Inhibitory Neurons Marked by the Connectivity Molecule Kirrel3 Regulate Memory Precision

J Neurosci. 2025 Sep 17;45(38):e1760242025. doi: 10.1523/JNEUROSCI.1760-24.2025.

Abstract

The homophilic adhesion molecule Kirrel3 drives synapse formation between dentate granule (DG) neurons and GABA neurons, and Kirrel3 gene variants are associated with neurodevelopmental disorders in humans. However, the circuit function and behavioral relevance of Kirrel3-expressing neurons are unknown. Using intersectional genetics, we identified a population of Kirrel3-expressing GABA neurons that regulate memory discrimination in male and female mice. Using chemogenetics with in vivo electrophysiology and behavioral assays, we discovered that activating Kirrel3-expressing GABA neurons, but not parvalbumin neurons, potently inhibits CA3 neuron activity and impairs contextual memory discrimination during recall, revealing a critical role for these neurons in the retrieval of precise memories. Light and electron microscopy of Kirrel3-expressing GABA neurons suggests that they receive direct excitation from DG neurons and project onto CA3 dendrites. Together, this multiscale approach demonstrates how cell type-specific expression of adhesion molecules mark subsets of neurons that control key features guiding memory and behavior.

Keywords: CA3; Kirrel3; inhibitory neuron; memory discrimination; memory generalization; mossy fiber synapse.

MeSH terms

  • Animals
  • CA3 Region, Hippocampal / cytology
  • CA3 Region, Hippocampal / physiology
  • Female
  • GABAergic Neurons* / metabolism
  • GABAergic Neurons* / physiology
  • Male
  • Membrane Proteins* / genetics
  • Memory* / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neural Inhibition* / physiology
  • Potassium Channels, Inwardly Rectifying* / genetics
  • Potassium Channels, Inwardly Rectifying* / metabolism
  • Potassium Channels, Inwardly Rectifying* / physiology

Substances

  • Kirrel3 protein, mouse
  • Potassium Channels, Inwardly Rectifying
  • Membrane Proteins