Vagus Nerve Stimulation (VNS) Modulates Synaptic Plasticity in the Infralimbic Cortex via Trk-B Receptor Activation to Reduce Drug-Seeking in Male Rats

J Neurosci. 2024 Jun 5;44(23):e0107242024. doi: 10.1523/JNEUROSCI.0107-24.2024.

Abstract

Drugs of abuse cause changes in the prefrontal cortex (PFC) and associated regions that impair inhibitory control over drug-seeking. Breaking the contingencies between drug-associated cues and the delivery of the reward during extinction learning reduces relapse. Vagus nerve stimulation (VNS) has previously been shown to enhance extinction learning and reduce drug-seeking. Here we determined the effects of VNS-mediated release of brain-derived neurotrophic factor (BDNF) on extinction and cue-induced reinstatement in male rats trained to self-administer cocaine. Pairing 10 d of extinction training with VNS facilitated extinction and reduced drug-seeking behavior during reinstatement. Rats that received a single extinction session with VNS showed elevated BDNF levels in the medial PFC as determined via an enzyme-linked immunosorbent assay. Systemic blockade of tropomyosin receptor kinase B (TrkB) receptors during extinction, via the TrkB antagonist ANA-12, decreased the effects of VNS on extinction and reinstatement. Whole-cell recordings in brain slices showed that cocaine self-administration induced alterations in the ratio of AMPA and NMDA receptor-mediated currents in Layer 5 pyramidal neurons of the infralimbic cortex (IL). Pairing extinction with VNS reversed cocaine-induced changes in glutamatergic transmission by enhancing AMPAR currents, and this effect was blocked by ANA-12. Our study suggests that VNS consolidates the extinction of drug-seeking behavior by reversing drug-induced changes in synaptic AMPA receptors in the IL, and this effect is abolished by blocking TrkB receptors during extinction, highlighting a potential mechanism for the therapeutic effects of VNS in addiction.

Keywords: BDNF; addiction; cocaine; electrophysiology; prefrontal cortex; vagus nerve stimulation.

MeSH terms

  • Animals
  • Brain-Derived Neurotrophic Factor / metabolism
  • Cocaine / administration & dosage
  • Cocaine / pharmacology
  • Drug-Seeking Behavior* / drug effects
  • Drug-Seeking Behavior* / physiology
  • Extinction, Psychological* / drug effects
  • Extinction, Psychological* / physiology
  • Male
  • Neuronal Plasticity* / drug effects
  • Neuronal Plasticity* / physiology
  • Prefrontal Cortex* / drug effects
  • Prefrontal Cortex* / metabolism
  • Prefrontal Cortex* / physiology
  • Rats
  • Rats, Sprague-Dawley*
  • Receptor, trkB* / antagonists & inhibitors
  • Receptor, trkB* / metabolism
  • Self Administration
  • Vagus Nerve Stimulation* / methods

Substances

  • Receptor, trkB
  • Brain-Derived Neurotrophic Factor
  • Cocaine