost transmission and EPSP size, summation of synaptic inputs remains unaffected during membrane oscillations.
url http://europepmc.org/articles/PMC3561309?pdf=render
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