Asymmetric responses to rotation at high frequencies in central vestibular neurons of the alert cat

Division of Neurology, Department of Medicine, University of Toronto, Toronto, ON, Canada M5T 2S8.
Brain Research (Impact Factor: 2.84). 05/2004; 1005(1-2):137-53. DOI: 10.1016/j.brainres.2004.01.042
Source: PubMed


The horizontal rotatory vestibulo-ocular reflex (VOR) stabilizes gaze by moving the eyes at an angular velocity proportional to head velocity, and can accomplish this for a broad range of frequencies and amplitudes of head motion. Rotation at 5 Hz and above may be processed differently than lower frequencies by the VOR network. We recorded discharges and calculated spike densities of a small sample of vestibular neurons in alert cats during low-velocity rotation at frequencies up to 8 Hz. At high frequencies, we found both vestibular-only (V-only) and eye-movement-sensitive (EM) cells that generated asymmetric output signals. Asymmetry was primarily of the cutoff type, i.e., changes in spike density were smallest for rotation in the inhibitory direction. Most cells were identified as secondary neurons. The mean spike density was 23 sp/s, which was lower than previously reported in vestibular neurons of monkeys. A few neurons had very high sensitivities, associated with phase-locking, to rotation at high frequencies. In general, vestibular neurons carried a high-pass-filtered version of rotational signals. When synaptic inputs from the vestibular commissure were quantified, we found that the immediate change in probability of firing due to commissural vestibular input was inversely correlated with the degree of high-pass filtering. At high frequencies, increased asymmetry and phase-locking occurred in some neurons. A small number of neurons responded with increased probability of firing to both directions of rotation. Together, these observations suggest that high frequencies of rotation may be encoded differently than low frequencies by central vestibular neurons in alert animals.


Available from: Adrian J Priesol, Feb 01, 2014
  • Source
    • "c o m w w w. e l s ev i e r. c o m / l o c a t e / b r a i n r e s many secondary vestibular neurons display cutoff responses (i.e., are silenced during rotation in their off-directions), even at low speeds (Melvill Jones and Milsum, 1970; Newlands and Perachio, 1990a; Escudero et al., 1992; Chen-Huang and McCrea, 1999; Broussard et al., 2004). In awake cats, most central vestibular neurons consistently have asymmetric responses to sinusoidal rotation (Broussard et al., 2004). Primary afferents from the semicircular canal endorgans also are not purely linear in their response characteristics, and irregularly-firing afferents can be silenced during contralateral rotation (Dickman and Correia, 1989; Hullar et al., 2005). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Adaptive rescaling is a widespread phenomenon that dynamically adjusts the input-output relationship of a sensory system in response to changes in the ambient stimulus conditions. Rescaling has been described in the central vestibular neurons of normal cats. After recovery from unilateral vestibular damage, the vestibulo-ocular reflex (VOR) remains nonlinear for rotation toward the damaged side. Therefore, rescaling in the VOR pathway may be especially important after damage. Here, we demonstrate that central vestibular neurons adjust their input-output relationships depending on the input velocity range, suggesting that adaptive rescaling is preserved after vestibular damage and can contribute to the performance of the VOR. We recorded from isolated vestibular neurons in alert cats that had recovered from unilateral vestibular damage. The peak velocity of 1-Hz sinusoidal rotation was varied from 10 to 120 degrees/s and the sensitivities and dynamic ranges of vestibular neurons were measured. Most neuronal responses showed significant nonlinearities even at the lowest peak velocity that we tested. Significant rescaling was seen in the responses of neurons both ipsilateral and contralateral to chronic unilateral damage. On the average, when the peak rotational velocity increased by a factor of 8, the average sensitivity to rotation decreased by roughly a factor of 2. Rescaling did not depend on eye movement signals. Our results suggest that the dynamic ranges of central neurons are extended by rescaling and that, after vestibular damage, adaptive rescaling may act to reduce nonlinearities in the response of the VOR to rotation at high speeds.
    Brain Research 05/2007; 1143(1):132-42. DOI:10.1016/j.brainres.2007.01.104 · 2.84 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Previous studies in humans and animals which have shown that DC galvanic vestibular stimulation (GVS) induces horizontal and torsional eye movements have been interpreted as being due to a preferential activation of primary vestibular afferents innervating the horizontal semicircular canals and otoliths by GVS. The present study sought to determine in guinea pigs whether GVS does indeed selectively activate primary horizontal canal and otolith afferents. Constant-current GVS was passed between electrodes implanted in the tensor-tympani muscle of each middle ear or between electrodes on the skin over the mastoid. During this stimulation, responses from single primary vestibular neurons were recorded extracellularly by glass microelectrodes in Scarpa's ganglion. Afferents from all vestibular sensory regions were activated by both surface and tensor-tympani galvanic stimulation. Tensor tympani GVS was approximately 10 times more effective than surface GVS. At larger current intensities irregularly discharging afferents showed an asymmetrical response: cathodal stimulation resulted in a larger change in firing (increase) than anodal stimulation (decrease), whereas regularly discharging afferents responded symmetrically to the two polarities of GVS. Across all afferents tuned for different types of natural vestibular stimulation, neuronal sensitivity for GVS was found to increase with discharge variability (as indexed by CV*). Anterior canal afferents showed a slightly higher sensitivity than afferents from other vestibular sensory regions. Hence, the present study concluded that GVS activates primary vestibular afferents innervating all sensory regions in a uniform fashion. Therefore, the specific pattern of GVS-induced eye movements reported in previous studies are not due to differential sensitivity between different vestibular sensory regions, but are likely to reflect an involvement of central processing.
    Brain Research Bulletin 10/2004; 64(3):265-71. DOI:10.1016/j.brainresbull.2004.07.008 · 2.72 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Motor learning must be capable of increasing or decreasing the amplitude of movements to meet the demands of the environment. One way to implement such opposite learned changes would be to store them with bidirectional plasticity mechanisms (i.e., long-term potentiation and depression at the same synapses). At the behavioral level, this scheme should result in similar patterns of stimulus generalization of increases and decreases in movement amplitude because the same synapses would be modified but in opposite directions. To test this idea, we quantitatively compared the stimulus generalization of learned increases and decreases in the gain (amplitude) of the vestibuloocular reflex (VOR) in mice and in monkeys. When examined across different sinusoidal frequencies of head rotation, decreases in VOR gain generalized more than increases in gain. This difference was apparent not only in the gain, but also the phase (timing) of the VOR. Furthermore, this difference held when animals were trained with high-frequency rotational stimuli, a manipulation that enhances frequency generalization. Our results suggest that increases and decreases in VOR gain are not exact inverses at the circuit level. At one or more sites, the plasticity mechanisms supporting decreases in VOR gain must be less synapse-specific, or affect neurons more broadly tuned for head rotation frequency, than the mechanisms supporting increases in gain.
    Journal of Neurophysiology 12/2005; 94(5):3092-100. DOI:10.1152/jn.00048.2005 · 2.89 Impact Factor
Show more