Responses of neurons of the cat central cervical nucleus to natural neck and vestibular stimulation

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.

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.


1984 ◽  
Vol 51 (3) ◽  
pp. 567-577 ◽  
Author(s):  
V. J. Wilson ◽  
K. Ezure ◽  
S. J. Timerick

In order to investigate the neural basis of the tonic neck reflex, we studied the response of neurons in the cervical spinal cord of decerebrate, paralyzed cats to neck rotation about the longitudinal axis (roll), to vestibular stimulation produced by roll tilt, and to a combination of these stimuli. Most neurons were outside the motoneuron nuclei and were arbitrarily classified as interneurons. Three types of preparation were used--one with intact labyrinths, one acutely labyrinthectomized, and one with acute spinal transection. The activity of 115 neurons recorded extracellularly was modulated by sinusoidal neck rotation in the range 0.02-4 Hz; their behavior was sufficiently linear for sinusoidal analysis. The phase and gain of the responses of neurons in all three preparations were similar except that the absolute gain in cats with intact labyrinths was higher than that of the others. The location of neurons in segments C4-C8 was mainly in laminae 7-8. Some neurons were excited by rotation of the chin to the ipsilateral side (type I) and others by contralateral chin rotation (type II). The dynamic behavior of type I and type II neurons was the same; phase was flat over most of the frequency range and close to the phase of peak neck rotation, while gain enhancement occurred at higher frequencies. This behavior was similar to that of the neckforelimb reflex evoked in unparalyzed intact-labyrinth and labyrinthectomized cats. In cats with intact labyrinths, vestibular input to neurons whose activity was modulated by the neck stimulus was studied using whole-body roll tilt. Many neurons received otolith input; some received canal input. Neck and vestibular inputs to spinal neurons always had opposite polarities (complementary inputs). Thus, type I neurons were always excited by tilt to the ipsilateral side (ipsilateral ear down) while type II neurons were excited by tilt to the contralateral side. Combined neck and vestibular stimulation indicated that the dynamic behavior of neurons was determined by a linear summation of the responses to these stimuli. Interaction of neck and vestibular input at the neuron level was similar to that observed previously at the reflex level in forelimb extensor muscles.(ABSTRACT TRUNCATED AT 400 WORDS)


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.


1990 ◽  
Vol 64 (6) ◽  
pp. 1695-1703 ◽  
Author(s):  
V. J. Wilson ◽  
Y. Yamagata ◽  
B. J. Yates ◽  
R. H. Schor ◽  
S. Nonaka

1. To compare the properties of the vestibulocollic reflex (VCR) with those of vestibular neurons projecting to the neck [vestibulocollic (VC) neurons], we have studied the behavior of the latter in the decerebrate cat. Neurons were identified by their antidromic responses to stimulation in C1-C2, but not C5. Responses to stimulation of vestibular and neck receptors were produced by rotation of the body and head in vertical planes. 2. We determined the plane of whole body (vestibular) or body with head counter-rotated (neck) rotation, which produced the maximal modulation of each neuron (response vector orientation). Neuron dynamics were then studied with sinusoidal (0.02–2 Hz) stimuli aligned with this orientation. 3. On the basis of dynamics and vector orientation, the neuron was assigned a vestibular input classification of otolith, vertical canal, otolith + canal, or spatial-temporal convergence (STC). 4. The properties of this sample of VC neurons are similar to those of a larger population of vestibular neurons whose projection was not identified. For example, the distributions of cells with different types of vestibular inputs were roughly the same; in particular, few cells showed STC responses. In addition, there was no evidence of significant convergence of like canals across the midline (e.g., right anterior + left anterior). 5. Also similar to the larger unidentified population, 80% of VC neurons tested for neck input received such an input. The neck and vestibular responses tended to be antagonistic; the vector orientations were usually opposite, and the response gains and phases similar.(ABSTRACT TRUNCATED AT 250 WORDS)


1993 ◽  
Vol 70 (3) ◽  
pp. 938-946 ◽  
Author(s):  
B. J. Yates ◽  
T. Goto ◽  
I. Kerman ◽  
P. S. Bolton

1. Over two thirds of caudal medullary raphespinal neurons respond to electrical stimulation of the vestibular nerve, and it has been suggested that these neurons may participate in the generation of vestibulospinal and vestibulosympathetic reflexes. The objective of the present study was to determine which vestibular endorgans (semicircular canals or otolith organs) provide inputs to these cells. 2. Experiments were conducted on decerebrate cats that were baroreceptor denervated and vagotomized, and that had a cervical spinal cord transection so that inputs from tilt-sensitive receptors outside of the labyrinth did not influence the units we recorded. 3. In most experiments, vertical vestibular stimulation was used to stimulate the anterior and posterior semicircular canals and the otolith organs. The plane of whole body rotation that produced maximal modulation of a neuron's firing rate (response vector orientation) was measured at one or more frequencies between 0.1 and 0.5 Hz. Neuron dynamics were then studied with sinusoidal (0.02-1 Hz) stimuli aligned with this orientation. Alternatively, in two animals horizontal rotations at 0.5 and 1.0 Hz were employed to stimulate the horizontal semicircular canals. 4. The properties of raphespinal neurons were similar to those of a larger sample of raphe neurons studied that either could not be antidromically activated from the cervical spinal cord or were not tested for a spinal projection. In response to vertical vestibular stimulation, > 85% of caudal medullary raphe neurons had response gains that remained relatively constant across stimulus frequencies, like regularly firing otolith afferents.(ABSTRACT TRUNCATED AT 250 WORDS)


1994 ◽  
Vol 71 (6) ◽  
pp. 2087-2092 ◽  
Author(s):  
B. J. Yates ◽  
A. D. Miller

1. To study the properties of vestibulosympathetic reflexes we recorded outflow from the splanchnic nerve during natural vestibular stimulation in multiple vertical planes in decerebrate cats. Most of the animals were cerebellectomized, although some responses were recorded in cerebellum-intact preparations. Vestibular stimulation was produced by rotating the head in animals whose upper cervical dorsal roots were transected to remove inputs from neck receptors; a baroreceptor denervation and vagotomy were also performed to remove visceral inputs. 2. The plane of head rotation that produced maximal modulation of splanchnic nerve activity (response vector orientation) was measured at 0.2–0.5 Hz. The dynamics of the response were then studied with sinusoidal (0.05- to 1-Hz) stimuli aligned with this orientation. 3. Typically, maximal modulation of splanchnic nerve outflow was elicited by head rotations in a plane near pitch; nose-up rotations produced increased outflow and nose-down rotations reduced nerve discharges. The gains of the responses remained relatively constant across stimulus frequencies and the phases were consistently near stimulus position, like regularly firing otolith afferents. Similar response dynamics were recorded in cerebellectomized and cerebellum-intact animals. 4. The splanchnic nerve responses to head rotation could be abolished by microinjections of the excitotoxin kainic acid into the medial and inferior vestibular nuclei, which is concordant with the responses resulting from activation of vestibular receptors. 5. The properties fo vestibulosympathetic reflexes recorded from the splanchnic nerve support the hypothesis that the vestibular system participates in compensating for posturally related changes in blood pressure.


1985 ◽  
Vol 54 (1) ◽  
pp. 123-133 ◽  
Author(s):  
I. Suzuki ◽  
S. J. Timerick ◽  
V. J. Wilson

In decerebrate cats, we have studied the response of neurons in the L3-L6 segments of the spinal cord to stimulation of neck and vestibular receptors. Neck receptors were stimulated by head rotation in labyrinthectomized cats or by body rotation with the head fixed in labyrinth-intact cats. Vestibular receptors were stimulated by whole-body tilt in the latter preparation. Most neurons were located outside the motoneuron nuclei and were arbitrarily classified as interneurons. Combinations of roll and pitch stimuli at frequencies of 0.1 or 0.05 Hz were used to determine the horizontal component of the polarization vector, i.e., the best direction of tilt, for each neuron. Two types of stimuli were used; rotation of a fixed angle of tilt around the head or body ("wobble," Ref. 22) or sinusoidal stimuli in several planes. Polarization vectors of the responses to neck stimulation were widely distributed; different neurons responded best to roll, pitch, and angles in between. For every neuron, the amplitude of the response decreased as the cosine of the angle between the direction of maximal sensitivity and the plane of the stimulus. The direction of the vector remained stable as the frequency of stimulation was varied. Neurons with different vectors had similar dynamics that resembled those of cervical interneurons (27). Many neurons responded to both neck and vestibular stimulation, although the vestibular response usually had a much lower gain. Neck and vestibular vectors were approximately opposite in direction. We suggest that neck responses originate in receptors, probably spindles, in perivertebral muscles. Each of these muscles presumably is best stretched by a particular direction of pull. It seems likely that convergence from receptors in selected muscles determines the direction of a spinal neuron's vector. Vestibular responses probably are due mainly to activity in otolith afferents.


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)


1988 ◽  
Vol 60 (5) ◽  
pp. 1765-1778 ◽  
Author(s):  
J. Kasper ◽  
R. H. Schor ◽  
V. J. Wilson

1. We have studied the responses of neurons in the lateral and descending vestibular nuclei of decerebrate cats to stimulation of neck receptors, produced by rotating the body in vertical planes with the head stationary. The responses to such neck stimulation were compared with the responses to vestibular stimulation produced by whole-body tilt, described in the preceding paper. 2. After determining the optimal vertical plane of neck rotation (response vector orientation), the dynamics of the neck response were studied over a frequency range of 0.02-1 Hz. The majority of the neurons were excited by neck rotations that brought the chin toward the ipsilateral side; most neurons responded better to roll than to pitch rotations. The typical neck response showed a low-frequency phase lead of 30 degrees, increasing to 60 degrees at higher frequencies, and a gain that increased about threefold per decade. 3. Neck input was found in about one-half of the vestibular-responsive neurons tested with vertical rotations. The presence of a neck response was correlated with the predominant vestibular input to these neurons; neck input was most prevalent on neurons with vestibular vector orientations near roll and receiving convergent vestibular input, either input from both ipsilateral vertical semicircular canals, or from canals plus the otolith organs. 4. Neurons with both vestibular and neck responses tend to have the respective orientation vectors pointing in opposite directions, i.e., a head tilt that produces an excitatory vestibular response would produce an inhibitory neck response. In addition, the gain components of these responses were similar. These results suggest that during head movements on a stationary body, these opposing neck and vestibular inputs will cancel each other. 5. Cancellation was observed in 12 out of 27 neurons tested with head rotation in the mid-frequency range. For most of the remaining neurons, the response to such a combined stimulus was greatly attenuated: the vestibular and neck interaction was largely antagonistic. 6. Neck response dynamics were similar to those of the vestibular input in many neurons, permitting cancellation to take place over a wide range of stimulus frequencies. Another pattern of interaction, observed in some neurons with canal input, produced responses to head rotation that had a relatively constant gain and remained in phase with position over the entire frequency range; such neurons possibly code head position in space.


1994 ◽  
Vol 71 (1) ◽  
pp. 11-16 ◽  
Author(s):  
K. Endo ◽  
J. Kasper ◽  
V. J. Wilson ◽  
B. J. Yates

1. To study their contribution to the vestibulocollic reflex, we have studied, in decerebrate paralyzed cats, the effect of sinusoidal vestibular stimulation in multiple vertical planes on the spontaneous activity of neurons in the C3 ventral horn. Antidromic microstimulation was used to identify 17/42 neurons as commissural; 10 of these were confirmed to have a projection to the contralateral ventral horn. 2. Dynamics of the responses of spontaneously firing neurons were studied with 0.05–1 Hz sinusoidal stimuli delivered near the plane of rotation that produced maximal modulation of neuron activity (response vector orientation). On the basis of their responses, we classified 38 neurons as receiving otolith, semicircular canal, or otolith + canal input. All three response types were found among commissure and nonantidromic neurons. 3. Two-thirds of neuron response vector orientations pointed contralaterally. They were either near the anterior or posterior canal planes or in the roll quadrant. In the case of neurons with input from canals, the latter indicates convergence from the vertical canals on the same side. There were almost no vectors in the pitch quadrants. The distribution of response vector orientations resembles that seen in the vestibular nuclei and pontomedullary reticular formation, suggesting that commissural neurons may not make a new contribution to spatial processing in the vertical vestibulocollic reflex. 4. It is presumed that commissural neurons are premotor. If so, some have the properties to be in the pathway between the contralateral utricle and neck motoneurons. More generally, their actions could modify the effectiveness of vestibulospinal and reticulospinal fibers that have similar spatial properties and make synapses with neck motoneurons.


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