Synaptic plasticity and roles of orexin in distinct domains of the olfactory tubercle

Front Neural Circuits. 2024 Nov 7:18:1473403. doi: 10.3389/fncir.2024.1473403. eCollection 2024.

Abstract

Olfactory behavior is highly plastic, and the olfactory tubercle (OT), a component of the olfactory cortex and ventral striatum, includes anteromedial (amOT) and lateral (lOT) domains with roles in attractive and aversive olfactory behavioral learning, respectively. However, the underlying properties of synaptic plasticity in these domains are incompletely understood. Synaptic plasticity is regulated by multiple signals including synaptic inputs and neuromodulators. Interestingly, the amOT domain exhibits high expression of various receptors for neuromodulators. We investigated synaptic plasticity in mouse OT slices by combining electrical stimulation and treatment with the appetite-promoting neuropeptide orexin, the receptors of which are highly expressed in the amOT. In both the amOT and lOT, one round of 2-Hz burst stimulation elicited short-term potentiation of the field excitatory postsynaptic potential, whereas three rounds of stimulation induced long-term potentiation (LTP) that persisted for 150 min. In the amOT, orexin-A induced LTP was blocked by the orexin receptor type 1 antagonist SB334867. Orexin-A also facilitated LTP induction in the amOT by one round of 2-Hz burst stimulation. By contrast, these effects were not observed in the lOT. These results highlighted the similarity and difference in synaptic plasticity between the OT domains and suggested that orexin facilitates synaptic plasticity in the amOT during olfactory learning processes such as food odor learning.

Keywords: glutamatergic transmission; olfactory cortex; olfactory memory; orexigenic neuromodulator; synaptic plasticity.

MeSH terms

  • Animals
  • Benzoxazoles / pharmacology
  • Electric Stimulation
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • Long-Term Potentiation / drug effects
  • Long-Term Potentiation / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Naphthyridines / pharmacology
  • Neuronal Plasticity* / drug effects
  • Neuronal Plasticity* / physiology
  • Olfactory Tubercle* / drug effects
  • Olfactory Tubercle* / physiology
  • Orexin Receptor Antagonists / pharmacology
  • Orexin Receptors / metabolism
  • Orexin Receptors / physiology
  • Orexins* / metabolism
  • Orexins* / pharmacology
  • Orexins* / physiology
  • Urea / analogs & derivatives

Substances

  • Orexins
  • Orexin Receptors
  • Naphthyridines
  • 1-(2-methylbenzoxazol-6-yl)-3-(1,5)naphthyridin-4-yl urea
  • Benzoxazoles
  • Orexin Receptor Antagonists
  • Urea

Grants and funding

The authors declare that financial support was received for the research, authorship, and/or publication of this article. This work was supported by the JSPS KAKENHI (grant numbers 19H03341, 22H02734, 22K02112, 22K06831, and 24K22038) and Research Grant from Urakami Foundation for Food and Food Culture Promotion.