Central versus peripheral origin of vestibuloocular reflex recovery following semicircular canal plugging in rhesus monkeys

Johns Hopkins University, Baltimore, Maryland, United States
Journal of Neurophysiology (Impact Factor: 2.89). 01/2001; 84(6):3078-82.
Source: PubMed


We have previously shown that there is a slowly progressing, frequency-specific recovery of the gain and phase of the horizontal vestibuloocular reflex (VOR) in rhesus monkeys following plugging of the lateral semicircular canals. The adapted VOR response exhibited both dynamic and spatial characteristics that were distinctly different from responses in intact animals. To discriminate between adaptation or recovery of central versus peripheral origin, we have tested the recovered vestibuloocular responses in three rhesus monkeys in which either one or both coplanar pairs of vertical semicircular canals had been plugged previously by occluding the remaining semicircular canals in a second plugging operation. We measured the spatial tuning of the VOR in two or three different mutually orthogonal planes in response to sinusoidal oscillations (1.1 Hz, +/-5 degrees, +/-35 degrees /s) over a period of 2-3 and 12-14 mo after each operation. Apart from a significant recovery of the torsional/vertical VOR following the first operation we found that these recovered responses were preserved following the second operation, whereas the responses from the newly operated semicircular canals disappeared acutely as expected. In the follow-up period of up to 3 mo after the second operation, responses from the last operated canals showed recovery in two of three animals, whereas the previously recovered responses persisted. The results suggest that VOR recovery following plugging may depend on a regained residual sensitivity of the plugged semicircular canals to angular head acceleration.

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Available from: Anna Lysakowski
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    • "In contrast, many of the neurons that control balance (Nyberg-Hansen and Mascitti, 1964; Petras, 1967; Peterson et al., 1978; Carleton and Carpenter, 1983; Carpenter, 1988) and influence blood pressure (Uchino et al., 1970; Yates et al., 1993; Kerman and Yates, 1998) are located caudally in the vestibular nucleus complex. In addition, the major components of vestibulo-ocular reflexes are dependent on inputs from semicircular canals (Money and Scott, 1962; Suzuki and Cohen, 1964, 1966; Baker et al., 1982; Hess et al., 2000; Sadeghi et al., 2009; Yakushin et al., 2011). Although data are limited, at least some cognitive responses related to vestibular inputs also appear to require inputs from semicircular canals (Muir et al., 2009). "
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    ABSTRACT: Bilateral loss of vestibular inputs affects far fewer patients than unilateral inner ear damage, and thus has been understudied. In both animal subjects and human patients, bilateral vestibular hypofunction (BVH) produces a variety of clinical problems, including impaired balance control, inability to maintain stable blood pressure during postural changes, difficulty in visual targeting of images, and disturbances in spatial memory and navigational performance. Experiments in animals have shown that non-labyrinthine inputs to the vestibular nuclei are rapidly amplified following the onset of BVH, which may explain the recovery of postural stability and orthostatic tolerance that occurs within 10 days. However, the loss of the vestibulo-ocular reflex and degraded spatial cognition appear to be permanent in animals with BVH. Current concepts of the compensatory mechanisms in humans with BVH are largely inferential, as there is a lack of data from patients early in the disease process. Translation of animal studies of compensation for BVH into therapeutic strategies and subsequent application in the clinic is the most likely route to improve treatment. In addition to physical therapy, two types of prosthetic devices have been proposed to treat individuals with bilateral loss of vestibular inputs: those that provide tactile stimulation to indicate body position in space, and those that deliver electrical stimuli to branches of the vestibular nerve in accordance with head movements. The relative efficacy of these two treatment paradigms, and whether they can be combined to facilitate recovery, is yet to be ascertained.
    Full-text · Article · Dec 2011 · Frontiers in Neurology
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    • "This simple model explains the characteristics of the aVOR for low and mid-band frequency responses without the necessity for assuming spatial adaptation of remaining canals (Yakushin et al. 1998). The model also predicts that the gain and phase of the canal responses changed toward normal as the frequency of head rotation increases from 3 to 20 Hz. (Yakushin et al. 1998), a finding confirmed by others (Lasker et al. 1999; Rabbitt et al. 1999; Hess et al. 2000). Changes in the firing rates of canal afferents in the eight nerves observed at different frequencies are consistent with a reduced time constant of the plugged canal (Rabbitt et al. 1999, 2009; Sadeghi et al. 2009). "
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    ABSTRACT: We investigated spatial responses of the aVOR to small and large accelerations in six canal-plugged and lateral canal nerve-sectioned monkeys. The aim was to determine whether there was spatial adaptation after partial and complete loss of all inputs in a canal plane. Impulses of torques generated head thrusts of ≈ 3,000°/s². Smaller accelerations of ≈ 300°/s² initiated the steps of velocity (60°/s). Animals were rotated about a spatial vertical axis while upright (0°) or statically tilted fore-aft up to ± 90°. Temporal aVOR yaw and roll gains were computed at every head orientation and were fit with a sinusoid to obtain the spatial gains and phases. Spatial gains peaked at ≈ 0° for yaw and ≈ 90° for roll in normal animals. After bilateral lateral canal nerve section, the spatial yaw and roll gains peaked when animals were tilted back ≈ 50°, to bring the intact vertical canals in the plane of rotation. Yaw and roll gains were identical in the lateral canal nerve-sectioned monkeys tested with both low- and high-acceleration stimuli. The responses were close to normal for high-acceleration thrusts in canal-plugged animals, but were significantly reduced when these animals were given step stimuli. Thus, high accelerations adequately activated the plugged canals, whereas yaw and roll spatial aVOR gains were produced only by the intact vertical canals after total loss of lateral canal input. We conclude that there is no spatial adaptation of the aVOR even after complete loss of specific semicircular canal input.
    Full-text · Article · Feb 2011 · Experimental Brain Research
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    • "It is thus likely that the UVD in this study precluded vestibular encoding of head motion but produced relatively mild and transient impairments in spontaneous firing of vestibular afferents. Some of the increases in VOR gain after physical plugging of the semicircular canal have been attributed to peripheral rather than central processes (Hess et al. 2000). The finding that Lurcher mice did not show increases in VOR gain indicates that the oculomotor plasticity we measured in this study resulted from central rather than peripheral adaptive mechanisms. "
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    ABSTRACT: Vestibular paradigms are widely used for investigating mechanisms underlying cerebellar motor learning. These include adaptation of the vestibuloocular reflex (VOR) after visual-vestibular mismatch training and vestibular compensation after unilateral damage to the vestibular apparatus. To date, various studies have shown that VOR adaptation may be supported by long-term depression (LTD) at the parallel fiber to Purkinje cell synapse. Yet it is unknown to what extent vestibular compensation may depend on this cellular process. Here we investigated adaptive gain changes in the VOR and optokinetic reflex during vestibular compensation in transgenic mice in which LTD is specifically blocked in Purkinje cells via expression of a peptide inhibitor of protein kinase C (L7-PKCi mutants). The results demonstrate that neither the strength nor the time course of vestibular compensation are affected by the absence of LTD. In contrast, analysis of vestibular compensation in spontaneous mutants that lack a functional olivo-cerebellar circuit (lurchers) shows that this form of motor learning is severely impaired. We conclude that oculomotor plasticity during vestibular compensation depends critically on intact cerebellar circuitry but not on the occurrence of cerebellar LTD.
    Full-text · Article · Oct 2006 · Journal of Neurophysiology
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