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

被引:23
作者
Aitken, Phillip [1 ,2 ]
Zheng, Yiwen [1 ,2 ,3 ,4 ]
Smith, Paul F. [1 ,2 ,3 ,4 ]
机构
[1] Univ Otago, Sch Biomed Sci, Dept Pharmacol & Toxicol, POB 56, Dunedin 9054, New Zealand
[2] Univ Otago, Brain Hlth Res Ctr, POB 56, Dunedin 9054, New Zealand
[3] Univ Auckland, Brain Res New Zealand Ctr Res Excellence, Auckland, New Zealand
[4] Univ Auckland, Eisdell Moore Ctr Hearing & Balance Res, Auckland, New Zealand
关键词
Bilateral vestibular lesions; Hippocampus; Acetylcholine; Theta rhythm; Pedunculopontine tegmental nucleus; Rat; URETHANE-ANESTHETIZED RATS; MESENCEPHALIC RETICULAR-FORMATION; WHOLE-BODY ROTATIONS; BRAIN-STEM; SPATIAL MEMORY; DEVELOPMENTAL-CHANGES; OPTICAL FRACTIONATOR; CUNEIFORM NUCLEUS; MENIERES-DISEASE; WORKING-MEMORY;
D O I
10.1007/s00429-017-1407-1
中图分类号
R602 [外科病理学、解剖学]; R32 [人体形态学];
学科分类号
100101 ;
摘要
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 brain-stem 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.
引用
收藏
页码:3319 / 3332
页数:14
相关论文
共 96 条
[1]   Hippocampal and striatal M1-muscarinic acetylcholine receptors are down-regulated following bilateral vestibular loss in rats [J].
Aitken, Phillip ;
Benoit, Alice ;
Zheng, Yiwen ;
Philoxene, Bruno ;
Le Gall, Anne ;
Denise, Pierre ;
Besnard, Stephane ;
Smith, Paul F. .
HIPPOCAMPUS, 2016, 26 (12) :1509-1514
[2]   VESTIBULAR RESPONSES IN THE MACAQUE PEDUNCULOPONTINE NUCLEUS AND CENTRAL MESENCEPHALIC RETICULAR FORMATION [J].
Aravamuthan, B. R. ;
Angelaki, D. E. .
NEUROSCIENCE, 2012, 223 :183-199
[3]   Evidence that spatial memory deficits following bilateral vestibular deafferentation in rats are probably permanent [J].
Baek, Jean Ha ;
Zheng, Yiwen ;
Darlington, Cynthia L. ;
Smith, Paul F. .
NEUROBIOLOGY OF LEARNING AND MEMORY, 2010, 94 (03) :402-413
[4]   Basal dendritic length is reduced in the rat hippocampus following bilateral vestibular deafferentation [J].
Balabhadrapatruni, Sangeeta ;
Zheng, Yiwen ;
Napper, Ruth ;
Smith, Paul F. .
NEUROBIOLOGY OF LEARNING AND MEMORY, 2016, 131 :56-60
[5]   Prolonged Voluntary Wheel-Running Stimulates Neural Precursors in the Hippocampus and Forebrain of Adult CD1 Mice [J].
Bednarczyk, Matthew R. ;
Aumont, Anne ;
Decary, Simon ;
Bergeron, Raynald ;
Fernandes, Karl J. L. .
HIPPOCAMPUS, 2009, 19 (10) :913-927
[6]   Influence of vestibular input on spatial and nonspatial memory and on hippocampal NMDA receptors [J].
Besnard, S. ;
Machado, M. L. ;
Vignaux, G. ;
Boulouard, M. ;
Coquerel, A. ;
Bouet, V. ;
Freret, T. ;
Denise, P. ;
Lelong-Boulouard, V. .
HIPPOCAMPUS, 2012, 22 (04) :814-826
[7]   The Vestibular System in Cognitive and Memory Processes in Mammalians [J].
Besnard, Stephane ;
Lopez, Christophe ;
Brandt, Thomas ;
Denise, Pierre ;
Smith, Paul F. .
FRONTIERS IN INTEGRATIVE NEUROSCIENCE, 2015, 9
[8]   Vestibular involvement in cognition: Visuospatial ability, attention, executive function, and memory [J].
Bigelow, Robin T. ;
Agrawal, Yuri .
JOURNAL OF VESTIBULAR RESEARCH-EQUILIBRIUM & ORIENTATION, 2015, 25 (02) :73-89
[9]   THE PHYSIOLOGY AND PHARMACOLOGY OF HIPPOCAMPAL-FORMATION THETA RHYTHMS [J].
BLAND, BH .
PROGRESS IN NEUROBIOLOGY, 1986, 26 (01) :1-54
[10]   THE PHARMACOLOGY OF HIPPOCAMPAL THETA-CELLS - EVIDENCE THAT THE SENSORY PROCESSING CORRELATE IS CHOLINERGIC [J].
BLAND, BH ;
SETO, MG ;
SINCLAIR, BR ;
FRASER, SM .
BRAIN RESEARCH, 1984, 299 (01) :121-131