Inhibitory Postsynaptic Potentials Participate in Intracellular and Extracellular Theta Rhythms in the Hippocampus: A Personal Narrative

IF 2.4 3区 医学 Q3 NEUROSCIENCES Hippocampus Pub Date : 2024-12-13 DOI:10.1002/hipo.23660
L. Stan Leung, Chi Yiu Conrad Yim
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Abstract

The hypothesis that the hippocampal theta rhythm consists of inhibitory postsynaptic potentials (IPSPs) was critical for understanding the theta rhythm. The dominant views in the early 1980s were that intracellularly recorded theta consisted of excitatory postsynaptic potentials (EPSPs) with little participation by IPSPs, and that IPSPs generated a closed monopolar field in the hippocampus. I (Leung) conceived of a new model for generation of the hippocampal theta rhythm, with theta-rhythmic IPSPs as an essential component, and thus sought to reinvestigate the relation between theta and IPSPs quantitatively with intracellular and extracellular recordings. The intracellular recordings were performed by Leung and Yim in the laboratory of Kris Krnjević at McGill University. Using protocols of passing steady-state holding currents and injection of chloride ions, the intracellular theta and IPSP in a CA1 neuron typically showed the same reversal potential and correlated change in amplitude. Low-intensity stimulation of the alveus evoked an antidromic action potential in CA1 neurons, identifying them as pyramidal cells with output axons in the alveus, which then activated a feedback IPSP with almost no excitatory component. Theta-rhythmic somatic inhibition, together with phase-shifted theta-rhythmic distal apical dendritic excitation were proposed as the two dipoles that generate a gradual extracellular theta phase shift in the CA1 apical dendritic layer. The distal apical excitation driven by the entorhinal cortex was proposed to be atropine-resistant and dominated during walking in rats. Other than serving a conventional role in limiting excitation, rhythmic proximal inhibition and distal dendritic excitation provide varying phasic modulation along the soma-dendritic axis of pyramidal cells, resulting in theta phase-dependent synaptic plasticity and gamma oscillations, which are likely involved in cognitive processing.

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抑制性突触后电位参与海马的细胞内和细胞外 Theta 节律:个人叙事。
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来源期刊
Hippocampus
Hippocampus 医学-神经科学
CiteScore
5.80
自引率
5.70%
发文量
79
审稿时长
3-8 weeks
期刊介绍: Hippocampus provides a forum for the exchange of current information between investigators interested in the neurobiology of the hippocampal formation and related structures. While the relationships of submitted papers to the hippocampal formation will be evaluated liberally, the substance of appropriate papers should deal with the hippocampal formation per se or with the interaction between the hippocampal formation and other brain regions. The scope of Hippocampus is wide: single and multidisciplinary experimental studies from all fields of basic science, theoretical papers, papers dealing with hippocampal preparations as models for understanding the central nervous system, and clinical studies will be considered for publication. The Editor especially encourages the submission of papers that contribute to a functional understanding of the hippocampal formation.
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