The Effects of Bilateral Vestibular Loss on Hippocampal Volume, Neuronal Number, and Cell Proliferation in Rats

Abstract

Previous studies in humans have shown that bilateral loss of vestibular function is associated with a significant bilateral atrophy of the hippocampus, which correlated with the patients’ spatial memory deficits. More recently, patients who had recovered from unilateral vestibular neuritis have been reported to exhibit a significant atrophy of the left posterior hippocampus. Therefore, we investigated whether bilateral vestibular deafferentation (BVD) would result in a decrease in neuronal number or volume in the rat hippocampus, using stereological methods. At 16 months post-BVD, we found no significant differences in hippocampal neuronal number or volume compared to sham controls, despite the fact that these animals exhibited severe spatial memory deficits. By contrast, using bromodeoxyuridine (BrdU) as a marker of cell proliferation, we found that the number of BrdU-labeled cells significantly increased in the dentate gyrus of the hippocampus between 48 h and 1 week following BVD. Although a substantial proportion of these cells survived for up to 1 month, the survival rate was significantly lower in BVD animals when compared with that in sham animals. These results suggest a dissociation between the effects of BVD on spatial memory and hippocampal structure in rats and humans, which cannot be explained by an injury-induced increase in cell proliferation.

From ear to uncertainty: vestibular contributions to cognitive function

“…their percentage of correct responses was still significantly below normal (Zheng et al, 2007). This result was recently replicated by Zheng et al (2012a,b), using rats at 4–5 months following BVD (see Figure 3). …”

“…It was speculated that vestibular information must be transmitted to the hippocampus, in order to be integrated with other sensory information relevant to spatial memory (Wiener and Berthoz, 1993; Berthoz, 1996; McNaughton et al, 1996; Etienne and Jeffery, 2004). Ultimately it was reported that place cells in the hippocampus, that respond to specific places in the environment, were modulated by vestibular stimulation (Gavrilov et al, 1995; Wiener et al, 1995), which was supported by numerous animal behavioral studies showing that the disruption of normal vestibular function resulted in spatial memory deficits (Potegal et al, 1977; Horn et al, 1981; Potegal, 1982; Miller et al, 1983; Petrosini, 1984; Mathews et al, 1988, 1989; Semenov and Bures, 1989; Chapuis et al, 1992; Ossenkopp and Hargreaves, 1993; Stackman and Herbert, 2002; Wallace et al, 2002; Russell et al, 2003a; Zheng et al, 2003, 2006, 2007, 2008, 2009a,b, 2012a,b; Baek et al, 2010; Besnard et al, 2012; Machado et al, 2012a,b; Smith et al, 2013). …”

“…Over the last decade in particular, many such studies have been conducted at much longer points after the lesion. Some compensation for the vestibular reflex deficits has occurred in the intervening period and yet the spatial memory deficits still persist (Zheng et al, 2006, 2007, 2008, 2009a,b, 2012a,b; Baek et al, 2010). In the study by Baek et al (2010), which employed the longest post-operative time interval to date, rats that were 14 months post-BVD were more severely impaired in a spatial memory foraging task in darkness than at 5 months post-op.…”

Bilateral Vestibular Hypofunction: Challenges in Establishing the Diagnosis in Adults

“…Also spatial learning and memory are affected by loss of labyrinthine input, probably influenced by the hippocampus, which is subject to functional and structural changes [52,69,70]. A bilateral atrophy of the hippocampus was found in 17% of a BVH population, which correlated with spatial memory deficits [71,72]. The anterior hippocampus is also critically involved in emotional processes.…”

Modulation of immune responses in stress by vestibular stimulation

“…[20,21] Interestingly, normal vestibular functioning is essential for normal functioning of hippocampus. [22,23] Hence, we hypothesized that vestibular stimulation may modulate immune functions through hippocampus. [6] Vestibular stimulation may limit stress induced changes in immunity by inhibiting both the stress axes, as both animal and human studies reported decrease in cortisol and blood pressure followed by vestibular stimulation.…”