Effects of bilateral vestibular deafferentation in rat on hippocampal theta response to somatosensory stimulation, acetylcholine release, and cholinergic neurons in the pedunculopontine tegmental nucleus

Brain Struct Funct. 2017 Sep;222(7):3319-3332. doi: 10.1007/s00429-017-1407-1. Epub 2017 Mar 27.

Abstract

Vestibular dysfunction has been shown to cause spatial memory impairment. Neurophysiological studies indicate that bilateral vestibular loss (BVL), in particular, is associated with an impairment of the response of hippocampal place cells and theta rhythm. However, the specific neural pathways through which vestibular information reaches the hippocampus are yet to be fully elucidated. The aim of the present study was to further investigate the hypothesised 'theta-generating pathway' from the brainstem vestibular nucleus to the hippocampus. BVL, and in some cases, unilateral vestibular loss (UVL), induced by intratympanic sodium arsanilate injections in rats, were used to investigate the effects of vestibular loss on somatosensory-induced type 2 theta rhythm, acetylcholine (ACh) release in the hippocampus, and the number of cholinergic neurons in the pedunculopontine tegmental nucleus (PPTg), an important part of the theta-generating pathway. Under urethane anaesthesia, BVL was found to cause a significant increase in the maximum power of the type 2 theta (3-6 Hz) frequency band compared to UVL and sham animals. Rats with BVL generally exhibited a lower basal level of ACh release than sham rats; however, this difference was not statistically significant. The PPTg of BVL rats exhibited significantly more choline-acetyltransferase (ChAT)-positive neurons than that of sham animals, as did the contralateral PPTg of UVL animals; however, the number of ChAT-positive neurons on the ipsilateral side of UVL animals was not significantly different from sham animals. The results of these studies indicate that parts of the theta-generating pathway undergo a significant reorganisation following vestibular loss, which suggests that this pathway is important for the interaction between the vestibular system and the hippocampus.

Keywords: Acetylcholine; Bilateral vestibular lesions; Hippocampus; Pedunculopontine tegmental nucleus; Rat; Theta rhythm.

MeSH terms

  • Acetylcholine / metabolism
  • Animals
  • Arsanilic Acid / toxicity
  • Cholinergic Neurons / chemistry
  • Cholinergic Neurons / pathology*
  • Disease Models, Animal
  • Electric Stimulation
  • Functional Laterality / physiology*
  • Hippocampus / physiopathology*
  • Linear Models
  • Male
  • Neural Pathways / pathology
  • Pedunculopontine Tegmental Nucleus / cytology*
  • Rats
  • Rats, Wistar
  • Temporal Bone / pathology
  • Theta Rhythm / physiology*
  • Time Factors
  • Vestibular Diseases / chemically induced
  • Vestibular Diseases / pathology*
  • Vestibular Diseases / physiopathology

Substances

  • Acetylcholine
  • Arsanilic Acid