EphB2 Signaling Is Implicated in Astrocyte-Mediated Parvalbumin Inhibitory Synapse Development

J Neurosci. 2024 Nov 6;44(45):e0154242024. doi: 10.1523/JNEUROSCI.0154-24.2024.

Abstract

Impaired inhibitory synapse development is suggested to drive neuronal hyperactivity in autism spectrum disorders (ASD) and epilepsy. We propose a novel mechanism by which astrocytes control the development of parvalbumin (PV)-specific inhibitory synapses in the hippocampus, implicating ephrin-B/EphB signaling. Here, we utilize genetic approaches to assess functional and structural connectivity between PV and pyramidal cells (PCs) through whole-cell patch-clamp electrophysiology, optogenetics, immunohistochemical analysis, and behaviors in male and female mice. While inhibitory synapse development is adversely affected by PV-specific expression of EphB2, a strong candidate ASD risk gene, astrocytic ephrin-B1 facilitates PV→PC connectivity through a mechanism involving EphB signaling in PV boutons. In contrast, the loss of astrocytic ephrin-B1 reduces PV→PC connectivity and inhibition, resulting in increased seizure susceptibility and an ASD-like phenotype. Our findings underscore the crucial role of astrocytes in regulating inhibitory circuit development and discover a new role of EphB2 receptors in PV-specific inhibitory synapse development.

Keywords: EphB receptor; astrocyte; hippocampus; inhibition; parvalbumin; synapse.

MeSH terms

  • Animals
  • Astrocytes* / metabolism
  • Ephrin-B1 / genetics
  • Ephrin-B1 / metabolism
  • Female
  • Hippocampus / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neural Inhibition / physiology
  • Parvalbumins* / metabolism
  • Pyramidal Cells / metabolism
  • Pyramidal Cells / physiology
  • Receptor, EphB2* / genetics
  • Receptor, EphB2* / metabolism
  • Signal Transduction* / physiology
  • Synapses* / metabolism
  • Synapses* / physiology

Substances

  • Receptor, EphB2
  • Parvalbumins
  • Ephb2 protein, mouse
  • Ephrin-B1