Conjunctive changes in multiple ion channels mediate activity-dependent intrinsic plasticity in hippocampal granule cells

Summary: Plasticity in the brain is ubiquitous. How do neurons and networks encode new information and simultaneously maintain homeostasis in the face of such ubiquitous plasticity? Here, we unveil a form of neuronal plasticity in rat hippocampal granule cells, which is mediated by conjunctive chang...

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Main Authors: Poonam Mishra, Rishikesh Narayanan
Format: Article
Language:English
Published: Elsevier 2022-03-01
Series:iScience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2589004222001924
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author Poonam Mishra
Rishikesh Narayanan
author_facet Poonam Mishra
Rishikesh Narayanan
author_sort Poonam Mishra
collection DOAJ
description Summary: Plasticity in the brain is ubiquitous. How do neurons and networks encode new information and simultaneously maintain homeostasis in the face of such ubiquitous plasticity? Here, we unveil a form of neuronal plasticity in rat hippocampal granule cells, which is mediated by conjunctive changes in HCN, inward-rectifier potassium, and persistent sodium channels induced by theta-modulated burst firing, a behaviorally relevant activity pattern. Cooperation and competition among these simultaneous changes resulted in a unique physiological signature: sub-threshold excitability and temporal summation were reduced without significant changes in action potential firing, together indicating a concurrent enhancement of supra-threshold excitability. This form of intrinsic plasticity was dependent on calcium influx through L-type calcium channels and inositol trisphosphate receptors. These observations demonstrate that although brain plasticity is ubiquitous, strong systemic constraints govern simultaneous plasticity in multiple components—referred here as plasticity manifolds—thereby providing a cellular substrate for concomitant encoding and homeostasis in engram cells.
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spelling doaj.art-e2b0f044890f4355b71c6d4aa25eeba12022-12-21T20:03:52ZengElsevieriScience2589-00422022-03-01253103922Conjunctive changes in multiple ion channels mediate activity-dependent intrinsic plasticity in hippocampal granule cellsPoonam Mishra0Rishikesh Narayanan1Cellular Neurophysiology Laboratory, Molecular Biophysics Unit, Indian Institute of Science, Bangalore 560012, IndiaCellular Neurophysiology Laboratory, Molecular Biophysics Unit, Indian Institute of Science, Bangalore 560012, India; Corresponding authorSummary: Plasticity in the brain is ubiquitous. How do neurons and networks encode new information and simultaneously maintain homeostasis in the face of such ubiquitous plasticity? Here, we unveil a form of neuronal plasticity in rat hippocampal granule cells, which is mediated by conjunctive changes in HCN, inward-rectifier potassium, and persistent sodium channels induced by theta-modulated burst firing, a behaviorally relevant activity pattern. Cooperation and competition among these simultaneous changes resulted in a unique physiological signature: sub-threshold excitability and temporal summation were reduced without significant changes in action potential firing, together indicating a concurrent enhancement of supra-threshold excitability. This form of intrinsic plasticity was dependent on calcium influx through L-type calcium channels and inositol trisphosphate receptors. These observations demonstrate that although brain plasticity is ubiquitous, strong systemic constraints govern simultaneous plasticity in multiple components—referred here as plasticity manifolds—thereby providing a cellular substrate for concomitant encoding and homeostasis in engram cells.http://www.sciencedirect.com/science/article/pii/S2589004222001924Biological sciencesMolecular physiologyMolecular neuroscienceCellular neuroscience
spellingShingle Poonam Mishra
Rishikesh Narayanan
Conjunctive changes in multiple ion channels mediate activity-dependent intrinsic plasticity in hippocampal granule cells
iScience
Biological sciences
Molecular physiology
Molecular neuroscience
Cellular neuroscience
title Conjunctive changes in multiple ion channels mediate activity-dependent intrinsic plasticity in hippocampal granule cells
title_full Conjunctive changes in multiple ion channels mediate activity-dependent intrinsic plasticity in hippocampal granule cells
title_fullStr Conjunctive changes in multiple ion channels mediate activity-dependent intrinsic plasticity in hippocampal granule cells
title_full_unstemmed Conjunctive changes in multiple ion channels mediate activity-dependent intrinsic plasticity in hippocampal granule cells
title_short Conjunctive changes in multiple ion channels mediate activity-dependent intrinsic plasticity in hippocampal granule cells
title_sort conjunctive changes in multiple ion channels mediate activity dependent intrinsic plasticity in hippocampal granule cells
topic Biological sciences
Molecular physiology
Molecular neuroscience
Cellular neuroscience
url http://www.sciencedirect.com/science/article/pii/S2589004222001924
work_keys_str_mv AT poonammishra conjunctivechangesinmultipleionchannelsmediateactivitydependentintrinsicplasticityinhippocampalgranulecells
AT rishikeshnarayanan conjunctivechangesinmultipleionchannelsmediateactivitydependentintrinsicplasticityinhippocampalgranulecells