A calcium-dependent plasticity rule for HCN channels maintains activity homeostasis and stable synaptic learning.

Theoretical and computational frameworks for synaptic plasticity and learning have a long and cherished history, with few parallels within the well-established literature for plasticity of voltage-gated ion channels. In this study, we derive rules for plasticity in the hyperpolarization-activated cy...

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Autores principales:	Suraj Honnuraiah, Rishikesh Narayanan
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2013
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/729703315e1647fcb53379e88a8a49ea
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spelling	oai:doaj.org-article:729703315e1647fcb53379e88a8a49ea2021-11-18T07:58:52ZA calcium-dependent plasticity rule for HCN channels maintains activity homeostasis and stable synaptic learning.1932-620310.1371/journal.pone.0055590https://doaj.org/article/729703315e1647fcb53379e88a8a49ea2013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23390543/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203Theoretical and computational frameworks for synaptic plasticity and learning have a long and cherished history, with few parallels within the well-established literature for plasticity of voltage-gated ion channels. In this study, we derive rules for plasticity in the hyperpolarization-activated cyclic nucleotide-gated (HCN) channels, and assess the synergy between synaptic and HCN channel plasticity in establishing stability during synaptic learning. To do this, we employ a conductance-based model for the hippocampal pyramidal neuron, and incorporate synaptic plasticity through the well-established Bienenstock-Cooper-Munro (BCM)-like rule for synaptic plasticity, wherein the direction and strength of the plasticity is dependent on the concentration of calcium influx. Under this framework, we derive a rule for HCN channel plasticity to establish homeostasis in synaptically-driven firing rate, and incorporate such plasticity into our model. In demonstrating that this rule for HCN channel plasticity helps maintain firing rate homeostasis after bidirectional synaptic plasticity, we observe a linear relationship between synaptic plasticity and HCN channel plasticity for maintaining firing rate homeostasis. Motivated by this linear relationship, we derive a calcium-dependent rule for HCN-channel plasticity, and demonstrate that firing rate homeostasis is maintained in the face of synaptic plasticity when moderate and high levels of cytosolic calcium influx induced depression and potentiation of the HCN-channel conductance, respectively. Additionally, we show that such synergy between synaptic and HCN-channel plasticity enhances the stability of synaptic learning through metaplasticity in the BCM-like synaptic plasticity profile. Finally, we demonstrate that the synergistic interaction between synaptic and HCN-channel plasticity preserves robustness of information transfer across the neuron under a rate-coding schema. Our results establish specific physiological roles for experimentally observed plasticity in HCN channels accompanying synaptic plasticity in hippocampal neurons, and uncover potential links between HCN-channel plasticity and calcium influx, dynamic gain control and stable synaptic learning.Suraj HonnuraiahRishikesh NarayananPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 8, Iss 2, p e55590 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Suraj Honnuraiah Rishikesh Narayanan A calcium-dependent plasticity rule for HCN channels maintains activity homeostasis and stable synaptic learning.
description	Theoretical and computational frameworks for synaptic plasticity and learning have a long and cherished history, with few parallels within the well-established literature for plasticity of voltage-gated ion channels. In this study, we derive rules for plasticity in the hyperpolarization-activated cyclic nucleotide-gated (HCN) channels, and assess the synergy between synaptic and HCN channel plasticity in establishing stability during synaptic learning. To do this, we employ a conductance-based model for the hippocampal pyramidal neuron, and incorporate synaptic plasticity through the well-established Bienenstock-Cooper-Munro (BCM)-like rule for synaptic plasticity, wherein the direction and strength of the plasticity is dependent on the concentration of calcium influx. Under this framework, we derive a rule for HCN channel plasticity to establish homeostasis in synaptically-driven firing rate, and incorporate such plasticity into our model. In demonstrating that this rule for HCN channel plasticity helps maintain firing rate homeostasis after bidirectional synaptic plasticity, we observe a linear relationship between synaptic plasticity and HCN channel plasticity for maintaining firing rate homeostasis. Motivated by this linear relationship, we derive a calcium-dependent rule for HCN-channel plasticity, and demonstrate that firing rate homeostasis is maintained in the face of synaptic plasticity when moderate and high levels of cytosolic calcium influx induced depression and potentiation of the HCN-channel conductance, respectively. Additionally, we show that such synergy between synaptic and HCN-channel plasticity enhances the stability of synaptic learning through metaplasticity in the BCM-like synaptic plasticity profile. Finally, we demonstrate that the synergistic interaction between synaptic and HCN-channel plasticity preserves robustness of information transfer across the neuron under a rate-coding schema. Our results establish specific physiological roles for experimentally observed plasticity in HCN channels accompanying synaptic plasticity in hippocampal neurons, and uncover potential links between HCN-channel plasticity and calcium influx, dynamic gain control and stable synaptic learning.
format	article
author	Suraj Honnuraiah Rishikesh Narayanan
author_facet	Suraj Honnuraiah Rishikesh Narayanan
author_sort	Suraj Honnuraiah
title	A calcium-dependent plasticity rule for HCN channels maintains activity homeostasis and stable synaptic learning.
title_short	A calcium-dependent plasticity rule for HCN channels maintains activity homeostasis and stable synaptic learning.
title_full	A calcium-dependent plasticity rule for HCN channels maintains activity homeostasis and stable synaptic learning.
title_fullStr	A calcium-dependent plasticity rule for HCN channels maintains activity homeostasis and stable synaptic learning.
title_full_unstemmed	A calcium-dependent plasticity rule for HCN channels maintains activity homeostasis and stable synaptic learning.
title_sort	calcium-dependent plasticity rule for hcn channels maintains activity homeostasis and stable synaptic learning.
publisher	Public Library of Science (PLoS)
publishDate	2013
url	https://doaj.org/article/729703315e1647fcb53379e88a8a49ea
work_keys_str_mv	AT surajhonnuraiah acalciumdependentplasticityruleforhcnchannelsmaintainsactivityhomeostasisandstablesynapticlearning AT rishikeshnarayanan acalciumdependentplasticityruleforhcnchannelsmaintainsactivityhomeostasisandstablesynapticlearning AT surajhonnuraiah calciumdependentplasticityruleforhcnchannelsmaintainsactivityhomeostasisandstablesynapticlearning AT rishikeshnarayanan calciumdependentplasticityruleforhcnchannelsmaintainsactivityhomeostasisandstablesynapticlearning
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A calcium-dependent plasticity rule for HCN channels maintains activity homeostasis and stable synaptic learning.

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