Horizontal Vestibuloocular Reflex Evoked by High-Acceleration Rotations in the Squirrel Monkey. II. Responses After Canal Plugging (original) (raw)
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Ramachandran, Ramnarayan and Stephen G. Lisberger. Transformation of vestibular signals into motor commands in the vestibuloocular reflex pathways of monkeys. . Parallel pathways mediate the rotatory vestibuloocular reflex (VOR). If the VOR undergoes adaptive modification with spectacles that change the magnification of the visual scene, signals in one neural pathway are modified, whereas those in another are not. By recording the responses of vestibular afferents and abducens neurons for vestibular oscillations at frequencies from 0.5 to 50 Hz, we have elucidated how vestibular signals are processed in the modified versus unmodified VOR pathways. For the small stimuli we used (Ϯ15°/s), the afferents with the most regular spontaneous discharge fired throughout the cycle of oscillation even at 50 Hz, whereas afferents with more irregular discharge showed phase locking. For all afferents, the firing rate was in phase with stimulus head velocity at low frequencies and showed progressive phase lead as frequency increased. Sensitivity to head velocity increased steadily as a function of frequency. Abducens neurons showed highly regular spontaneous discharge and very little evidence of phase locking. Their sensitivity to head velocity during the VOR was relatively flat across frequencies; firing rate lagged head velocity at low frequencies and shifted to large phase leads as stimulus frequency increased. When afferent responses were provided as inputs to a two-pathway model of the VOR, the output of the model reproduced the responses of abducens neurons if the unmodified and modified VOR pathways had frequency-dependent internal gains and included fixed time delays of 1.5 and 9 ms. The phase shifts predicted by the model provide fingerprints for identifying brain stem neurons that participate in the modified versus unmodified VOR pathways.
Experimental Brain Research, 2011
To determine whether the COR compensates for the loss of aVOR gain, independent of species, we studied cynomolgus and rhesus monkeys in which all six semicircular canals were plugged. Gains and phases of the aVOR and COR were determined at frequencies ranging from 0.02 to 6 Hz and fit with model-based transfer functions. Following canal plugging in a rhesus monkey, the acute stage aVOR gain was small and there were absent responses to thrusts of yaw rotation. In the chronic state, aVOR behavior was characterized by a cupula/endolymph time constant of ≈0.07 s, responding only to high frequencies of head rotation. COR gains were ≈0 before surgery but increased to ≈0.15 at low frequencies just after surgery; the COR gains increased to ≈0.4 over the next 12 weeks. Nine weeks after surgery, the summated aVOR + COR responses compensated for head velocity in space in the 0.5-3 Hz frequency range. The gains and phases continued to improve until the 35th week, where the combined aVOR + COR stabilized with gains of ≈0.5-0.6 and the phases were compensatory over all frequencies. Two cynomolgus monkeys operated 3-12 years earlier had similar frequency characteristics of the aVOR and COR. The combined aVOR + COR gains were ≈0.4-0.8 with compensatory phases. To achieve gains close to 1.0, other mechanisms may contribute to gaze compensation, especially with the head free. Thus, while there are individual variations in the time of adaptation of the gain and phase parameters, the essential functional organization of the adaption to vestibular lesions is uniform across these species.
Journal of Neurophysiology, 2009
Yakushin, Sergei B., Theodore Raphan, Jun-Ichi Suzuki, Yaresults in three push-pull pairs, right and left lateral (RLLL), suko Arai, and Bernard Cohen. Dynamics and kinematics of the right anterior and left posterior (RALP), and left anterior angular vestibulo-ocular reflex in monkey: effects of canal plugand right posterior (LARP), that code all angular head ging. J. Neurophysiol. 80: 3077-3099, 1998. Horizontal and roll movements. The precise angles of the individual semicircucomponents of the angular vestibulo-ocular reflex (aVOR) were lar canals have been estimated in several studies, which elicited by sinusoidal rotation at frequencies from 0.2 Hz (60Њ/s) indicate that the canal planes form a nonorthogonal basis to 4.0 Hz (É6Њ/s) in cynomolgus monkeys. Animals had both for sensing head acceleration (Blanks et al. 1985; Curthoys lateral canals plugged (VC, vertical canals intact), both lateral et al . 1977; Dickman 1996; Reisine et al. 1985. The canals and one pair of the vertical canals plugged (RALP, right 0022-3077/98 $5.00
Journal of neurophysiology, 2000
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 torsiona...
2010
Ris, Laurence and Emile Godaux. Neuronal activity in the vestib-metries caused by a unilateral labyrinthectomy the driving force for restoration of activity? Here, we addressed these two questions ular nuclei after contralateral or bilateral labyrinthectomy in the alert guinea pig. J. Neurophysiol. 80: 2352Neurophysiol. 80: -2367Neurophysiol. 80: , 1998. In the by studying the spiking behavior of 473 second-order vestibular neurons in the alert guinea pig after a bilateral labyrinthectomy. guinea pig, a unilateral labyrinthectomy is followed by an initial depression and a subsequent restoration of the spontaneous activity In the acute stage, 1 h after bilateral labyrinthectomy, the resting discharge of the second-order vestibular neurons was 16.2 { 22.4 in the neurons of the ipsilateral vestibular nuclei. In two previous works, we have established the time course of these changes in spikes/s. From comparison with the results obtained in the acute stage after a unilateral labyrinthectomy, we inferred that the ipsilat-the alert guinea pig using electrical stimulation as a search stimulus to select the analyzed neurons. The latter criterion was important eral excitatory influence was between two and three times more powerful than the contralateral inhibitory influence. After bilateral to capture the many ipsilateral neurons that are silent at rest during the immediate postlabyrinthectomy stage. Because it is known that labyrinthectomy as well as after unilateral labyrinthectomy, the resting activity of the second-order vestibular neurons returned to a pathway originating from the vestibular nuclei on one side crosses the midline and functionally inhibits the activity of the vestibular normal, reaching 20.8 { 23.1 spikes/s 1 day after the lesion and 38.6 { 21.1 spikes/s 1 wk after the lesion. From this fact, we nuclei on the other side, we investigated in the first part of this study the spiking behavior of the neurons in the vestibular nuclei concluded that the left-right asymmetries caused by a unilateral labyrinthectomy were not the error signals inducing the restoration contralateral to the labyrinthectomy using the same procedure as that used for the ipsilateral neurons. The spiking behavior of 976 of activity. neurons was studied during 4-h recording sessions in intact animals and 1 h, 1 day, 2 days, or 1 wk postlabyrinthectomy. Neurons I N T R O D U C T I O N selected according to the electrical activation criterion were classified further as type I (their firing rate increased during ipsilateral 0022-3077/98 $5.00
Journal of Neurophysiology, 2006
Sadeghi SG, Minor LB, Cullen KE. Response of vestibular-nerve afferents to active and passive rotations under normal conditions and after unilateral labyrinthectomy. . We investigated the possible contribution of signals carried by vestibular-nerve afferents to long-term processes of vestibular compensation after unilateral labyrinthectomy. Semicircular canal afferents were recorded from the contralesional nerve in three macaque monkeys before [horizontal (HC) ϭ 67, anterior (AC) ϭ 66, posterior (PC) ϭ 50] and 1-12 mo after (HC ϭ 192, AC ϭ 86, PC ϭ 57) lesion. Vestibular responses were evaluated using passive sinusoidal rotations with frequencies of 0.5-15 Hz (20 -80°/s) and fast whole-body rotations reaching velocities of 500°/s. Sensitivities to nonvestibular inputs were tested by: 1) comparing responses during active and passive head movements, 2) rotating the body with the head held stationary to activate neck proprioceptors, and 3) encouraging head-restrained animals to attempt to make head movements that resulted in the production of neck torques of Յ2 Nm. Mean resting discharge rate before and after the lesion did not differ for the regular, D (dimorphic)-irregular, or C (calyx)-irregular afferents. In response to passive rotations, afferents showed no change in sensitivity and phase, inhibitory cutoff, and excitatory saturation after unilateral labyrinthectomy. Moreover, head sensitivities were similar during voluntary and passive head rotations and responses were not altered by neck proprioceptive or efference copy signals before or after the lesion. The only significant change was an increase in the proportion of C-irregular units postlesion, accompanied by a decrease in the proportion of regular afferents. Taken together, our findings show that changes in response properties of the vestibular afferent population are not likely to play a major role in the long-term changes associated with compensation after unilateral labyrinthectomy. Allum JH, Yamane M, Pfaltz CR. Long-term modifications of vertical and horizontal vestibulo-ocular reflex dynamics in man. I. After acute unilateral peripheral vestibular paralysis. Acta Otolaryngol 105: 328 -337, 1988. Andre-Deshays C, Revel M, Berthoz A. Eye-head coupling in humans. II. Phasic components. Exp Brain Res 84: 359 -366, 1991. Armand M, Minor LB. Relationship between time-and frequency-domain analyses of angular head movements in the squirrel monkey. J Comput Neurosci 11: 217-239, 2001. Baird RA, Desmadryl G, Fernandez C, Goldberg JM. The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J Neurophysiol 60: 182-203, 1988. Beraneck M, Idoux E, Uno A, Vidal PP, Moore LE, Vibert N. Unilateral labyrinthectomy modifies the membrane properties of contralesional vestibular neurons. J Neurophysiol 92: 1668 -1684, 2004. Bizzi E, Kalil RE, Tagliasco V. Eye-head coordination in monkeys: evidence for centrally patterned organization. Science 173: 452-454, 1971. Boyle R, Highstein SM. Efferent vestibular system in the toadfish: action upon horizontal semicircular canal afferents. J Neurosci 10: 1570 -1582, 1990. Bricout-Berthout A, Caston J, Reber A. Influence of stimulation of auditory and somatosensory systems on the activity of vestibular nuclear neurons in the frog. Brain Behav Evol 24: 21-34, 1984. Bronte-Stewart HM, Lisberger SG. Physiological properties of vestibular primary afferents that mediate motor learning and normal performance of the vestibulo-ocular reflex in monkeys. J Neurosci 14: 1290 -1308, 1994. Caston J, Bricout-Berthout A. Responses to somatosensory input by afferent and efferent neurons in the vestibular nerve of the frog. Brain Behav Evol 24: 135-143, 1984. Cullen KE, 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, Galiana HL. The use of system identification techniques in the analysis of oculomotor burst neuron spike train dynamics. J Comput Neurosci 3: 347-368, 1996. Curthoys IS, Halmagyi GM. Vestibular compensation: a review of the oculomotor, neural, and clinical consequences of unilateral vestibular loss.