Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as an adaptive filter of natural spike trains.

Short-term synaptic plasticity (STP) is an important mechanism for modifying neural circuits during computation. Although STP is much studied, its role in the processing of complex natural spike patterns is unknown. Here we analyze the responses of excitatory and inhibitory hippocampal synapses to n...

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Main Authors: Vitaly A Klyachko, Charles F Stevens
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2006-07-01
Series:PLoS Biology
Online Access:http://europepmc.org/articles/PMC1479695?pdf=render
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author Vitaly A Klyachko
Charles F Stevens
author_facet Vitaly A Klyachko
Charles F Stevens
author_sort Vitaly A Klyachko
collection DOAJ
description Short-term synaptic plasticity (STP) is an important mechanism for modifying neural circuits during computation. Although STP is much studied, its role in the processing of complex natural spike patterns is unknown. Here we analyze the responses of excitatory and inhibitory hippocampal synapses to natural spike trains at near-physiological temperatures. Our results show that excitatory and inhibitory synapses express complementary sets of STP components that selectively change synaptic strength during epochs of high-frequency discharge associated with hippocampal place fields. In both types of synapses, synaptic strength rapidly alternates between a near-constant level during low activity and another near-constant, but elevated (for excitatory synapses) or reduced (for inhibitory synapses) level during high-frequency epochs. These history-dependent changes in synaptic strength are largely independent of the particular temporal pattern within the discharges, and occur concomitantly in the two types of synapses. When excitatory and feed-forward inhibitory synapses are co-activated within the hippocampal feed-forward circuit unit, the net effect of their complementary STP is an additional increase in the gain of excitatory synapses during high-frequency discharges via selective disinhibition. Thus, excitatory and feed-forward inhibitory hippocampal synapses in vitro act synergistically as an adaptive filter that operates in a switch-like manner and is selective for high-frequency epochs.
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spelling doaj.art-4236fda8a6f8474e9020effc473784162022-12-21T23:28:28ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852006-07-0147e20710.1371/journal.pbio.0040207Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as an adaptive filter of natural spike trains.Vitaly A KlyachkoCharles F StevensShort-term synaptic plasticity (STP) is an important mechanism for modifying neural circuits during computation. Although STP is much studied, its role in the processing of complex natural spike patterns is unknown. Here we analyze the responses of excitatory and inhibitory hippocampal synapses to natural spike trains at near-physiological temperatures. Our results show that excitatory and inhibitory synapses express complementary sets of STP components that selectively change synaptic strength during epochs of high-frequency discharge associated with hippocampal place fields. In both types of synapses, synaptic strength rapidly alternates between a near-constant level during low activity and another near-constant, but elevated (for excitatory synapses) or reduced (for inhibitory synapses) level during high-frequency epochs. These history-dependent changes in synaptic strength are largely independent of the particular temporal pattern within the discharges, and occur concomitantly in the two types of synapses. When excitatory and feed-forward inhibitory synapses are co-activated within the hippocampal feed-forward circuit unit, the net effect of their complementary STP is an additional increase in the gain of excitatory synapses during high-frequency discharges via selective disinhibition. Thus, excitatory and feed-forward inhibitory hippocampal synapses in vitro act synergistically as an adaptive filter that operates in a switch-like manner and is selective for high-frequency epochs.http://europepmc.org/articles/PMC1479695?pdf=render
spellingShingle Vitaly A Klyachko
Charles F Stevens
Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as an adaptive filter of natural spike trains.
PLoS Biology
title Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as an adaptive filter of natural spike trains.
title_full Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as an adaptive filter of natural spike trains.
title_fullStr Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as an adaptive filter of natural spike trains.
title_full_unstemmed Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as an adaptive filter of natural spike trains.
title_short Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as an adaptive filter of natural spike trains.
title_sort excitatory and feed forward inhibitory hippocampal synapses work synergistically as an adaptive filter of natural spike trains
url http://europepmc.org/articles/PMC1479695?pdf=render
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AT charlesfstevens excitatoryandfeedforwardinhibitoryhippocampalsynapsesworksynergisticallyasanadaptivefilterofnaturalspiketrains