During Passive and Active Head Rotations Effects of Canal Plugging on the Vestibuloocular Reflex and Vestibular Nerve Discharge (original) (raw)
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Activity-dependent modulation: a non-linearity in the unilateral vestibulo-ocular reflex pathways
Experimental Brain Research, 2005
It is well established that the vestibulo-ocular reflex (VOR) depends not only on sensory stimulation but also on the behavioral context associated with the stimulation. Recent modeling studies suggested that including a non-linearity in the activation function of the VOR neurons achieves the desired context-dependence for the VOR without resorting to currently assumed complex cortical computations. With the non-linearity, neurons operate as non-linear summers of incoming activity with sensitivities modulated by their activation levels. In this study we examined whether such a nonlinearity exists in the unilateral VOR pathways in behaving monkeys. Acoustic clicks were employed to evoke unilateral VOR responses during fixation, head motion and smooth pursuit. We found that the clickevoked unilateral VOR responses did not simply sum in a linear manner with the eye movements initiated by head or target motion. Instead, the same acoustic click evoked larger eye movements if the ongoing eye movements were in the same direction. We also showed that the interaction between the ongoing eye movement and the click-evoked response was close to being multiplicative. These results revealed a previous unknown nonlinearity in the unilateral VOR pathways, which may have important implications on the neural implementation of the context-dependence for the VOR.
Distinct Patterns of Stimulus Generalization of Increases and Decreases in VOR Gain
Journal of Neurophysiology, 2005
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 synapsespecific, or affect neurons more broadly tuned for head rotation frequency, than the mechanisms supporting increases in gain.
Annals of The New York Academy of Sciences, 2002
Abstract: The horizontal vestibulo-ocular reflex (VOR) evoked by passive, high-acceleration, head-on-body rotations (head thrusts) while viewing a far (124-cm) or near (15-cm) target was recorded (scleral search coil) in four subjects with normal vestibular function and in one subject with unilateral vestibular hypofunction. For responses in the subjects with normal vestibular function, the latency of responses relative to the onset of head movement was 7.5 ± 1.5 ms for the VOR and 21.6 ± 1.2 ms for the vergence-mediated increase in VOR gain. The gain of the VOR at the peak of the velocity response while viewing a far target was 1.01 ± 0.06; while viewing a near target, it was 1.25 ± 0.08 (p <0.003). The responses were modeled with two pathways based on the different latencies. The “far-viewing” pathway was represented by a constant gain term. The “near-viewing” pathway was represented by a first-order lead term, a gain that was dependent on viewing distance, and a delay. Analysis of the responses revealed that the lead term was greater for the adducting than the abducting eye. In the subject with unilateral vestibular hypofunction, ipsilesional responses showed no change in VOR gain with respect to viewing distance. Contralesional responses retained the vergence-dependent increase in gain. A bilateral model was developed based on the data from the subjects with normal vestibular function. Simulations of this model when inputs were eliminated from one side predict the changes observed in the subject with unilateral vestibular hypofunction. The response asymmetries arise because the near-viewing pathway is more susceptible to inhibitory cutoff than is the far-viewing pathway.
Journal of Neurophysiology, 2008
The distinction between sensory inputs that are a consequence of our own actions from those that result from changes in the external world is essential for perceptual stability and accurate motor control. In this study, we investigated whether linear translations are encoded similarly during active and passive translations by the otolith system. Vestibularnerve afferents innervating the saccule or utricle were recorded in alert macaques. Single unit responses were compared during passive whole body, passive head-on-body, and active head-on-body translations (vertical, fore-aft or lateral) to assess the relative influence of neck proprioceptive and efference copy related-signals on translational coding. The response dynamics of utricular and saccular afferents were comparable and similarly encoded head translation during passive whole-body versus head-on-body translations. Furthermore, when monkeys produced active head-on-body translations with comparable dynamics, the responses of both regular and irregular afferents remained comparable to those recorded during passive movements. Our findings refute the proposal that neck proprioceptive and/or efference copy inputs coded by the efferent system function to modulate the responses of the otolith afferents during active movements. We conclude that the vestibular periphery provides faithful information about linear movements of the head in the space coordinates, regardless of whether they are self-or externally-generated. Angelaki DE, and Dickman JD. Spatiotemporal processing of linear acceleration: primary afferent and central vestibular neuron responses. Journal of neurophysiology 84: 2113-2132, 2000. Angelaki DE, Perachio AA, Mustari MJ, and Strunk CL. Role of irregular otolith afferents in the steady-state nystagmus during off-vertical axis rotation. Birinyi A, Straka H, Matesz C, and Dieringer N. Location of dye-coupled second order and of efferent vestibular neurons labeled from individual semicircular canal or otolith organs in the frog. Brain research 921: 44-59, 2001. Blakemore SJ, Wolpert DM, and Frith CD. Central cancellation of self-produced tickle sensation. Nature neuroscience 1: 635-640, 1998. Blakemore SJ, Wolpert DM, and Frith CD. The cerebellum contributes to somatosensory cortical activity during self-produced tactile stimulation. NeuroImage 10: 448-459, 1999. Boyle R, and Highstein SM. Efferent vestibular system in the toadfish: action upon horizontal semicircular canal afferents. J Neurosci 10: 1570-1582, 1990. Brooks J, and Cullen KE. Reference frames and reafference in the rostral fastigial nucleus. Soc Neurosci Abstr 37: 861.2: 2007. Caston J, and Bricout-Berthout A. Responses to somatosensory input by afferent and efferent neurons in the vestibular nerve of the frog. Brain, behavior and evolution 24: 135-143, 1984. Cherif S, Cullen KE, and Galiana HL. An improved method for the estimation of firing rate dynamics using an optimal digital filter. Journal of neuroscience methods 173: 165-181, 2008. 27 Crapse TB, and Sommer MA. Corollary discharge across the animal kingdom. Nat Rev Neurosci 9: 587-600, 2008. Cullen KE. Sensory signals during active versus passive movement. Current opinion in neurobiology 14: 698-706, 2004. Cullen KE, and Minor LB. Semicircular canal afferents similarly encode active and passive head-on-body rotations: implications for the role of vestibular efference. J Neurosci 22: RC226, 2002. Cullen KE, Rey CG, Guitton D, and Galiana HL. The use of system identification techniques in the analysis of oculomotor burst neuron spike train dynamics. Journal of computational neuroscience 3: 347-368, 1996. Curthoys IS, and Markham CH. Convergence of labyrinthine influences on units in the vestibular nuclei of the cat. I. Natural stimulation. Brain research 35: 469-490, 1971. Dickman JD, and Angelaki DE. Vestibular convergence patterns in vestibular nuclei neurons of alert primates. Journal of neurophysiology 88: 3518-3533, 2002. Dickman JD, and Correia MJ. Bilateral communication between vestibular labyrinths in pigeons. Neuroscience 57: 1097-1108, 1993. Fernandez C, and Goldberg JM. Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. Journal of neurophysiology 39: 970-984, 1976a. Fernandez C, and Goldberg JM. Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. II. Directional selectivity and force-response relations. Journal of neurophysiology 39: 985-995, 1976b. Fernandez C, and Goldberg JM. Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics. Journal of neurophysiology 39: 996-1008, 1976c. Fernandez C, Goldberg JM, and Abend WK. Response to static tilts of peripheral neurons innervating otolith organs of the squirrel monkey. Journal of neurophysiology 35: 978-987, 1972.
Differential Sensorimotor Processing of Vestibulo-Ocular Signals during Rotation and Translation
The Journal of Neuroscience, 2001
Rotational and translational vestibulo-ocular reflexes (RVOR and TrVOR) function to maintain stable binocular fixation during head movements. Despite similar functional roles, differences in behavioral, neuroanatomical, and sensory afferent properties suggest that the sensorimotor processing may be partially distinct for the RVOR and TrVOR. To investigate the currently poorly understood neural correlates for the TrVOR, the activities of eye movement-sensitive neurons in the rostral vestibular nuclei were examined during pure translation and rotation under both stable gaze and suppression conditions. Two main conclusions were made. First, the 0.5 Hz firing rates of cells that carry both sensory head movement and motor-like signals during rotation were more strongly related to the oculomotor output than to the vestibular sensory signal during translation. Second, neurons the firing rates of which increased for ipsilaterally versus contralaterally directed eye movements (eye-ipsi and eye-contra cells, respectively) exhibited distinct dynamic properties during TrVOR suppression. Eye-ipsi neurons demonstrated relatively flat dynamics that was similar to that of the majority of vestibular-only neurons. In contrast, eye-contra cells were characterized by low-pass filter dynamics relative to linear acceleration and lower sensitivities than eye-ipsi cells. In fact, the main secondary eye-contra neuron in the disynaptic RVOR pathways (position-vestibular-pause cell) that exhibits a robust modulation during RVOR suppression did not modulate during TrVOR suppression. To explain these results, a simple model is proposed that is consistent with the known neuroanatomy and postulates differential projections of sensory canal and otolith signals onto eye-contra and eye-ipsi cells, respectively, within a shared premotor circuitry that generates the VORs.
Journal of Neuroscience, 2008
Differential adaptation of the linear and nonlinear components of the horizontal vestibuloocular reflex in squirrel monkeys. J Neurophysiol 88: 3534 -3540, 2002; 10.1152/jn.00404.2002. Previous work in squirrel monkeys has demonstrated the presence of linear and nonlinear components to the horizontal vestibuloocular reflex (VOR) evoked by high-acceleration rotations. The nonlinear component is seen as a rise in gain with increasing velocity of rotation at frequencies more than 2 Hz (a velocity-dependent gain enhancement). We have shown that there are greater changes in the nonlinear than linear component of the response after spectacle-induced adaptation. The present study was conducted to determine if the two components of the response share a common adaptive process. The gain of the VOR, in the dark, to sinusoidal stimuli at 4 Hz (peak velocities: 20 -150°/s) and 10 Hz (peak velocities: 20 and 100°/s) was measured pre-and postadaptation. Adaptation was induced over 4 h with ϫ0.45 minimizing spectacles. Sum-of-sines stimuli were used to induce adaptation, and the parameters of the stimuli were adjusted to invoke only the linear or both linear and nonlinear components of the response. Preadaptation, there was a velocity-dependent gain enhancement at 4 and 10 Hz. In postadaptation with the paradigms that only recruited the linear component, there was a decrease in gain and a persistent velocity-dependent gain enhancement (indicating adaptation of only the linear component). After adaptation with the paradigm designed to recruit both the linear and nonlinear components, there was a decrease in gain and no velocity-dependent gain enhancement (indicating adaptation of both components). There were comparable changes in the response to steps of acceleration. We interpret these results to indicate that separate processes drive the adaptation of the linear and nonlinear components of the response.