Responses of rostral fastigial nucleus neurons of conscious cats to rotations in vertical planes.

The rostral fastigial nucleus (RFN) of the cerebellum is thought to play an important role in postural control, and recent studies in conscious nonhuman primates suggest that this region also participates in the sensory processing required to compute body motion in space. The goal of the present study was to examine the dynamic and spatial responses to sinusoidal rotations in vertical planes of RFN neurons in conscious cats, and determine if they are similar to responses reported for monkeys. Approximately half of the RFN neurons examined were classified as graviceptive, since their firing was synchronized with stimulus position and the gain of their responses was relatively unaffected by the frequency of the tilts. The large majority (80%) of graviceptive RFN neurons were activated by pitch rotations. Most of the remaining RFN units exhibited responses to vertical oscillations that encoded stimulus velocity, and approximately 50% of these velocity units had a response vector orientation aligned near the plane of a single vertical semicircular canal. Unlike in primates, few feline RFN neurons had responses to vertical rotations that suggested integration of graviceptive (otolith) and velocity (vertical semicircular canal) signals. These data indicate that the physiological role of the RFN may differ between primates and lower mammals. The RFN in rats and cats in known to be involved in adjusting blood pressure and breathing during postural alterations in the transverse (pitch) plane. The relatively simple responses of many RFN neurons in cats are appropriate for triggering such compensatory autonomic responses.

Responses of caudal vestibular nucleus neurons of conscious cats to rotations in vertical planes, before and after a bilateral vestibular neurectomy.

Although many previous experiments have considered the responses of vestibular nucleus neurons to rotations and translations of the head, little data are available regarding cells in the caudalmost portions of the vestibular nuclei (CVN), which mediate vestibulo-autonomic responses among other functions. This study examined the responses of CVN neurons of conscious cats to rotations in vertical planes, both before and after a bilateral vestibular neurectomy. None of the units included in the data sample had eye movement-related activity. In labyrinth-intact animals, some CVN neurons (22%) exhibited graviceptive responses consistent with inputs from otolith organs, but most (55%) had dynamic responses with phases synchronized with stimulus velocity. Furthermore, the large majority of CVN neurons had response vector orientations that were aligned either near the roll or vertical canal planes, and only 18% of cells were preferentially activated by pitch rotations. Sustained head-up rotations of the body provide challenges to the cardiovascular system and breathing, and thus the response dynamics of the large majority of CVN neurons were dissimilar to those of posturally-related autonomic reflexes. These data suggest that vestibular influences on autonomic control mediated by the CVN are more complex than previously envisioned, and likely involve considerable processing and integration of signals by brainstem regions involved in cardiovascular and respiratory regulation. Following a bilateral vestibular neurectomy, CVN neurons regained spontaneous activity within 24 h, and a very few neurons (<10%) responded to vertical tilts <15 degrees in amplitude. These findings indicate that nonlabyrinthine inputs are likely important in sustaining the activity of CVN neurons; thus, these inputs may play a role in functional recovery following peripheral vestibular lesions.

Semicircular canal-otolith organ interaction during off-vertical axis rotation in humans.

The aim of this study was to examine the interaction of signals from the semicircular canals and the otolith organs during off-vertical axis rotation (OVAR). We recorded horizontal eye position using electro-oculography in 22 young normal human subjects and stimulated the vestibulo-ocular reflex with both constant velocity trapezoids and sinusoidal yaw rotations, using both earth-vertical axis rotation (EVAR) and OVAR. We found that per-rotatory long vestibulo-ocular reflex (VOR) time constants during velocity trapezoids were shorter for OVAR than for EVAR, suggesting a reduction in the efficacy of the velocity storage system during OVAR. However, when we tested with very-low-frequency sinusoids (0.01 Hz and below), the phase lead of the VOR re head velocity was smaller during OVAR than EVAR, suggesting a longer time constant and enhanced efficacy of velocity storage during OVAR. These rotational responses can be explained by two competing influences of signals from the otolith organs, one that diminishes the effectiveness of velocity storage and another that contributes to an estimate of head velocity.

Localization of proprioceptive reflexes in the splenius muscle of the cat.

Activity of the cat splenius muscle was modulated by sinusoidal rotation of the head around the C1-C2 joint in decerebrate cats with labyrinth intact or with all semicircular canals plugged, or, in one intact and alert cat, by rotation of the body with the head fixed in space. EMG modulation, recorded from the areas of splenius innervated by the C1-C4 nerves, was due to the cervicocollic reflex. Modulation was not uniform, but decreased with progressively more caudal recording locations; with stimuli of small amplitude it was often possible to obtain modulation of the rostral part of the muscle only. The results demonstrate localization of proprioceptive reflexes, including the stretch reflex, within the splenius muscle.

Off-vertical axis rotation: a test of the otolith-ocular reflex.

The vestibulo-ocular reflex was studied via off-vertical axis rotation (OVAR) in the dark. The axis of the turntable could be tilted from vertical by up to 30 degrees. Eye movements were measured with electro-oculography. Results from healthy asymptomatic subjects indicated that 1) a reliable otolith-induced response could be obtained during constant velocity OVAR using a velocity of 60 degrees/s with a tilt of 30 degrees; 2) constant velocity OVAR rotation was nausea-producing and, especially if subjects were rotated in the dark about an earth-vertical axis prior to being tilted, disorienting; and 3) sinusoidal OVAR produced minimal nausea; the eye movement response appeared to be the result of a combination of semicircular canal and otolith components. We conclude that OVAR has the potential of becoming a useful method for clinically assessing both the otolith-ocular reflex and semicircular canal-otolith interaction.

Off-vertical axis rotational responses in patients with unilateral peripheral vestibular lesions.

Off-vertical axis rotation (OVAR) stimulates the otolith organs in a manner that is suitable for assessment of the otolith-ocular reflex. To further assess the potential clinical usefulness of OVAR, the eye movement responses of seven patients with surgically confirmed unilateral peripheral vestibular lesions were compared with the eye movement responses of a group of age-matched, healthy, asymptomatic control subjects. Patients and controls were tested with constant velocity rotations that followed a brief period of angular acceleration (velocity trapezoid) using either earth-vertical axis (EVA) rotation or OVAR. Both EVA and OVAR sinusoidal velocity profiles were also performed. Results indicated that each patient had 1) an asymmetric OVAR response, ie, a bias component whose direction was opposite normal when rotating toward the lesioned ear, and 2) a normal modulation component. Population data suggested that patients had 1) a more rapid decay of response than normal subjects during OVAR velocity trapezoids, 2) an increased phase lead as compared to normal subjects during sinusoidal OVAR, and 3) like normal subjects, a less rapid decay of response during OVAR velocity trapezoids than during EVA rotational velocity trapezoids. Taken together, these findings suggest that patients with unilateral peripheral vestibular deficits have abnormal otolith-ocular and semicircular canal-ocular reflexes but that a single labyrinth appears to provide an otolithic signal sufficient for qualitatively normal semicircular canal-otolith interaction.

Horizontal rotation responses of medullary reticular neurons in the decerebrate cat.

This study examines the response of neurons in the medullary reticular formation of the decerebrate cat to sinusoidal yaw rotations in the plane of the horizontal semicircular canals. Responsive neurons that could be antidromically activated from the spinal cord appeared to be less sensitive to the rotary stimulus than the rest of the population or responsive neurons. Most neurons had response dynamics similar to those of semicircular canal afferents.

Influence of otolith organs, semicircular canals, and neck afferents on post-rotatory nystagmus.

The duration of post-rotatory nystagmus is known to be shortened by head tilt, a phenomenon that has been attributed to rapid discharge of the velocity storage mechanism. The relative importance of the various sensory signals associated with post-rotatory head tilt is unknown. Using both earth-vertical axis and off-vertical axis rotation, we investigated this issue in humans by combining sudden termination of constant velocity rotation with several post-rotatory maneuvers that stimulated combinations of otolith organ, somatosensory, and vertical semicircular canal afferents. Results indicated that horizontal post-rotatory nystagmus was shortened by maneuvers that move the head from upright to off-vertical and by cessation of dynamic otolith stimuli. Somatosensory, neck afferent, and transient vestibular stimulation had no consistent effect. We conclude that tilt suppression of postrotatory nystagmus and the short time constant following off-vertical axis rotation is primarily a function of otolith influence on the velocity storage system.

Characteristics of secondary phase post-rotatory nystagmus following off-vertical axis rotation in humans.

The nystagmus following yaw earth-vertical axis rotation often reverses direction, a phenomenon known as the "secondary phase". The purpose of this study was to examine the existence and the spatial and temporal properties of the secondary phase of post-rotatory nystagmus following off-vertical axis rotation (OVAR). Eleven normal human subjects were rotated at 120 or 180 degrees/s about an off-vertical axis and stopped in the left ear down or right ear down lateral position. Horizontal and vertical eye positions were recorded with a scleral search coil, and horizontal and vertical slow component eye velocities were computed. Our results indicate that (a) there is a robust secondary phase nystagmus following OVAR, and (b) the direction of the secondary phase nystagmus tends to align with earth-horizontal. These results can be explained by a minor modification of an existing VOR model that has been shown to produce secondary phase responses.

Horizontal linear and angular responses of neurons in the medial vestibular nucleus of the decerebrate cat.

Responses to linear accelerations in the earth-horizontal plane (typically provoked by tilts of the head or body) are characterized by a stimulus direction that produces the maximal excitation. Although changes in cardiovascular, sympathetic, and respiratory outflow are maximized during pitch, no collection of central vestibular neurons had been identified where pitch responses predominate. In the present study, response properties of neurons in the medial vestibular nucleus were examined in decerebrate cats placed on a turntable. Activation of otolith afferents was provided by constant velocity rotation with the turntable axis tilted 5 degrees from the vertical. Responsive neurons exhibited a sinusoidal modulation in their firing rate; the optimal excitatory stimulus direction was derived from responses to clockwise and counterclockwise rotations. Many of these neurons were also tested for input from horizontal semicircular canals using 0.5 Hz sinusoidal rotation about an earth-vertical axis. Of 22 tilt-sensitive neurons in the medial vestibular nucleus whose optimal stimulus direction was determined, 9 were best stimulated by pitch, 10 by stimuli in one of the two vertical semicircular canal planes, and 3 by roll. Of the 33 neurons in this nucleus tested for possible convergent inputs from the otolith organs and the horizontal semicircular canals, 8 responded to both the constant velocity (otolith) stimulus and to the sinusoidal rotation, 7 appeared to receive otolith, but not horizontal canal, input, while 18 had a canal, but no otolith, response. Thus, besides serving as a relay for horizontal canal signals, the medial vestibular nucleus may also be an important relay for information about orientation within the sagittal (pitch) plane.

Design and fitting of neural network transfer functions.

An algorithm is presented which (a) allows construction of mathematical models involving arbitrary combinations of linear cascades, parallel pathways, and feedback loops, (b) computes a total transfer function of the system, (c) performs a least-squares optimization of model parameters to best fit the model to experimental data, and (d) provides a measure of goodness-of-fit to the data. The technique has been employed to construct and test models of neural networks which mimic a class of responses observed in the cat vestibular nuclei in response to tilt, namely responses which show both a gain increase and progressive phase lag as the stimulation frequency goes from 0.01 to 2 Hz. A network consisting of a simple gain element in parallel with an inhibitory high-pass filtered version of the input provided a satisfactory fit to these data.

Relationship of cat vestibular neurons to otolith-spinal reflexes.

The dynamics of neurons in the vestibular nuclei of canal-plugged, decerebrate cats were studied in response to lateral (roll) tilt. Forelimb and neck extensor reflexes recorded simultaneously develop a progressive phase lag above 0.1 Hz. Neurons which exhibited a muscle-like phase lag were excited during low frequency stimuli by ipsilateral side-up tilt (beta response). Neurons with alpha responses, excited during side-down tilt, exhibited a constant phase, without a high frequency lag. Vestibulospinal neurons were present in both of these response groups, as were units driven at monosynaptic latencies by electrical stimulation of the ipsilateral labyrinth. The phase-lagging beta responses are appropriate for contributing to the reflexes observed in the ipsilateral neck and contralateral forelimb.

The "practical mathematics" of recording three-dimensional eye position using scleral coils.

The "gold standard" for recording the three-dimensional rotation of the eye involves placing two coils of wire, embedded in a soft plastic ring, on the sclera of the eye, then placing the subject inside a set of orthogonal oscillating magnetic fields, and using the currents induced in the eye coils to deduce the position of the coil, and hence of the eye, in space. Eye movements are actually eye rotations, which can be described mathematically by a special class of matrices, rotation matrices, or, alternatively, by a rotation vector related to the axis of the rotation. This article deals with the mathematical tools needed to implement the signal processing from such a multifield, dual-coil system and compute the precise rotational movement of the eye. One reason for making such careful measurements is to study an interesting constraint on eye movements, called Listing's law, which expresses ocular torsion, or rotation of the eye about its line of sight, in terms of the direction of gaze. Techniques for experimentally quantitating these constraints are also presented. Following a treatment of the "ideal" case, with coils and eye in perfect alignment, the additional techniques for dealing with various departures from ideality that are almost always encountered experimentally are examined. A final section deals with developing a validation protocol for eye movement analysis techniques using mechanical and computer simulations of eye movements.

The neural substrate of the vestibulocollic reflex. What needs to be learned.

The purpose of this review is to assess the role of short-latency pathways in the vestibulocollic reflex (VCR). First the current knowledge about the disynaptic and trisynaptic pathways linking semicircular canal and otolith afferents with cat neck motoneurons is summarized. We then discuss whether these pathways are sufficient or necessary to produce the responses observed in neck muscles by natural vestibular stimulation and conclude that they are neither. Finally, alternate pathways are considered, most likely involving reticulospinal fibers, which are an important part of the neural substrate of the VCR.

Response of vestibular neurons to head rotations in vertical planes. I. Response to vestibular stimulation.

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.