Move it or lose it—Is stimulation of the vestibular system necessary for normal spatial memory?

Abstract

Studies in both experimental animals and human patients have demonstrated that peripheral vestibular lesions, especially bilateral lesions, are associated with spatial memory impairment that is long-lasting and may even be permanent. Electrophysiological evidence from animals indicates that bilateral vestibular loss causes place cells and theta activity to become dysfunctional; the most recent human evidence suggests that the hippocampus may cause atrophy in patients with bilateral vestibular lesions. Taken together, these studies suggest that self-motion information provided by the vestibular system is important for the development of spatial memory by areas of the brain such as the hippocampus, and when it is lost, spatial memory is impaired. This naturally suggests the converse possibility that activation of the vestibular system may enhance memory. Surprisingly, there is some human evidence that this may be the case. This review considers the relationship between the vestibular system and memory and suggests that the evolutionary age of this primitive sensory system as well as how it detects self-motion (i.e., detection of acceleration vs. velocity) may be the reasons for its unique contribution to spatial memory.

Vestibular stimulation enhances hippocampal long-term potentiation via activation of cholinergic septohippocampal cells

“…Besides participating in formation of spatial memory [3,88,89], septohippocampal cholinergic neurons may also be important for sensorimotor processing in which activation of the vestibular system provides a sensory signal to assist in motor planning [90]. A number of studies have demonstrated that vestibular stimulation can improve cognition in humans (reviewed in [91][92][93]). Given that synaptic plasticity is altered in patients with Alzheimer's disease [94] and degeneration of basal forebrain cholinergic neurons is a pathological hallmark of this disease [14,15,95,96], vestibular stimulation may provide a novel treatment to improve hippocampus-dependent cognitive deficits in affected patients.…”

Acute loss of spatial navigational skills in a case of a right posterior hippocampus stroke

“…Each one of these processes has been studied in rodents, primates, and humans from which several anatomical and behavioral correlates have been described. An example of these anatomical-clinical correlations is that a lesion involving the vestibular system results in decreased volume of the posterior hippocampus that causes impairment of navigational skills [8][9][10][11][12].…”

The thalamocortical vestibular system in animals and humans

“…Other vestibular regions include somatosensory cortex (area 2v, 3av), intraparietal sulcus (area VIP and MIP), posterior parietal cortex (area 7), area MST, frontal cortex (FEF), cingulum (cingulate vestibular cortex) and hippocampus. These regions are involved in various functions ranging from the perception of body rotation and translation, oculomotor and balance control, visual and postural vertical perception, to spatial navigation and memory (Angelaki et al, 2009;Berthoz, 1996;Smith et al, 2010).…”

“…In particular, how animals and human navigate in space -i.e. integrate and memorize the paths taken, elaborate and use cognitive maps of the spatial displacements -has been associated with vestibular processing (Berthoz et al, 1995;Mittelstaedt, 1999;Smith et al, 2010). In addition, vestibular signals, and the neural structures involved in vestibular processing, are crucial for distinguishing self-motion and object-motion (Straube and Brandt, 1987), perceiving the world as upright Mittelstaedt, 1999), elaborating an internal model of gravity and of one's body motion (Angelaki et al, 2004;Merfeld et al, 1999), as well as for visual perception related to gravity (Indovina et al, 2005;Lopez et al, 2009).…”