Location analysis of presynaptically active and silent synapses in single-cultured hippocampal neurons

Front Neural Circuits. 2024 Apr 23:18:1358570. doi: 10.3389/fncir.2024.1358570. eCollection 2024.

Abstract

A morphologically present but non-functioning synapse is termed a silent synapse. Silent synapses are categorized into "postsynaptically silent synapses," where AMPA receptors are either absent or non-functional, and "presynaptically silent synapses," where neurotransmitters cannot be released from nerve terminals. The presence of presynaptically silent synapses remains enigmatic, and their physiological significance is highly intriguing. In this study, we examined the distribution and developmental changes of presynaptically active and silent synapses in individual neurons. Our findings show a gradual increase in the number of excitatory synapses, along with a corresponding decrease in the percentage of presynaptically silent synapses during neuronal development. To pinpoint the distribution of presynaptically active and silent synapses, i.e., their positional information, we employed Sholl analysis. Our results indicate that the distribution of presynaptically silent synapses within a single neuron does not exhibit a distinct pattern during synapse development in different distance from the cell body. However, irrespective of neuronal development, the proportion of presynaptically silent synapses tends to rise as the projection site moves farther from the cell body, suggesting that synapses near the cell body may exhibit higher synaptic transmission efficiency. This study represents the first observation of changes in the distribution of presynaptically active and silent synapses within a single neuron.

Keywords: Sholl analysis; autapse culture; location analysis; silent synapse; single neuron.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cells, Cultured
  • Excitatory Postsynaptic Potentials / physiology
  • Hippocampus* / cytology
  • Hippocampus* / physiology
  • Neurons* / physiology
  • Presynaptic Terminals / physiology
  • Rats
  • Synapses* / physiology
  • Synaptic Transmission / physiology

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was supported by a KAKENHI Grant-in-Aid for Transformative Research Areas (B) “Multicellular Neurobiocomputing” (21H05165), and a KAKENHI Grant-in-Aid for Scientific Research (B) (20H04506, 23H02805, 23H02884, 23H02572, 23K27496, and 23K27263) from the Japan Society for the Promotion of Science.