scholarly journals Vestibular nucleus neurons respond to hindlimb movement in the conscious cat

2016 ◽  
Vol 116 (4) ◽  
pp. 1785-1794 ◽  
Author(s):  
Andrew A. McCall ◽  
Derek M. Miller ◽  
William M. DeMayo ◽  
George H. Bourdages ◽  
Bill J. Yates

The limbs constitute the sole interface with the ground during most waking activities in mammalian species; it is therefore expected that somatosensory inputs from the limbs provide important information to the central nervous system for balance control. In the decerebrate cat model, the activity of a subset of neurons in the vestibular nuclei (VN) has been previously shown to be modulated by hindlimb movement. However, decerebration can profoundly alter the effects of sensory inputs on the activity of brain stem neurons, resulting in epiphenomenal responses. Thus, before this study, it was unclear whether and how somatosensory inputs from the limb affected the activity of VN neurons in conscious animals. We recorded brain stem neuronal activity in the conscious cat and characterized the responses of VN neurons to flexion and extension hindlimb movements and to whole body vertical tilts (vestibular stimulation). Among 96 VN neurons whose activity was modulated by vestibular stimulation, the firing rate of 65 neurons (67.7%) was also affected by passive hindlimb movement. VN neurons in conscious cats most commonly encoded hindlimb movement irrespective of the direction of movement ( n = 33, 50.8%), in that they responded to all flexion and extension movements of the limb. Other VN neurons overtly encoded information about the direction of hindlimb movement ( n = 27, 41.5%), and the remainder had more complex responses. These data confirm that hindlimb somatosensory and vestibular inputs converge onto VN neurons of the conscious cat, suggesting that VN neurons integrate somatosensory inputs from the limbs in computations that affect motor outflow to maintain balance.

2014 ◽  
Vol 111 (12) ◽  
pp. 2423-2432 ◽  
Author(s):  
Milad S. Arshian ◽  
Candace E. Hobson ◽  
Michael F. Catanzaro ◽  
Daniel J. Miller ◽  
Sonya R. Puterbaugh ◽  
...  

The vestibular nuclei integrate information from vestibular and proprioceptive afferents, which presumably facilitates the maintenance of stable balance and posture. However, little is currently known about the processing of sensory signals from the limbs by vestibular nucleus neurons. This study tested the hypothesis that limb movement is encoded by vestibular nucleus neurons and described the changes in activity of these neurons elicited by limb extension and flexion. In decerebrate cats, we recorded the activity of 70 vestibular nucleus neurons whose activity was modulated by limb movements. Most of these neurons (57/70, 81.4%) encoded information about the direction of hindlimb movement, while the remaining neurons (13/70, 18.6%) encoded the presence of hindlimb movement without signaling the direction of movement. The activity of many vestibular nucleus neurons that responded to limb movement was also modulated by rotating the animal's body in vertical planes, suggesting that the neurons integrated hindlimb and labyrinthine inputs. Neurons whose firing rate increased during ipsilateral ear-down roll rotations tended to be excited by hindlimb flexion, whereas neurons whose firing rate increased during contralateral ear-down tilts were excited by hindlimb extension. These observations suggest that there is a purposeful mapping of hindlimb inputs onto vestibular nucleus neurons, such that integration of hindlimb and labyrinthine inputs to the neurons is functionally relevant.


1988 ◽  
Vol 60 (5) ◽  
pp. 1753-1764 ◽  
Author(s):  
J. Kasper ◽  
R. H. Schor ◽  
V. J. Wilson

1. We have studied, in decerebrate cats, the responses of neurons in the lateral and descending vestibular nuclei to whole-body rotations in vertical planes that activated vertical semicircular canal and utricular receptors. Some neurons were identified as vestibulospinal by antidromic stimulation with floating electrodes placed in C4. 2. The direction of tilt that caused maximal excitation (response vector orientation) of each neuron was determined. Neuron dynamics were then studied with sinusoidal stimuli closely aligned with the response vector orientation, in the range 0.02-1 Hz. A few cells, for which we could not identify a response vector, probably had spatial-temporal convergence. 3. On the basis of dynamics, neurons were classified as receiving their input primarily from vertical semicircular canals, primarily from the otolith organs, or from canal+otolith convergence. 4. Response vector orientations of canal-driven neurons were often near +45 degrees or -45 degrees with respect to the transverse (roll) plane, suggesting these neurons received excitatory input from the ipsilateral anterior or posterior canal, respectively. Some neurons had canal-related dynamics but vector orientations near roll, presumably because they received convergent input from the ipsilateral anterior and posterior canals. Few neurons had their vectors near pitch. 5. In the lateral vestibular nucleus, neurons with otolith organ input (pure otolith or otolith+canal) tended to have vector orientations closer to roll than to pitch. In the descending nucleus the responses were evenly divided between the roll and pitch quadrants. 6. We conclude that most of our neurons have dynamics and response vector orientations that make them good candidates to participate in vestibulospinal reflexes acting on the limbs, but not those acting on the neck.


2004 ◽  
Vol 96 (6) ◽  
pp. 2301-2316 ◽  
Author(s):  
Richard C. Fitzpatrick ◽  
Brian L. Day

Galvanic vestibular stimulation (GVS) is a simple, safe, and specific way to elicit vestibular reflexes. Yet, despite a long history, it has only recently found popularity as a research tool and is rarely used clinically. The obstacle to advancing and exploiting GVS is that we cannot interpret the evoked responses with certainty because we do not understand how the stimulus acts as an input to the system. This paper examines the electrophysiology and anatomy of the vestibular organs and the effects of GVS on human balance control and develops a model that explains the observed balance responses. These responses are large and highly organized over all body segments and adapt to postural and balance requirements. To achieve this, neurons in the vestibular nuclei receive convergent signals from all vestibular receptors and somatosensory and cortical inputs. GVS sway responses are affected by other sources of information about balance but can appear as the sum of otolithic and semicircular canal responses. Electrophysiological studies showing similar activation of primary afferents from the otolith organs and canals and their convergence in the vestibular nuclei support this. On the basis of the morphology of the cristae and the alignment of the semicircular canals in the skull, rotational vectors calculated for every mode of GVS agree with the observed sway. However, vector summation of signals from all utricular afferents does not explain the observed sway. Thus we propose the hypothesis that the otolithic component of the balance response originates from only the pars medialis of the utricular macula.


1996 ◽  
Vol 75 (3) ◽  
pp. 1242-1249 ◽  
Author(s):  
V. J. Wilson ◽  
H. Ikegami ◽  
R. H. Schor ◽  
D. B. Thomson

1. In decerebrate cats with intact cerebellums, we studied the responses of neurons in the caudal areas of the vestibular nuclei to natural vestibular stimulation in vertical planes and to neck rotation. The activity of most neurons was recorded in the caudal half of the descending nucleus. 2. One goal of our experiments was to compare the dynamic and spatial properties of responses to sinusoidal vestibular stimulation with those seen in previous experiments in which the caudal cerebellar vermis, including the nodulus and uvula, was removed. This part of the cerebellum receives vestibular input and projects to the caudal areas of the vestibular nuclei, suggesting that it could influence responses to stimulation of the labyrinth. 3. As in our previous experiments, most neurons could be classified as receiving predominant input either from the otoliths or from one vertical semicircular canal. When mean gain and phase and response vector orientations were compared, there were no obvious differences between the behavior of neurons in the partially decerebellate preparation and the one with the cerebellum intact, demonstrating that in the decerebrate cat the nodulus and uvula have little or no influence on the processing of vertical vestibular input in this region of the vestibular nuclei. 4. Only 23 of 74 (31%) of neurons tested responded to neck rotation. This contrasts with the much larger fractions that respond to this stimulus in Deiters' nucleus and in the rostral descending nucleus. We also recorded from neurons near the vestibular nuclei, mainly in the external cuneate nucleus. All of them (9 of 9) responded to neck rotation. 5. Responses to neck rotation also differed in their dynamics from those found more rostrally in the vestibular nuclei. Dynamics of more rostral neurons resemble those of neck muscle spindles, as do those of external cuneate neurons. The dynamics of caudal vestibular neurons, on the other hand, have a steeper gain slope and more advanced phases than do those of neurons in the more rostral vestibular nuclei. This suggests the possibility of involvement of additional receptors in the production of these responses. 6. In the more rostral vestibular nuclei, responses to vestibular and neck rotation are most often antagonistic, so that head rotation results in little or no response. This is not the case in the caudal areas of the vestibular nuclei, where less than half the neurons tested displayed antagonistic behavior. Further experiments are required to put the neck projection to the caudal vestibular nuclei in a functional context.


2007 ◽  
Vol 98 (3) ◽  
pp. 1549-1565 ◽  
Author(s):  
M. Beraneck ◽  
K. E. Cullen

As a result of the availability of genetic mutant strains and development of noninvasive eye movements recording techniques, the mouse stands as a very interesting model for bridging the gap among behavioral responses, neuronal response dynamics studied in vivo, and cellular mechanisms investigated in vitro. Here we characterized the responses of individual neurons in the mouse vestibular nuclei during vestibular (horizontal whole body rotations) and full field visual stimulation. The majority of neurons (∼2/3) were sensitive to vestibular stimulation but not to eye movements. During the vestibular-ocular reflex (VOR), these neurons discharged in a manner comparable to the “vestibular only” (VO) neurons that have been previously described in primates. The remaining neurons [eye-movement-sensitive (ES) neurons] encoded both head-velocity and eye-position information during the VOR. When vestibular and visual stimulation were applied so that there was sensory conflict, the behavioral gain of the VOR was reduced. In turn, the modulation of sensitivity of VO neurons remained unaffected, whereas that of ES neurons was reduced. ES neurons were also modulated in response to full field visual stimulation that evoked the optokinetic reflex (OKR). Mouse VO neurons, however, unlike their primate counterpart, were not modulated during OKR. Taken together, our results show that the integration of visual and vestibular information in the mouse vestibular nucleus is limited to a subpopulation of neurons which likely supports gaze stabilization for both VOR and OKR.


1996 ◽  
Vol 76 (4) ◽  
pp. 2786-2789 ◽  
Author(s):  
D. B. Thomson ◽  
N. Isu ◽  
V. J. Wilson

1. The central cervical nucleus (CCN) is known to receive neck and vestibular input and to project to the contralateral cerebellum and vestibular nuclei. To investigate the processing of neck and vestibular input by cells in the CCN, we studied their responses to sinusoidal neck rotation and to whole-body tilt in vertical planes in decerebrate, paralyzed cats. CCN neurons were identified by antidromic stimulation with electrodes placed in or near the contralateral restiform body. 2. For every neuron, we first identified the preferred direction of neck rotation (response vector orientation), then studied the neuron's dynamics with rotations in a plane close to this direction at 0.05-1 Hz. 3. Responses of CCN neurons to neck rotation resembled those of previously studied neck spindle primary afferents in terms of their dynamics and nonlinear responses to stimuli of differing amplitudes. They also resembled the neck responses of Deiters' neurons studied in similar preparations. 4. The activity of two-thirds of CCN neurons also was modulated by natural vestibular stimulation. Orientation and dynamics of vestibular responses were characterized in the same way as neck responses. Labyrinthine input originated predominantly from the contralateral vertical canals, and there was no evidence of otolith input. Neck and vestibular inputs were always antagonistic, but the gain of the vestibular response was lower than that of the neck response at all frequencies studied. 5. The quantitative aspects of the interaction between neck and vestibular inputs can be expected to vary with the type of preparation and with stimulus parameters, and its functional significance remains to be investigated.


2019 ◽  
Author(s):  
Derek M. Miller ◽  
Carey D. Balaban ◽  
Andrew A. McCall

1.AbstractWe recently demonstrated in both decerebrate and conscious cat preparations that hindlimb somatosensory inputs converge with vestibular afferent input onto neurons in multiple CNS locations that participate in balance control. While it is known that head position and limb state modulate postural reflexes, presumably through both vestibulospinal and reticulospinal pathways, the combined influence of the two inputs on the activity of neurons in these brainstem regions is unknown. In the present study, we evaluated the responses of vestibular nucleus (VN) neurons to vestibular and hindlimb stimuli delivered separately and together in conscious cats. We hypothesized that VN neuronal firing during activation of vestibular and limb proprioceptive inputs would be well-fit by an additive model. Extracellular single-unit recordings were obtained from neurons in the caudal aspects of the VN. Sinusoidal whole-body rotation in the roll plane was used as the search stimulus. Units responding to the search stimulus were tested for their responses to 10° ramp-and-hold roll body rotation, 10° extension hindlimb movement, and both movements delivered simultaneously. Composite response histograms were fit by a model of low and high pass filtered limb and body position signals using least squares nonlinear regression. We found that VN neuronal activity during combined vestibular and hindlimb proprioceptive stimulation in the conscious cat is well-fit by a simple additive model for signals with similar temporal dynamics. The mean R2 value for goodness of fit across all units was 0.74 ± 0.17. It is likely that VN neurons that exhibit these integrative properties participate in adjusting vestibulospinal outflow in response to limb state.New and NoteworthyVestibular nucleus neurons receive convergent information from hindlimb somatosensory inputs and vestibular inputs. In this study, extracellular single unit recordings of vestibular nucleus neurons during conditions of passively applied limb movement, passive whole-body rotations, and combined stimulation, were well fit by an additive model. The integration of hindlimb somatosensory inputs with vestibular inputs at the first stage of vestibular processing suggests vestibular nucleus neurons account for limb position in determining vestibulospinal responses to postural perturbations.


1989 ◽  
Vol 62 (4) ◽  
pp. 917-923 ◽  
Author(s):  
J. Kasper ◽  
V. J. Wilson ◽  
Y. Yamagata ◽  
B. J. Yates

1. Using floating electrodes, we recorded from neck-muscle spindle afferents in the C2 dorsal root ganglion of the decerebrate cat. Nerves to dorsal neck muscles were cut so that the afferents presumably originated mainly from ventral and ventrolateral perivertebral muscles and sternocleidomastoid. One goal of our experiments was to study possible vestibular influence exerted on these spindles via the fusimotor system. Unparalyzed preparations were therefore used. 2. Stimuli consisted of sinusoidal rotations in vertical planes. Neck tilt stretched neck muscles, whereas whole-body tilt stimulated vestibular receptors. 3. For each afferent we first determined the most effective direction of neck tilt, then used stimuli oriented close to this direction to study response dynamics, particularly gain of responses to stimuli of different amplitudes (0.5-7.5 degrees). 4. Three-quarters of the afferents failed to respond to 0.5 degrees, 0.2-Hz neck rotations. Stimuli that were effective usually elicited responses that had low gain and were linear over the whole range of amplitudes. Only a few afferents had behavior typical of spindle primary afferents: high-gain responses to small sinusoidal stimuli, gain decreasing as stimulus amplitude increases. This prevalence of static spindle responses in the unparalyzed cat is in striking contrast to results obtained on neck-muscle spindles in paralyzed, decerebrate cats, and on hindlimb extensor muscle spindles in decerebrate, unparalyzed cats. 5. Paralysis produced by injection of Flaxedil changed the behavior of 2/4 spindle afferents tested, causing the appearance of high-gain responses to 0.5 degrees stimuli and of nonlinear behavior.(ABSTRACT TRUNCATED AT 250 WORDS)


2006 ◽  
Vol 59 (11-12) ◽  
pp. 585-590 ◽  
Author(s):  
Slobodanka Lemajic-Komazec ◽  
Zoran Komazec

Dizziness is one of the most common reasons patients visit their physicians. Balance control depends on receiving afferent sensory information from several sensory systems: vestibular, optical and proprioceptive. Bioelectric signals, generated by body movements in the semicircular canals and in the otolithic apparatus, are transported via the vestibular nerve to the vestibular nucleus. All four vestibular nuclei, located bilaterally in medial longitudinal fasciculus, are linked with central nervous system structures. These central nervous system structures are involved in maintaining visual stability, spatial orientation and balance control. Nystagmus is a result of afferent signals balance disorders. Nystagmus due to peripheral lesions is conjugate nystagmus, because there is a bilateral central connection. Lesions above the vestibular nuclei induce deficits in synchronization and conjugation of eye movements, thus the nystagmus is dissociated. This paper shows that in peripheral vestibular disorders spontaneous nystagmus is rhythmic, associated, horizontal-rotatory or horizontal, with subjective sensation of dizziness which decreases with time and harmonic signs whose direction coincides with the slow phase of nystagmus and it is associated with mild disorders during pendular stimulation with statistically significant vestibular hypofunction. Spontaneous nystagmus in central vestibular lesions is severe, dissociated, horizontal, rotatory or vertical, without changes related to optical suppression; if vestibular symptoms are present, they are non-harmonic. In central disorders, findings after thermal stimulation are either normal or pathological, with dysrhythmias and inhibition in pendular stimulation. This paper deals with differential diagnosis of vertigo based on anamnesis and clinical examination, as well as objective diagnostic tests. .


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