Vestibular cerebellar evoked potentials in humans and their modulation during optokinetic stimulation

Abstract

We recorded evoked potentials (EPs) from over the posterior fossa and in parallel ocular vestibular evoked myogenic potentials (OVEMPs) during visuo-vestibular stimulation in a sample of 7 male and 11 female human subjects. In 9 of the 18 subjects we were able to record EPs reliably in the form of an early biphasic positive-negative wave with latencies ~12 and 17 ms ipsilateral to head acceleration direction (P12-N17) and a slightly later, contralateral, biphasic positive-negative wave with latencies ~19 and 23 ms (P19-N23). The amplitudes of the responses varied widely between subjects. Both P12 and N23 EPs were modulated by the mode of visual stimulation, larger for vection (sense of movement) compared with optokinetic nystagmus and for congruent movement. We suggest that the EPs measured over the posterior fossa are a manifestation of climbing fiber responses of cerebellar cortical Purkinje cells, i.e., a form of vestibular cerebellar EP (VsCEP). The two subject groups with and without VsCEPs were distinguished by the magnitude of their OVEMPs and their subjective experience of vection. The modulation of VsCEPs by visual context may be a manifestation of cerebellar control of linear vestibular ocular reflex gain. NEW & NOTEWORTHY We report likely vestibular cerebellar evoked potentials (VsCEPs) produced by lateral head impulses recorded in intact humans over the posterior fossa. VsCEPs occurred as short-latency P12-N17 waves ipsilateral to the direction of head motion and as P19-N23 contralaterally and were present in half our subjects. Their properties suggest that the VsCEPs may be of a climbing-fiber origin. VsCEPs are related to the perception of motion and, possibly, control of linear vestibular ocular reflex gain.

Vestibular-Evoked Cerebral Potentials

“…Several components with peak latencies between 10 and 20 ms appear to reflect parallel spreading of vestibular information to the cerebellum ( 41 , 108 , 110 , 115 , 120 , 149 ) and to several cortical regions, including the precentral sulcus, the precuneus, and cuneus, as well as several frontal areas ( 108 , 113 , 133 ). The exact origin and differentiation of these potentials remain to be clarified, and their cerebellar and cortical generators need to be disentangled from myogenic contributions ( 41 , 108 , 115 ).…”

“…Our review of the literature shows that short, middle and late VestEPs have been found to originate from various cortical areas at similar or close latencies, such as both frontal and occipital activations at 10 ms, or later at 80 ms, for example. The studies available to date suggest that VestEPs with latencies between 10 and 20 ms may have a cerebellar origin ( 41 , 108 , 110 , 115 , 120 , 149 , 150 ), and/or a cerebral origin with several generators in the precentral sulcus ( 108 ) or the precuneus and cuneus ( 113 ) for the n15. Vestibular-evoked potentials with latencies from 20 to 30 ms have been associated to activity in the bilateral anterior insula and posterior operculum ( 111 ) while components with latencies from 40 to 50 ms have been associated with a mid-cingulate source with contributions of the bilateral superior temporal cortex ( 42 , 110 ).…”

“…Impulsive acceleration stimulation has been used in a few studies to evoke VestEPs, as it creates rapid and highly reproducible translational accelerations up to 0.2 g ( 108 , 120 ). However, IAS activates the somatosensory and auditory systems and can cause small head movements creating artifacts in fMRI and EEG studies.…”

“…Vestibular-evoked potentials with a latency below 10 ms have been related to signal conduction in the vestibular nerve and vestibular information processing in the vestibular nuclei ( 40 , 56 , 57 , 104 – 106 , 109 , 132 , 133 , 146 , 147 ). Vestibular-evoked potentials with a peak latency between 10 and 20 ms have been attributed to myogenic, cerebellar or cortical sources ( 41 , 42 , 56 , 57 , 107 , 108 , 110 , 113 – 115 , 120 , 133 , 148 – 150 ). In this section, we describe the short latency components that emerge across the studies and briefly discuss their origin.…”

“…Responses with a peak latency of 10–20 ms may be myogenic, but also reveal a rapid spreading of vestibular information to the cerebellum and cerebral cortex. To our knowledge, only one group documented cerebellar VestEPs in humans ( 41 , 108 , 110 , 115 , 120 , 149 , 150 ). Of note, short latency VestEPs were evoked by SVS or IAS at the mastoids, both techniques targeting the otolithic receptors, so that we lack information about the potential cerebellar evoked responses to semicircular canal stimulation.…”