Constant Velocity Off-vertical Axis Rotation Research Articles

Ocular Reflex Phase during Off-Vertical Axis Rotation in Humans is Modified by Head-Turn-On-Trunk Position

Constant velocity Off-Vertical Axis Rotation (OVAR) imposes a continuously varying orientation of the head and body relative to gravity, which generates a modulation of horizontal (conjugate and vergence), vertical, and torsional eye movements. We introduced the head-turn-on-trunk paradigm during OVAR to examine the extent to whether the modulation of these ocular reflexes is mediated by graviceptors in the head, i.e., otoliths, versus other body graviceptors. Ten human subjects were rotated in darkness about their longitudinal axis 20° off-vertical at a constant velocity of 45 and 180°/s, corresponding to 0.125 and 0.5 Hz. Binocular responses were obtained with the head and trunk aligned, and then with the head turned relative to the trunk 40° to the right or left of center. The modulation of vertical and torsional eye position was greater at 0.125 Hz while the modulation of horizontal and vergence slow phase velocity was greater at 0.5 Hz. The amplitude modulation was not significantly altered by head-on-trunk position, but the phases shifted towards alignment with the head. These results are consistent with the modulation of ocular reflexes during OVAR being primarily mediated by the otoliths in response to the sinusoidally varying linear acceleration along the interaural and naso-occipital head axis.

Translational otolith-ocular reflex during off-vertical axis rotation in humans

Two characteristics of otolith-ocular responses – linear vestibulo-ocular reflex and vergence – were examined during constant velocity off-vertical axis rotation (OVAR) in the dark. Sixteen subjects were rotated about their longitudinal axis when tilted 30° relative to the direction of gravity. Rotational velocities were 36 and 288/s corresponding to frequencies of 0.1 and 0.8Hz, respectively. Subjects were asked to imagine stationary targets located at 0.5m, 1m, and 2m in the straight-ahead direction. Binocular eye movements were recorded in the dark using infrared videography. The modulation of horizontal slow phase velocity during OVAR was larger at 0.8Hz than at 0.1Hz, and the modulation at the high frequency was larger for the near target than for the mid and far targets. These characteristics confirm that the horizontal slow phase velocity during yaw OVAR represents a translational otolith-ocular reflex in response to acceleration along the inter-aural axis that is dependent on imagined fixation distance.

Neural Representation of Orientation Relative to Gravity in the Macaque Cerebellum

A fundamental challenge for maintaining spatial orientation and interacting with the world is knowledge of our orientation relative to gravity, i.e., head tilt. Sensing gravity is complicated because of Einstein's equivalence principle, in which gravitational and translational accelerations are physically indistinguishable. Theory has proposed that this ambiguity is solved by tracking head tilt through multisensory integration. Here we identify a group of Purkinje cells in the caudal cerebellar vermis with responses that reflect an estimate of head tilt. These tilt-selective cells are complementary to translation-selective Purkinje cells, such that their population activities sum to the net gravitoinertial acceleration encoded by the otolith organs, as predicted by theory. These findings reflect the remarkable ability of the cerebellum for neural computation and provide quantitative evidence for a neural representation of gravity, whose calculation relies on long-postulated theoretical concepts such as internal models and Bayesian priors.

Eye movements and motion perception during off-vertical axis rotation after spaceflight1

Constant velocity off-vertical axis rotation (OVAR) provides dynamic linear acceleration stimuli that can be used to assess otolith function. Eight astronauts were rotated in darkness about their longitudinal axis 20° off vertical at low (0.125 Hz) and high (0.5 Hz) frequencies and their responses were compared before and after spaceflight. Eye movements were recorded using infrared videography and perceived motion was evaluated using a joystick with four degrees of freedom - pitch and roll tilt, front-back and lateral translation. Low-frequency OVAR generates tilt otolith-induced responses - modulation of ocular counter-roll and counter-pitch with perceived conical motion path - whereas high-frequency OVAR generates translational otolith-induced responses - modulation of horizontal and vergence slow phase velocity with perceived cylindrical motion path. While there were transient changes in the amplitude of the translational ocular responses on landing day, there were no major changes in the tilt ocular reflexes after adaptation to weightlessness. However, there was an increase in sensitivity to motion perception after spaceflight. Direct comparisons of pre- and postflight stimuli suggested that OVAR on landing day was less provocative of motion sickness than before spaceflight. These results confirm that some otolith reflexes elicited during passive motion may not be altered by short-duration spaceflight - or may readapt very quickly - and that the resolution of sensory conflict associated with postflight recovery involves higher-order neural processes.

Parabrachial nucleus neuronal responses to off-vertical axis rotation in macaques

The caudal aspect of the parabrachial nucleus (PBN) contains neurons responsive to whole body, periodic rotational stimulation in alert monkeys (Balaban et al. in J Neurophysiol 88:3175-3193, 2002). This study characterizes the angular and linear motion-sensitive response properties of PBN unit responses during off-vertical axis rotation (OVAR) and position trapezoid stimulation. The OVAR responses displayed a constant firing component which varied from the firing rate at rest. Nearly two-thirds of the units also modulated their discharges with respect to head orientation (re: gravity) during constant velocity OVAR stimulation. The modulated response magnitudes were equal during ipsilateral and contralateral OVARs, indicative of a one-dimensional accelerometer. These response orientations during OVAR divided the units into three spatially tuned populations, with peak modulation responses centered in the ipsilateral ear down, contralateral anterior semicircular canal down, and occiput down orientations. Because the orientation of the OVAR modulation response was opposite in polarity to the orientation of the static tilt component of responses to position trapezoids for the majority of units, the linear acceleration responses were divided into colinear dynamic linear and static tilt components. The orientations of these unit responses formed two distinct population response axes: (1) units with an interaural linear response axis and (2) units with an ipsilateral anterior semicircular canal-contralateral posterior semicircular canal plane linear response axis. The angular rotation sensitivity of these units is in a head-vertical plane that either contains the linear acceleration response axis or is perpendicular to the linear acceleration axis. Hence, these units behave like head-based ('strapdown') inertial guidance sensors. Because the PBN contributes to sensory and interoceptive processing, it is suggested that vestibulo-recipient caudal PBN units may detect potentially dangerous anomalies in control of postural stability during locomotion. In particular, these signals may contribute to the range of affective and emotional responses that include panic associated with falling, malaise associated with motion sickness and mal-de-debarquement, and comorbid balance and anxiety disorders.

Developmental expression of NMDA and AMPA receptor subunits in vestibular nuclear neurons that encode gravity‐related horizontal orientations

We examined the expression profile of subunits of ionotropic glutamate receptors [N-methyl-D-aspartate (NMDA) and alpha-amino-3-hydroxy-5-methyl-4-isoxazole-proprionate (AMPA)] during postnatal development of connectivity in the rat vestibular nucleus. Vestibular nuclear neurons were functionally activated by constant velocity off-vertical axis rotation, a strategy to stimulate otolith organs in the inner ear. These neurons indicated Fos expression as a result. By immunodetection for Fos, otolith-related neurons that expressed NMDA/AMPA receptor subunits were identified as early as P7, and these neurons were found to increase progressively up to adulthood. Although there was developmental invariance in the percentage of Fos-immunoreactive neurons expressing the NR1, NR2A, GluR1, or GluR2/3 subunits, those expressing the NR2B subunit decreased from P14 onward, and those expressing the GluR4 subunit decreased in adults. These double-immunohistochemical data were corroborated by combined immuno-/hybridization histochemical data obtained from Fos-immunoreactive neurons expressing NR2B mRNA or GluR4 mRNA. The staining of both NR2B and GluR4 in the cytoplasm of these neurons decreased upon maturation. The percentage of Fos-immunoreactive neurons expressing the other ionotropic glutamate receptor subunits (viz. NR1, NR2A, GluR1, and GluR2/3) remained relatively constant throughout postnatal maturation. Triple immunofluorescence further demonstrated coexpression of NR1 and NR2 subunits in Fos-immunoreactive neurons. Coexpression of NR1 subunit with each of the GluR subunits was also observed among the Fos-immunoreactive neurons. Taken together, the different expression profiles of ionotropic glutamate receptor subunits constitute the histological basis for glutamatergic neurotransmission in the maturation of central vestibular connectivity for the coding of gravity-related horizontal head movements.

Otolith-ocular responses in Meniere's patients before and after endolymphatic shunt operation

Caloric testing in prone/supine position and constant velocity off-vertical axis rotation (OVAR) in yaw axis (rotate-then-tilt paradigm) can evaluate labyrinth function and vestibular-ocular reflex (VOR) behaviour before and after endolymphatic shunt surgery (ESS). Preoperative and postoperative otolith dysfunction can be documented by constant velocity OVAR, before the VOR is modulated by the vestibular compensation. Vestibulo-ocular responses in prone/supine position and linear VOR (lVOR) OVAR responses were observed in 10 patients before and after ESS. Ipsilateral caloric reaction in prone/supine position was reduced after ESS. Otolith-ocular function and canal-otolith-interaction were improved postoperatively. Meniere's patients with bias component opposite to normal when rotating towards the lesioned ear showed relief of symptoms postoperatively. The bias component returning to normal can help to identify the relief of Meniere's attacks after ESS. The canal-otolith interaction can be observed pre- and postoperatively by means of caloric reaction in prone/supine position as part of the clinical routine.

Tilt and translation motion perception during off-vertical axis rotation

The effect of stimulus frequency on tilt and translation motion perception was studied during constant velocity off-vertical axis rotation (OVAR), and compared to the effect of stimulus frequency on eye movements. Fourteen healthy subjects were rotated in darkness about their longitudinal axis 10 degrees and 20 degrees off-vertical at 45 degrees /s (0.125 Hz) and 20 degrees off-vertical at 180 degrees /s (0.5 Hz). Perceived motion was evaluated using verbal reports and a joystick capable of recording tilt and translation in both sagittal and lateral planes. Eye movements were also recorded using videography. At the lower frequency, subjects reported the perception of progressing along the edge of a cone, whereas at the higher frequency they had the sensation of progressing along the edge of an upright cylinder. Tilt perception and ocular torsion significantly increased as the tilt angle increased from 10 degrees to 20 degrees at the lower frequency, and then decreased at the higher frequency. The phase lag of ocular torsion increased as a function of frequency, while the phase lag of tilt perception did not change. Horizontal eye movements were small at the lower frequency and showed a phase lead relative to the linear acceleration stimulus. While the phase lead of horizontal eye movements decreased at 0.5 Hz, the phase of translation perception did not vary with stimulus frequency and was similar to the phase of tilt perception during all conditions. A second data set was obtained in 12 subjects to compare motion perception phase when using a simple push-button to indicate nose-up orientation, continuous setting of pitch tilt alone, or continuous setting of tilt and translation in both pitch and roll planes as in the first data set. This set of measurements indicated that in the frequency range studied subjects tend to lead the stimulus when using a push-button task while lagging the stimulus when using a continuous setting of tilt with a joystick. Both amplitude and phase of tilt perception using the joystick were not different whether concentrating on pitch tilt alone or attempting a more complex reporting of tilt and translation in both sagittal and lateral planes. During dynamic linear stimuli in the absence of canal and visual input, a change in stimulus frequency alone elicits similar changes in the amplitude of both self-motion perception and eye movements. However, in contrast to the eye movements, the phase of both perceived tilt and translation motion is not altered by stimulus frequency over this limited range. These results are consistent with the hypothesis that neural processing to distinguish tilt and translation stimuli differs between eye movements and motion perception.

Evaluation of the otolith function using sinusoidal off-vertical axis rotation in patients with benign paroxysmal positional vertigo

The vestibulo-ocular reflex (VOR) was studied via sinusoidal off-vertical axis rotation (OVAR) to evaluate the otolith function in patients with benign paroxysmal positional vertigo (BPPV). Subjects were sinusoidally rotated with eyes open in complete darkness at frequencies of 0.4 and 0.8 Hz with a maximum angular velocity of 60 degrees s(-1) in earth-vertical axis rotation (EVAR) and OVAR. Twenty-three controls and 24 BPPV patients were investigated. Results showed that VOR gain during OVAR at 0.8 Hz in a 30 degrees nose-up position in BPPV patients was significantly less than the gain during EVAR, whereas the gain was not significantly different between EVAR and OVAR in the controls in each condition. In addition, to examine each type of BPPV, we also investigated whether there were any differences between the patients who suffered from dizziness and those who did not. VOR gain in OVAR of BPPV patients who were suffering from dizziness was significantly less than that of BPPV patients without dizziness. Not only cupulolithiasis or canalolithiasis, but also otolith dysfunction was considered to be the possible origin of BPPV. Because sinusoidal OVAR produced minimal nausea compared to constant velocity OVAR, the stimulation of 0.8 Hz nose-up in sinusoidal OVAR may be used to evaluate otolith function without discomfort for patients.

Vestibulo-ocular function in anxiety disorders

Previous studies of vestibulo-ocular function in patients with anxiety disorders have suggested a higher prevalence of peripheral vestibular dysfunction compared to control populations, especially in panic disorder with agoraphobia. Also, our recent companion studies have indicated abnormalities in postural control in patients with anxiety disorders who report a high degree of space and motion discomfort. The aim of the present study was to assess the VOR, including the semicircular canal-ocular reflex, the otolith-ocular reflex, and semicircular canal-otolith interaction, in a well-defined group of patients with anxiety disorders. The study included 72 patients with anxiety disorders (age 30.6 +/- 10.6 yrs; 60 (83.3% F) and 29 psychiatrically normal controls (age 35.0 +/minus; 11.6 yrs; 24 (82.8% F). 25 patients had panic disorder; 47 patients had non-panic anxiety. Patients were further categorized based on the presence (45 of 72) or absence (27 of 72) of height phobia and the presence (27 of 72) or absence (45 of 72) of excessive space and motion discomfort (SMD). Sinusoidal and constant velocity earth-vertical axis rotation (EVAR) was used to assess the semicircular canal-ocular reflex. Constant velocity off-vertical axis rotation (OVAR) was used to assess both the otolith-ocular reflex and static semicircular canal-otolith interaction. Sinusoidal OVAR was used to assess dynamic semicircular canal-otolith interaction. The eye movement response to rotation was measured using bitemporal electro-oculography. Results showed a significantly higher VOR gain and a significantly shorter VOR time constant in anxiety patients. The effect of anxiety on VOR gain was significantly greater in patients without SMD as compared to those with SMD. Anxiety patients without height phobia had a larger OVAR modulation. We postulate that in patients with anxiety, there is increased vestibular sensitivity and impaired velocity storage. Excessive SMD and height phobia seem to have a mitigating effect on abnormal vestibular sensitivity, possibly via a down-weighting of central vestibular pathways.

Response properties of Y group neurons to crossed otolith inputs in the cat.

The response properties of extracellularly recorded Y group neurons on the lesioned side were examined in decerebrate cats after acute hemilabyrinthectomy, with the use of constant velocity off-vertical axis rotations (OVAR) to stimulate the remaining intact otolith receptors. During rotation in the clockwise or counterclockwise direction, Y group neurons displayed a spectrum of position-dependent bidirectional response sensitivities, ranging from one- to two-dimensional. Some two-dimensional neurons even exhibited unidirectional responses with change in OVAR velocity. These findings indicate that Y group neurons have the capacity to code spatiotemporal signals arising from the contralateral otolith. The best response orientations of one-dimensional and two-dimensional neurons were found predominantly along the antero-posterior direction, thus providing a spatial framework for the otolithic reflexes.

Human otolith–ocular reflexes during off-vertical axis rotation: effect of frequency on tilt–translation ambiguity and motion sickness

The purpose of this study was to examine how the modulation of tilt and translation otolith–ocular responses during constant velocity off-vertical axis rotation varies as a function of stimulus frequency. Eighteen human subjects were rotated in darkness about their longitudinal axis 30° off-vertical at stimulus frequencies between 0.05 and 0.8 Hz. The modulation of torsion decreased while the modulation of horizontal slow phase velocity (SPV) increased with increasing frequency. It is inferred that the ambiguity of otolith afferent information is greatest in the frequency region where tilt (torsion) and translational (horizontal SPV) otolith–ocular responses crossover. It is postulated that the previously demonstrated peak in motion sickness susceptibility during linear accelerations around 0.3 Hz is the result of frequency segregation of ambiguous otolith information being inadequate to distinguish between tilt and translation.

Spontaneous discharge and response characteristics of central otolith neurons of rats during postnatal development.

To study the developmental profile of otolith-related vestibular nuclear neurons, their spontaneous activities and response dynamics were examined in decerebrate rats aged seven, 14, 21 and 84 (adult) days. Extracellular recordings were performed in the lateral and descending vestibular nucleus of animals held at the stationary position in the earth-horizontal or subjected to constant velocity off-vertical axis rotation, which selectively stimulates the otolith receptors. All neurons displayed sinusoidal position-dependent modulation in discharge rate, indicating their capability in coding spatial information during low-frequency head movement. Some neurons showed a full-cycle response to off-vertical axis rotation (non-clipped), while other neurons were silenced in discharge during parts of each rotary cycle (clipped). In seven-day-old rats, three-quarters of the responsive neurons sampled were clipped and the proportion progressively decreased to less than one-quarter in adult rats. In each age group, the clipped neurons discharged in approximately 60% of the stimulus cycle. Response gains of the neurons increased with age, reaching a plateau from 21 days of age for clipped neurons and 14 days for non-clipped neurons. The clipped neurons demonstrated higher response gains than the non-clipped neurons at or beyond 21 days of age. Spontaneous activities of the neurons at the stationary and earth-horizontal positions were analysed in relation to their response gains; a positive correlation was observed from 14 days of age onwards. Both types of neurons showed progressive increase in spontaneous activity as the rats matured, though the clipped neurons exhibited significantly lower resting rates than the non-clipped neurons at each of the age groups studied. Some neurons that responded to off-vertical axis rotation were not spontaneously active at the stationary position, but the proportion of these decreased significantly with age. The coefficient of variation of each age group showed a bimodal distribution, thereby allowing spontaneously active neurons to be assigned as regular or irregular. Though the vast majority of both the clipped and non-clipped neurons showed irregular discharge patterns at seven days of age, the overall population became more regular as the rats matured. Irregular neurons of young rats exhibited phase-stable and phase-shift responses, while those of older rats showed only the phase-stable response. This distinction was not observed amongst regular neurons over the ages studied. Our results reveal features of central otolith neurons that can be taken as signs of maturation during the first three postnatal weeks. These neuronal features provide the framework for the analysis of behaviours mediated by the otolith system during postnatal maturation.

Low-frequency otolith and semicircular canal interactions after canal inactivation.

During sustained constant velocity and low-frequency off-vertical axis rotations (OVAR), otolith signals contribute significantly to slow-phase eye velocity. The adaptive plasticity of these responses was investigated here after semicircular canal plugging. Inactivation of semicircular canals results in a highly compromised and deficient vestibulo-ocular reflex (VOR). Based on the VOR enhancement hypothesis, one could expect an adaptive increase of otolith-borne angular velocity signals due to combined otolith/canal inputs after inactivation of the semicircular canals. Contrary to expectations, however, the steady-state slow-phase velocity during constant velocity OVAR decreased in amplitude over time. A similar progressive decrease in VOR gain was also observed during low-frequency off-vertical axis oscillations. This response deterioration was present in animals with either lateral or vertical semicircular canals inactivated and was limited to the plane(s) of the plugged canals. The results are consistent with the idea that the low-frequency otolith signals do not simply enhance VOR responses. Rather, the nervous system appears to correlate vestibular sensory information from the otoliths and the semicircular canals to generate an integral response to head motion.

Neuronal response sensitivity to bidirectional off-vertical axis rotations: a dimension of imbalance in the bilateral vestibular nuclei of cats after unilateral labyrinthectomy

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, δ, 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 δ values (i.e. between 0/∞ and finite values) with velocity can be computed for each neuron. The shifts in δ 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-side-down/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.

Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys. III. Responses To translation.

The three-dimensional (3-D) properties of the translational vestibulo-ocular reflexes (translational VORs) during lateral and fore-aft oscillations in complete darkness were studied in rhesus monkeys at frequencies between 0.16 and 25 Hz. In addition, constant velocity off-vertical axis rotations extended the frequency range to 0.02 Hz. During lateral motion, horizontal responses were in phase with linear velocity in the frequency range of 2-10 Hz. At both lower and higher frequencies, phase lags were introduced. Torsional response phase changed more than 180 degrees in the tested frequency range such that torsional eye movements, which could be regarded as compensatory to "an apparent roll tilt" at the lowest frequencies, became anticompensatory at all frequencies above approximately 1 Hz. These results suggest two functionally different frequency bandwidths for the translational VORs. In the low-frequency spectrum (<<0.5 Hz), horizontal responses compensatory to translation are small and high-pass-filtered whereas torsional response sensitivity is relatively frequency independent. At higher frequencies however, both horizontal and torsional response sensitivity and phase exhibit a similar frequency dependence, suggesting a common role during head translation. During up-down motion, vertical responses were in phase with translational velocity at 3-5 Hz but phase leads progressively increased for lower frequencies (>90 degrees at frequencies <0.2 Hz). No consistent dependence on static head orientation was observed for the vertical response components during up-down motion and the horizontal and torsional response components during lateral translation. The frequency response characteristics of the translational VORs were fitted by "periphery/brain stem" functions that related the linear acceleration input, transduced by primary otolith afferents, to the velocity signals providing the input to the velocity-to-position neural integrator and the oculomotor plant. The lowest-order, best-fit periphery/brain stem model that approximated the frequency dependence of the data consisted of a second order transfer function with two alternating poles (at 0.4 and 7.2 Hz) and zeros (at 0.035 and 3.4 Hz). In addition to clearly differentiator dynamics at low frequencies (less than approximately 0.5 Hz), there was no frequency bandwidth where the periphery/brain stem function could be approximated by an integrator, as previously suggested. In this scheme, the oculomotor plant dynamics are assumed to perform the necessary high-frequency integration as required by the reflex. The detailed frequency dependence of the data could only be precisely described by higher order functions with nonminimum phase characteristics that preclude simple filtering of afferent inputs and might be suggestive of distributed spatiotemporal processing of otolith signals in the translational VORs.

The coding of head orientations in neurons of bilateral vestibular nuclei of cats after unilateral labyrinthectomy: response to off-vertical axis rotation.

In decerebrate cats that had been acutely hemilabyrinthectomized (HL), the extracellular activities of vestibular nuclear neurons on the lesioned and labyrinth-intact sides were studied during constant-velocity off-vertical axis rotations (OVAR) in the clockwise (CW) and counterclockwise (CCW) directions (at 10 degrees tilt). Over the range of 1.75-15 degrees/s, two types of neuronal responses were identified on both sides. Some neurons showed symmetric and velocity-stable bidirectional response sensitivity (delta defined as the CW gain over the CCW gain) while other neurons exhibited asymmetric and velocity-variable delta. The mathematically derived gain tuning ratios of these two groups of neurons were within the range of one-dimensional and two-dimensional neurons respectively. The best response orientations in one-dimensional neurons and the orientations of the maximum response vector, S(max), in two-dimensional neurons were found to point in all directions on the horizontal plane. On the labyrinth-intact side, both the one-dimensional and two-dimensional neurons showed asymmetry in the neuron numbers and/or the response gains between the two roll quadrants as well as between the two pitch quadrants. In addition, both the neuron number and gain were significantly higher for neurons in the head-down/ipsilateral-side-down half-circle than those in the head-up/contralateral-side-down half-circle. None of the aforementioned asymmetries was observed on the lesioned side. That a comparable pattern of distribution was observed in the one-dimensional and two-dimensional neurons suggests that these neurons maintain a common spatial reference frame in encoding head orientational signals arising from the ipsilateral and contralateral otoliths. Furthermore, a predominance of two-dimensional neurons that exhibited a greater gain with CW rotations was observed on both sides of HL cats. Of the response dynamics observed amongst neurons on the two sides of HL cats, no difference was found with regard to the response gain and the pattern of response lead. However, a difference in response lag was observed between neurons on the two sides of HL cats. These suggest that there is a segregation of otolithic signals to reach the ipsilateral and contralateral vestibular nuclei. Taken together, the present study demonstrates that one-dimensional and two-dimensional neuronal responses could be elicited with inputs arising solely from the ipsilateral or contralateral otoliths. The observed orientational tuning and the CW-CCW asymmetry to bidirectional rotation may provide the essential directional coding of head orientations. Further, the imbalance of spatial/dynamic response patterns between the bilateral vestibular nuclei following the restriction of otolith inputs by HL implies that converging otolithic inputs from the bilateral labyrinths are essential for producing the neuronal responses in control animals. The results are also discussed in terms of the possible contribution of the various neural asymmetries between neuronal subpopulations in the bilateral vestibular nuclei to the behavioral symptoms accompanying acute HL.

Spontaneous activity of otolith-related vestibular nuclear neurons in the decerebrate rat

The discharge properties of lateral and descending vestibular neurons responsive to constant velocity off-vertical axis rotations (OVAR) in the clockwise (CW) and counterclockwise (CCW) directions, were studied at the stationary and earth-horizontal position of decerebrate adult rats. From the coefficient of variation (CV), the spontaneous activities of OVAR-responsive neurons were classified into regular and irregular patterns. Of the neurons (n = 36) that showed symmetric and stable bidirectional response sensitivity (δ defined as CW gain over CCW gain) to OVAR (10° tilt), some exhibited progressive phase shift with velocity (1.75–15°/s) while others exhibited stable response phase. Most neurons of the former group (93% or 1213) showed regular discharge pattern while only 22% (n = 523) of the latter group showed such a pattern. Though the phase-stable neurons showed a significantly higher average CV than the phase-shifted neurons, there was no significant difference between the mean spontaneous firing rates of these neurons. The neurons (n = 17) that showed asymmetric and variable δ to OVAR velocity can also be grouped - those that exhibited a greater gain with rotations directed towards the side of recording (I neurons) showed irregular discharge pattern while those that exhibited a greater gain with rotations directed towards the side contralateral to recording (C neurons) showed regular discharge pattern. The I and C neurons also exhibited significant difference in mean firing rates. The relationship between the response characteristics of the OVAR-responsive neurons and their spontaneous activity at the stationary and earth-horizontal position is discussed.

Response of medial medullary reticular neurons to otolith stimulation during bidirectional off-vertical axis rotation of the cat

In decerebrate cats, the extracellular activities of neurons in the medial medullary reticular formation were studied during constant velocity off-vertical axis rotations (OVAR) in the clockwise (CW) and counterclockwise (CCW) directions (at 10° tilt). Spontaneously active neurons demonstrated sinusoidal position-dependent discharge modulations to OVAR which selectively stimulates the otoliths. Two features of neuronal responses to bidirectional OVAR were identified. Within the velocity spectrum tested (1.75–15° /s), some neurons showed symmetric bidirectional response sensitivity (δ value) to CW and CCW rotations. The spread of the δ values of each of these neurons with velocity was small. This group of reticular neurons were described as exhibiting symmetric and velocity-stable bidirectional response sensitivity. The mathematically derived gain tuning ratios of these neurons were within the range of narrowly spatiotemporal-tuned neurons. Another group of reticular neurons, however, showed asymmetric bidirectional response sensitivity to CW and CCW rotations; a few of these neurons were responsive only to OVAR of one direction but not to both. For each of this second group of neurons, the spread of the δ values with velocity was large. These reticular neurons were described as exhibiting asymmetric and velocity-variable bidirectional response sensitivity. The gain tuning ratios of these latter neurons were found to be within the range of broadly spatiotemporal-tuned neurons. Single neurons of both groups displayed orientational tuning. Both the best response orientations of neurons that showed symmetric and velocity-stable bidirectional response sensitivity and the preferred orientations of neurons that showed asymmetric and velocity-variable bidirectional response sensitivity were found to point in all directions on the rotary plane. The response dynamics of the former group of neurons was also examined. All showed flat response gain across the entire velocity range. Some showed a flat response lead while others showed a progressive shift from small response lead at low velocity to phase close to zero at higher velocities. The functional significance of these medial medullary reticular neurons to the direction and orientation of head tilt is discussed.

Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys. II. Inertial detection of angular velocity.

1. The dynamic contribution of otolith signals to three-dimensional angular vestibuloocular reflex (VOR) was studied during off-vertical axis rotations in rhesus monkeys. In an attempt to separate response components to head velocity from those to head position relative to gravity during low-frequency sinusoidal oscillations, large oscillation amplitudes were chosen such that peak-to-peak head displacements exceeded 360 degrees. Because the waveforms of head position and velocity differed in shape and frequency content, the particular head position and angular velocity sensitivity of otolith-ocular responses could be independently assessed. 2. During both constant velocity rotation and low-frequency sinusoidal oscillations, the otolith system generated two different types of oculomotor responses: 1) modulation of three-dimensional eye position and/or eye velocity as a function of head position relative to gravity, as presented in the preceding paper, and 2) slow-phase eye velocity as a function of head angular velocity. These two types of otolith-ocular responses have been analyzed separately. In this paper we focus on the angular velocity responses of the otolith system. 3. During constant velocity off-vertical axis rotations, a steady-state nystagmus was elicited that was maintained throughout rotation. During low-frequency sinusoidal off-vertical axis oscillations, dynamic otolith stimulation resulted primarily in a reduction of phase leads that characterize low-frequency VOR during earth-vertical axis rotations. Both of these effects are the result of an internally generated head angular velocity signal of otolithic origin that is coupled through a low-pass filter to the VOR. No change in either VOR gain or phase was observed at stimulus frequencies larger than 0.1 Hz. 4. The dynamic otolith contribution to low-frequency angular VOR exhibited three-dimensional response characteristics with some quantitative differences in the different response components. For horizontal VOR, the amplitude of the steady-state slow-phase velocity during constant velocity rotation and the reduction of phase leads during sinusoidal oscillation were relatively independent of tilt angle (for angles larger than approximately 10 degrees). For vertical and torsional VOR, the amplitude of steady-state slow-phase eye velocity during constant velocity rotation increased, and the phase leads during sinusoidal oscillation decreased with increasing tilt angle. The largest steady-state response amplitudes and smallest phase leads were observed during vertical/torsional VOR about an earth-horizontal axis. 5. The dynamic range of otolith-borne head angular velocity information in the VOR was limited to velocities up to approximately 110 degrees/s. Higher head velocities resulted in saturation and a decrease in the amplitude of the steady-state response components during constant velocity rotation and in increased phase leads during sinusoidal oscillations. 6. The response characteristics of otolith-borne angular VORs were also studied in animals after selective semicircular canal inactivation. Otolith angular VORs exhibited clear low-pass filtered properties with a corner frequency of approximately 0.05-0.1 Hz. Vectorial summation of canal VOR alone (elicited during earth-vertical axis rotations) and otolith VOR alone (elicited during off-vertical axis oscillations after semicircular canal inactivation) could not predict VOR gain and phase during off-vertical axis rotations in intact animals. This suggests a more complex interaction of semicircular canal and otolith signals. 7. The results of this study show that the primate low-frequency enhancement of VOR dynamics during off-vertical axis rotation is independent of a simultaneous activation of the vertical and torsional "tilt" otolith-ocular reflexes that have been characterized in the preceding paper. (ABSTRACT TRUNCATED)