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Initiation of dendritic NMDA spikes co-regulated via distance-dependent and dynamic distribution of the spine number and morphology in neuron dendrites

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Abstract

Dendritic spines are small membranous protrusions that receive synaptic inputs from other neurons, enabling the initiation of dendritic N-methyl-D-aspartic (NMDA) spikes and somatic action potentials. During learning and memory processes, both the number of spines on a dendrite and the morphology of individual spines are constantly changing. The individual influence of spine number and morphology on dendritic NMDA spikes has already been revealed, but the functional significance of the co-regulation of spine number and morphology on NMDA spikes remains elusive. Here, we systematically investigated the initiation of local dendritic NMDA spikes by the dynamic distributions of the spine number and morphology on single dendrites in reconstructed neuron models. Different from the traditional cognition, we found the threshold number of spines required to generate local dendrite NMDA spikes on distal dendrites is fewer than that on proximal ones, because the thinner distal dendrites own higher impedance. As for the spine morphology, the presence of more α-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid (AMPA) receptors on the spine leads to larger NMDA spikes rather than an increase in the spine dimension alone. Furthermore, we first suggested that a single dendrite containing spines with gradually increasing head diameters away from the soma could generate larger NMDA spikes than that irrational distribution of spine morphology containing spines with decreasing head diameters, which can be compensated by the increasing spine number. Complementarily, the distance-dependent distribution of spine number and morphology co-regulate the intension of dendritic NMDA spikes. These findings about the threshold for NMDA spikes provide novel insights into the role of the irrational dynamic distribution of the spine number and morphology in senescence and disease processes such as Alzheimer’s disease, schizophrenia, and Parkinson’s disease, which causes abnormal neuron firing.

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Authors and Affiliations

  1. State Key Laboratory of Tribology, Department of Mechanical Engineering, Tsinghua University, Beijing, 100084, China

    YuWei Cao & WanLin Guo

  2. State Key Laboratory of Mechanics and Control of Mechanical Structure and Key Laboratory for Intelligent Nano Materials and Devices of the Ministry of Education, Institute for Frontier Science and Institute of Nanoscience, Nanjing University of Aeronautics and Astronautics, Nanjing, 210016, China

    Chun Shen, Hu Qiu & WanLin Guo

Authors
  1. YuWei Cao
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  2. Chun Shen
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  3. Hu Qiu
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  4. WanLin Guo
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Corresponding authors

Correspondence to Chun Shen or WanLin Guo.

Additional information

This work was supported by the National Key Research and Development Program of China (Grant No. 2019YFA0705400), the Natural Science Foundation of Jiangsu Province (Grant No. BK20212008), the National Natural Science Foundation of China (Grant No. 12002158), the Research Fund of State Key Laboratory of Mechanics and Control of Mechanical Structures (Grant Nos. MCMS-I-0421K01, MCMS-I-0422K01), the Fundamental Research Funds for the Central Universities (Grant No. NJ2022002), A Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions.

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The supporting information is available online at https://tech.scichina.com and https://link.springer.com. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors.

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11431_2022_2165_MOESM1_ESM.pdf

Initiation of dendritic NMDA spikes co-regulated via distance-dependent and dynamic distribution of the spine number and morphology in neuron dendrites

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Cao, Y., Shen, C., Qiu, H. et al. Initiation of dendritic NMDA spikes co-regulated via distance-dependent and dynamic distribution of the spine number and morphology in neuron dendrites. Sci. China Technol. Sci. 66, 429–438 (2023). https://doi.org/10.1007/s11431-022-2165-3

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  • DOI: https://doi.org/10.1007/s11431-022-2165-3

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