Interpreting the meaning of changes in hippocampal volume associated with vestibular loss

Abstract

Many studies have documented cognitive deficits, especially spatial cognitive deficits, in patients with some form of vestibular loss. Almost 20 years ago, hippocampal (HPC) atrophy was reported to be correlated with spatial memory deficits in such patients and the idea has gradually emerged that HPC atrophy may be causally responsible for the cognitive deficits. However, the results of studies of HPC volume following vestibular loss have not always been consistent, and a number of studies have reported no evidence of HPC atrophy. This paper argues that HPC atrophy, if it does occur following vestibular loss, may not be directly, causally responsible for the cognitive deficits, and that it is more likely that rapid functional changes in the HPC are responsible, due to the interruption of the transmission of vestibular information to the HPC. The argument presented here rests on 3 tranches of evidence: (1) Cognitive deficits have been observed in humans even in the absence of HPC atrophy; (2) HPC atrophy has not been reported in animal studies following vestibular loss, despite cognitive deficits; and (3) Animal studies have shown that the interruption of the transmission of vestibular information to the HPC has immediate consequences for HPC place cells, far too quickly to be explained by HPC atrophy. It is possible that HPC atrophy, when it does occur, is related to the longer-term consquences of living with vestibular loss, which are likely to increase circulating cortisol.

Vestibular contribution to spatial orientation and navigation

“…Parahippocampal place area activation may reflect a compensatory visually guided navigation strategy in patients with bilateral vestibular loss. Volumetric brain imaging studies have reported differential results in terms of structural consequences of vestibular loss for hippocampal volume (for a recent review see [ 2 ▪ ]). While single studies showed a global atrophy of the hippocampus [ 28 ] following bilateral vestibular loss, others reported a decrease of volume only in hippocampal subregions [ 43 ▪ , 44 ▪ ], while some studies found no volumetric changes at all [ 35 ▪▪ , 45 ].…”

“…It is currently hypothesized that hippocampal volumetric changes depend on several cofactors such as disease duration, extent of the vestibular lesion, or concomitant hearing loss. It seems that hippocampal volume loss is not a prerequisite nor a core substrate of spatial disorientation but rather a morphological correlate of an enduring loss of hippocampal signal input [ 2 ▪ ].…”

“…Preclinical and clinical studies in the past decades have clearly shown a contribution of vestibular signals to cognitive processes foremost in the domains of spatial orientation, navigation and cognition [ 1 , 2 ▪ ]. Based on theoretical considerations, it is reasonable that target-oriented navigation relies on both allothetic, that is, mostly visual cues from the environment, and idiothetic, that is, vestibular and somatosensory cues for a continuous updating of one's own position in space during active and passive movement [ 3 – 5 ].…”