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

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...

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Published iniScience Vol. 25; no. 3; p. 103922
Main Authors Mishra, Poonam, Narayanan, Rishikesh
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 18.03.2022
Elsevier
Subjects
Biological sciences
Cellular neuroscience
Molecular neuroscience
Molecular physiology
Molecular neuroscience
Biological sciences
Cellular neuroscience
Molecular physiology
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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. [Display omitted] •Theta-burst firing induces intrinsic plasticity in dentate gyrus granule cells•Changes in HCN, inward-rectifier K+, and persistent Na+ channels mediate plasticity•Ca2+ influx through L-type Ca2+ channels and InsP3 receptors governs plasticity•Intrinsic plasticity could drive encoding and homeostasis in engram cells Biological sciences; Molecular physiology; Molecular neuroscience; Cellular neuroscience
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ISSN:2589-0042
2589-0042
DOI:10.1016/j.isci.2022.103922