Changes in compensatory eye movements after unilateral labyrinthectomy in the rabbit (original) (raw)
Related papers
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.
Neck muscle activity after unilateral labyrinthectomy in the alert guinea pig
Experimental Brain Research, 1999
In the guinea pig, lateral deviation of the head is a cardinal symptom of the vestibular syndrome caused by unilateral labyrinthectomy. In the course of recovery from this syndrome (vestibular compensation), lateral deviation of the head disappears completely in 2-3 days. Because this symptom is known to be due to the lesion of the horizontal semicircular canal system, and since obliquus capitis inferior (OCI) muscle is activated predominantly by yaw rotation (horizontal vestibulocollic reflex), we hypothesized that changes in the activity of this muscle could be at least in part responsible for the lateral head deviation caused by unilateral labyrinthectomy. In order to test this hypothesis, electromyographic (EMG) activities of the right and left OCI muscles, as well as eye movements, were recorded in 12 head-fixed alert guinea pigs at various times after left surgical labyrinthectomy (performed with the animals under halothane anesthesia). After the operation, a decrease in tonic EMG activity was observed in the right (contralateral to the lesion) OCI muscle while an increase in tonic EMG activity was detected in the left (ipsilateral) OCI muscle. In addition, phasic changes in EMG activity associated with ocular nystagmic beats occurred in the OCI muscles. These phasic changes were in the opposite direction to those of the tonic changes. There were bursts of activity in the right OCI and pauses in the left OCI. From measurements of rectified averaged EMG activities which took into account both parts (tonic and phasic) of the phenomenon, it was concluded that the labyrinthectomyinduced asymmetry between the activities of the left and right OCI muscles was high enough and lasted long enough to be an important mechanism in the lateral deviation of the head caused by unilateral labyrinthectomy. Exp Brain Res (1999) 124:159-165
The horizontal vestibulo-ocular reflex in the hemilabyrinthectomized guinea-pig
Experimental Brain Research, 1993
The horizontal vestibulo-ocular reflex (HVOR) in the alert guinea-pig elicited by sinusoidal rotations and by velocity steps was studied with scleral search coil measurement between 3 and 7 days (short term) and between 35 and 160 days (long term) after hemilabyrinthectomy. Animals of the short-term group were always tested after spontaneous nystagmus in darkness had disappeared. The HVOR gain in response to sinusoidal rotations (peak angular velocity: 40 deg/s) in the short-term group was bilaterally depressed compared to normal animals. The HVOR phase showed a shift towards larger phase leads over the whole frequency range tested (from 0.05 to 3 Hz). In addition, both the mean number of fast phases per half-cycle of sinusoidal rotation and the mean amplitude were reduced. HVOR responses to velocity steps at a constant acceleration of 300 deg/s 2 up to final velocity (0 to 100 deg/s) and of 1000 deg/s 2 up to final velocity (0 to 300 deg/s) were depressed bilaterally and asymmetrically such that the gain for rotation towards the intact side greatly exceeded that obtained for rotation towards the lesioned side. Finally, the latency of the vestibular responses was increased and the time constant reduced for both sides of rotation. The HVOR gain values for sinusoidal rotations in the long-term group were lower than normal but higher than in the short-term group: they were asymmetric as a result of a greater compensation for rotation towards the intact side. Neither the phase lead nor the HVOR latency and time constant recovered values close to normal. Finally, the mean number of fast phases per half-cycle remained depressed although the mean amplitude recovered. These results demonstrate that in the guinea-pig, the dynamic deficits show a certain degree of recovery after unilateral labyrinthectomy. However, compared to the compensation of the static deficits previously quantified, the rate of recovery is much lower. This suggests that different processes may be involved in the compensation of the static and dynamic deficits.
Journal of Neurophysiology
The role of the otoliths in mammals on the normal angular vestibulo-ocular reflex (VOR) was characterised in an accompanying study based on the Otopetrin1 (Otop1) mouse, which lacks functioning otoliths due to failure to develop otoconia but seems to have otherwise normal peripheral anatomy and neural circuitry. That study showed that otoliths do not contribute to the normal horizontal (rotation about Earth-vertical axis parallel to dorso-ventral axis) and vertical angular VOR (rotation about Earth-vertical axis parallel to inter-aural axis), but do affect gravity context-specific VOR adaptation. By using these animals, we sought to determine whether the otoliths play a role in the angular VOR after unilateral labyrinthectomy when the total canal signal is reduced. In 5 Otop1 and 5 control littermates we measured horizontal and vertical left-ear-down (LED) and (RED) sinusoidal VOR (0.2-10Hz, 20-100°/s) during the early (3-5 days) and plateau (28-32 days) phases of compensation follo...
Neuroscience, 1999
In decerebrate cats after acute hemilabyrinthectomy, the response sensitivity of extracellularly recorded vestibular nuclear neurons on the lesioned and labyrinth-intact sides were examined quantitatively during constant velocity off-vertical axis rotations with an aim to elucidate the functional contribution of otolithic inputs to the ipsilateral and contralateral vestibular nuclei. The bidirectional response sensitivity, d, was determined as the ratio of the gain during clockwise to that during counterclockwise rotations. A continuum of response sensitivity was identified: one-dimensional neurons showed symmetrically bidirectional response patterns, while two-dimensional neurons showed asymmetrically bidirectional patterns that in some cases approached unidirectional patterns with change in velocity. The proportion of two-dimensional neurons was significantly increased after acute hemilabyrinthectomy. Two-dimensional neurons that responded only to one direction of rotation in at least one of the velocities tested were described as unidirectional neurons. This unidirectional response pattern was observed in one-third of the entire neuronal population studied, but not in cats with both labyrinths intact, thus suggesting that such prominent broadly tuned responses are normally masked by converging otolithic inputs from the contralateral side. These neurons were found in higher proportion on the lesioned side than on the labyrinth-intact side. Among the 70% of unidirectional neurons that exhibited bidirectional response at some velocities and unidirectional response at others, prominent shifts in d values (i.e. between 0/∞ and finite values) with velocity can be computed for each neuron. The shifts in d values correlated with large shifts in the response dynamics and spatial orientation as the response pattern changed with velocity. The response orientations of the unidirectional neurons pointed in all directions on the horizontal plane. When all the two-dimensional neurons (i.e. both the unidirectionally and bidirectionally responsive ones) were pooled, imbalances in the distribution of the response orientations and in response gain were found between the ipsilateral-sidedown/head-down half-circle and the contralateral-side-down/head-up half-circle on the labyrinth-intact side, but not on the lesioned side. These results, derived from spatiotemporal processing of gravitational signals, reveal a novel dimension of imbalance between neuronal populations in the two vestibular nuclear complexes after acute lesion of one labyrinth. This feature would provide, on the one hand, deranged cues of spatial orientation and direction during slow head excursions and, on the other, a framework for the dynamic behavioral deficits associated with hemilabyrinthectomy.
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
Data on galvanic-evoked head movements in healthy and unilaterally labyrinthectomized rats
Data in Brief, 2016
In this dataset, we analyzed galvanic-evoked head movements (GEHMs) in the spatial planes of yaw, and roll in normal and unilaterally labyrinthectomized (UL) Wistar rats. The rats were assigned in 4 groups of 10: control, sham, right-UL and left-UL. Bilateral galvanic vestibular stimulation (GVS) was presented by our "ring-shaped electrode" design (see "Short-term galvanic vestibular stimulation promotes functional recovery and neurogenesis in unilaterally labyrinthectomized rats" (M. Shaabani et al., 2016) [1]). Required data were collected through video recording of GEHMs followed by image processing and statistical analysis.