Comparison between habituation of the cat vestibulo-ocular reflex by velocity steps and sinusoidal vestibular stimulation in the dark

Abstract

Changes in the horizontal vestibulo-ocular reflex (VOR) in darkness were investigated in naive cats during: (1) repeated sessions of angular velocity steps, (2) one continuous 1-h session of sinusoidal oscillations at 0.01, 0.02, 0.04, or 0.12 Hz, and (3) repeated sessions of 1-h sinusoidal oscillations at 0.02 and 0.04 Hz. Before and after each vestibular training, the VOR response parameters elicited by both velocity steps and sinusoidal oscillations were measured in order to evaluate the transfer of habituation from one stimulus to the other. After training with velocity steps, the amplitude and duration of the VOR to velocity steps decreased by about 67% and 52%, respectively. This vestibular habituation transferred to the VOR response generated by sinusoidal oscillations, since a decrease in VOR gain was observed at 0.02 and 0.04 Hz, and an increase in phase lead was observed at 0.02, 0.04, and 0.08 Hz. After 1 h exposure to sinusoidal oscillations, the VOR gain was only reduced by 21-28%, whereas VOR phase lead decreased. The same changes were observed during subsequent sessions, with no retention of the response decrements from one session to the next. At the end of sinusoidal training, the amplitude of the VOR generated by velocity steps was slightly altered. After sinusoidal training, the weak changes in the VOR gain accompanied by a decrease in the VOR phase lead, and the absence of retention of these effects from one session to the next, suggest these changes are not characteristics of a vestibular habituation. Previous reports of vestibular habituation induced by repeated sinusoidal oscillations may be confounded by the fact that the angular velocity steps used for quantifying the effects may have been responsible for this habituation.

Vestibulo-ocular reflex and motion sickness in figure skaters

“…Moreover, during sinusoidal stimulation, we saw a 10°p hase advance in the skaters. Experimental works on VOR habituation in animals also showed a decrease in gain and a increased phase advance (Baloh et al 1982;Blair and Gavin 1979;Clement et al 2002;Jäger and Henn 1981). Similar results were observed in umans performing ballet (Osterhammel et al 1968;Tschiassny 1957) and gymnastics (Quarck and Denise 2005).…”

“…The VOR can be modelled as a Wrst order high-pass linear Wlter entirely deWned by two parameters: gain, the ratio between maximum slow phase eye velocity and head angular velocity, and the time constant of the exponential decrease (TC) (Robinson 1981). Results from experiments on Monkeys, Cats and Humans (Blair and Gavin 1979;Clement et al 2002;Jäger and Henn 1981) show that repeated vestibular stimulations induce a decrease in the gain and a shortening of the TC, a phenomenon known as habituation. An increase in phase advance is also reported during stimulations at sinusoidal velocity ( Fig.…”

The repetition timing of high frequency afferent stimulation drives the bidirectional plasticity at central synapses in the rat medial vestibular nuclei

“…Moreover, induction of LTP or LTD depends on association timing of vestibular afferent HFS and postsynaptic membrane hyperpolarization (McElvain et al, 2010;Menzies et al, 2010), like that driven by the cerebellar gabaergic input during visuovestibular calibration (Lisberger, 1988;du Lac et al, 1995;Lisberger, 1996, 1998;Blazquez et al, 2004;Boyden et al, 2004;Gittis and du Lac, 2006;Masuda and Amari, 2008). However, other plasticity phenomena, for instance vestibular compensation and habituation, might be associated with synaptic LTP or LTD induced by change in the vestibular afferent activity alone (Courjon et al, 1985;Cle´ment et al, 2002;Pettorossi et al, 2003;Lewis et al, 2010). Actually, LTP or LTD may be elicited by different patterns of vestibular afferent HFS in the MVN, through activation of the Nmethyl-D aspartate receptors (NMDARs), without any combined postsynaptic membrane change (Grassi and Pettorossi, 2001;McElvain et al, 2010;Pettorossi et al, 2011b).…”

“…The vestibular system shows various adaptive and compensatory phenomena like visuo-vestibular calibration (Lisberger and Miles, 1980;Miles and Lisberger, 1981;du Lac et al, 1995;Broussard and Kassardjian, 2004), vestibular compensation (Curthoys and Halmagyi, 1995;Cameron and Dutia, 1997;Beraneck et al, 2003), vestibular habituation (Collins, 1973;Jeannerod et al, 1976;Cle´ment et al, 1981Cle´ment et al, , 2002Courjon et al, 1985) and homeostatic processes (Sadeghi et al, 2010). The mechanisms underlying these plasticity phenomena are not completely clarified as yet, but many evidences suggest that synaptic longterm potentiation (LTP) and long-term depression (LTD), as well as neuronal excitability changes, taking place within the medial vestibular nucleus (MVN) might be the neural basis for ocular motor learning (Lisberger, 1988;du Lac et al, 1995;Cameron and Dutia, 1997;Raymond and Lisberger, 1998;Beraneck et al, 2003;Pettorossi et al, 2003;Gittis and du Lac, 2006).…”

The Vestibular Implant

“…While significant habituation has been observed for lowfrequency stimuli (Buettner et al, 1981;Jäger & Henn, 1981a,b;Anastasio, 1997, 1999;Clément et al, 2002), repeated stimulation at higher modulation frequencies shows little or no change in VOR gain (Ito et al, 1974;Jäger & Henn, 1981a;Dow & Anastasio, 1999). Consequently, some authors suggest sinusoidal oscillations should be limited to a few cycles or having a delay between two series of tests (Clément et al, 2002). Other key factors involved in the result of vestibular tests are general level of arousal and instruction set (Wall & Furman, 1989;Weissman et al, 1989;.…”