Dynamics of vestibular neurons during rotational motion in alert rhesus monkeys

The temporal processing in the encoding of head rotation was investigated by comparing the dynamics of vestibular nuclei neurons with those of the regularly and irregularly firing semicircular canal afferents in alert rhesus monkeys. During earth-vertical axis rotations, neurons without eye movement sensitivity differed in their response dynamics from both regularly and irregularly firing semicircular canal afferents. At high frequencies, central responses increased in sensitivity and maintained phase leads of nearly 30° relative to head velocity. These persistent high-frequency phase leads resembled those of irregularly firing (but not regularly firing) semicircular canal afferents. However, at low frequencies, central responses exhibited significantly smaller phase leads than those of irregularly firing semicircular canal afferents, and dynamics resembled more those of the regularly firing afferents. The response dynamics of central non-eye movement cells were significantly different from those of position-vestibular-pause and eye-head neurons (collectively referred to as eye movement cells). In contrast to the persistent phase leads of non-eye movement neurons, all eye movement cells modulated closely in phase with head velocity at all frequencies down to 0.05 Hz during visual suppression tasks. Vertical canal non-eye movement neurons that were insensitive to both translations and static head tilts led head velocity by approximately 5–30° during high-frequency earth-horizontal axis rotations. Unlike the earth-vertical axis responses that led head velocity at low frequencies by as much as 20–40°, vertical canal neurons only slightly led or even lagged behind head velocity during low-frequency earth-horizontal axis rotations. Posterior canal central non-eye movement cells lagged behind head velocity significantly more than anterior canal neurons. These frequency dependencies of central vestibular neurons in comparison with those of the afferents suggest that both low- and high-pass filtering might be necessary to convert primary semicircular canal afferent response dynamics to central neuron ones.     

Spatial orientation of semicircular canals and afferent sensitivity vectors in pigeons

Rotational head motion in vertebrates is detected by the semicircular canal system, whose innervating primary afferent fibers carry information about movement in specific head planes. The semicircular canals have been qualitatively examined over a number of years, and the canal planes have been quantitatively characterized in several animal species. The present study first determined the geometric relationship between individual semicircular canals and between the canals and the stereotactic head planes in pigeons. Stereotactic measurements of multiple points along the circumference of the bony canals were taken, and the measured points fitted with a three-dimensional planar surface. Direction normals to the plane's surface were calculated and used to define angles between semicircular canal pairs. Because of the unusual shape of the anterior semicircular canals in pigeons, two planes, a major and a minor, were fitted to the canal's course. Calculated angle values for all canals indicated that the horizontal and posterior semicircular canals are nearly orthogonal, but the anterior canals have substantial deviations from orthogonality with other canal planes. Next, the responses of the afferent fibers that innervate each of the semicircular canals to 0.5 Hz sinusoidal rotation about an earth-vertical axis were obtained. The head orientation relative to the rotation axis was systematically varied so that directions of maximum sensitivity for each canal afferent could be determined. These sensitivity vectors were then compared with the canal plane direction normals. The afferents that innervated specific semicircular canals formed homogeneous clusters of sensitivity vectors in different head planes. The horizontal and posterior afferents had average sensitivity vectors that were largely coincident with the innervated canal plane direction normals. Anterior canal afferents, however, appeared to synthesize contributions from the major and minor plane components of the bony canal structure to produce a resultant sensitivity vector that was positioned between the canal planes. Calculated angles between the average canal afferent sensitivity vectors revealed that direction orthogonality is preserved at the afferent signal level, even though deviations from canal plane orthogonality exist.     

The response of horizontal semicircular canal afferents to sinusoidal rotation in the cat

Summary Dynamic characteristics of primary vestibular afferents innervating the horizontal semicircular canal were studied in decerebrate, unanesthetized cats. Activities of individual afferent fibers were recorded intracranially by glass micropipettes. Frequency of sinusoidal rotation was varied from 0.014 Hz to 0.42 Hz, and phase and gain properties were examined.All of the fibers recorded fired spontaneously, and their firing rate ranged from 7 to 128 spikes/sec. Regularity of firing, phase lags, and gains were calculated in individual fibers. There was a tendency that the units with high spontaneous firing rates showed regular firing, larger phase lags, and lower gains than the units with low spontaneous firing rates.The transfer function of the system (firing rate of the primary afferent per angular acceleration of the head) was . A high frequency phase lead component was needed to account for the data obtained, indicating a slight deviation from the relationship predicted by the torsion pendulum model.The present phase properties were compared with those of vestibular nucleus neurons reported previously. It was suggested that a group of vestibular nucleus neurons transmits fairly faithfully the phase properties of primary afferents, and that another group of vestibular nucleus neurons receive additional influences from central structures, exhibiting larger phase lags than primary afferents.     

Asymmetric integration recorded from vestibular-only cells in response to position transients

Angular and translational accelerations excite the semicircular canals and otolith organs, respectively. While canal afferents approximately encode head angular velocity due to the biomechanical integration performed by the canals, otolith signals have been found to approximate head translational acceleration. Because central vestibular pathways require velocity and position signals for their operation, the question has been raised as to how the integration of the otolith signals is accomplished. We recorded responses from 62 vestibular-only neurons in the vestibular nucleus of two monkeys to position transients in the naso-occipital and interaural orientations and varying directions in between. Responses to the transients were directionally asymmetric; one direction elicited a response that approximated the integral of the acceleration of the stimulus. In the opposite direction, the cells simply encoded the acceleration of the motion. We present a model that suggests that a neural integrator is not needed. Instead a neuron with a long membrane time constant and an excitatory postsynaptic potential duration that increases with the firing rate of the presynaptic cell can emulate the observed behavior.     

Properties of cerebellar fastigial neurons during translation, rotation, and eye movements

The most medial of the deep cerebellar nuclei, the fastigial nucleus (FN), receives sensory vestibular information and direct inhibition from the cerebellar vermis. We investigated the signal processing in the primate FN by recording single-unit activities during translational motion, rotational motion, and eye movements. Firing rate modulation during horizontal plane translation in the absence of eye movements was observed in all non-eye-movement-sensitive cells and 26% of the pursuit eye-movement-sensitive neurons in the caudal FN. Many non-eye-movement-sensitive cells recorded in the rostral FN of three fascicularis monkeys exhibited convergence of signals from both the otolith organs and the semicircular canals. At low frequencies of translation, the majority of these rostral FN cells changed their firing rates in phase with head velocity rather than linear acceleration. As frequency increased, FN vestibular neurons exhibited a wide range of response dynamics with most cells being characterized by increasing phase leads as a function of frequency. Unlike cells in the vestibular nuclei, none of the rostral FN cells responded to rotational motion alone, without simultaneously exhibiting sensitivity to translational motion. Modulation during earth-horizontal axis rotation was observed in more than half (77%) of the neurons, although with smaller gains than during translation. In contrast, only 47% of the cells changed their firing rates during earth-vertical axis rotations in the absence of a dynamic linear acceleration stimulus. These response properties suggest that the rostral FN represents a main processing center of otolith-driven information for inertial motion detection and spatial orientation.     

Afferent innervation patterns of the pigeon horizontal crista ampullaris

The vestibular semicircular canals are responsible for detection of rotational head motion although the precise mechanisms underlying the transduction and encoding of movement information are still under study. In the present investigation, we utilized neural tracers and immunohistochemistry to quantitatively examine the topology and afferent innervation patterns of the horizontal semicircular canal crista (HCC) in pigeons (Columba livia). Two hundred and eighty-six afferents from five horizontal canal organs were identified of which 92 units were sufficiently labeled and isolated to perform anatomical reconstructions. In addition, a three-dimensional contour map of the crista was constructed. Bouton afferents were located only in the peripheral regions of the receptor epithelium. Bouton afferents had the most complex innervation patterns with significantly longer and more numerous branches as well as a higher branch order than any other fiber type. Bouton fibers also contained significantly more bouton terminals than did dimorph afferents. Calyx afferents were located only in the apex and central planar regions. Calyx fibers had the largest axonal diameters yet the smallest fiber lengths and innervation areas, the fewest number of branches, the lowest branch order, and the fewest total number of terminals of all fiber types. Dimorph afferents were located throughout the central crista with afferent terminations that were larger and more complex than calyx fibers but less so than bouton fibers. Overall, the pigeon HCC morphology and innervation shares many common features with those of other animal classes.     

Angular velocity detection by head movements orthogonal to the plane of rotation

Sinusoidal oscillation of rhesus monkeys about a head-fixed, earth-horizontal axis while rotating at constant velocity about an earth-vertical axis generates a characteristic ocular nystagmus where the three-dimensional slow phase eye velocity is compensatory to the spatially and temporally changing head angular velocity vector. This includes the generation of a unidirectional nystagmus characterised by a bias slow phase velocity component, albeit of small gain (0.2–0.7), that persists for the duration of the combined two-axes stimulation and is compensatory to the constant velocity earth-vertical axis rotation. Specifically, there is a torsional bias velocity in supine position, a vertical bias velocity in ear down position and a horizontal bias velocity in upright position. Since the semicircular canals can not sense prolonged constant velocity rotation, the ocular bias velocity must be centrally constructed from canal afferent signals using head position information. Thus, optimal performance of the vestibular system as a three-dimensional rate sensor relies on afferent information from both the semicircular canals and the otolith organs.     

Habituation and adaptation of the vestibuloocular reflex: a model of differential control by the vestibulocerebellum

Summary We habituated the dominant time constant of the horizontal vestibuloocular reflex (VOR) of rhesus and cynomolgus monkeys by repeated testing with steps of velocity about a vertical axis and adapted the gain of the VOR by altering visual input with magnifying and reducing lenses. After baseline values were established, the nodulus and ventral uvula of the vestibulocerebellum were ablated in two monkeys, and the effects of nodulouvulectomy and flocculectomy on VOR gain adaptation and habituation were compared. The VOR time constant decreased with repeated testing, rapidly at first and more slowly thereafter. The gain of the VOR was unaffected. Massed trials were more effective than distributed trials in producing habituation. Regardless of the schedule of testing, the VOR time constant never fell below the time constant of the semicircular canals (5 s). This finding indicates that only the slow component of the vestibular response, the component produced by velocity storage, was habituated. In agreement with this, the time constant of optokinetic after-nystagmus (OKAN) was habituated concurrently with the VOR. Average values for VOR habituation were obtained on a per session basis for six animals. The VOR gain was adapted by natural head movements in partially habituated monkeys while they wore ×2.2 magnifying or ×0.5 reducing lenses. Adaptation occurred rapidly and reached about ±30%, similar to values obtained using forced rotation. VOR gain adaptation did not cause additional habituation of the time constant. When the VOR gain was reduced in animals with a long VOR time constant, there were overshoots in eye velocity that peaked at about 6–8 s after the onset or end of constant-velocity rotation. These overshoots occurred at times when the velocity storage integrator would have been maximally activated by semicircular canal input. Since the activity generated in the canals is not altered by visual adaptation, this finding indicates that the gain element that controls rapid changes in eye velocity in the VOR is separate from that which couples afferent input to velocity storage. Nodulouvulectomy caused a prompt and permanent loss of habituation, returning VOR time constants to initial values. VOR gain adaptation, which is lost after flocculectomy, was unaffected by nodulouvulectomy. Flocculectomy did not alter habituation of the VOR or of OKAN. Using a simplified model of the VOR, the decrease in the duration of vestibular nystagmus due to habituation was related to a decrement in the dominant time constant of the velocity storage integrator (1/h ₀). Nodulouvulectomy, which reversed habituation, would be effected by decreasing h ₀, thereby increasing the VOR time constant. Small values of h ₀ would cause velocity storage to approach an ideal integrative process, leading the system to become unstable. By controlling the VOR time constant through habituation, the nodulus and uvula can stabilize the slow component of the VOR. VOR gain adaptation was related to a modification of the direct vestibular path gain g ₁, without altering the coupling to velocity storage g ₀ or its time constant (1/h ₀). The mismatched direct- and indirect-pathway gains simulated the overshoots in the dynamic response to a step in velocity, that were observed experimentally. We conclude that independent distributed elements in the VOR modify its dynamic response, under control of separate parts of the vestibulocerebellum.     

Spatiotemporal processing of linear acceleration: primary afferent and central vestibular neuron responses

Spatiotemporal convergence and two-dimensional (2-D) neural tuning have been proposed as a major neural mechanism in the signal processing of linear acceleration. To examine this hypothesis, we studied the firing properties of primary otolith afferents and central otolith neurons that respond exclusively to horizontal linear accelerations of the head (0.16-10 Hz) in alert rhesus monkeys. Unlike primary afferents, the majority of central otolith neurons exhibited 2-D spatial tuning to linear acceleration. As a result, central otolith dynamics vary as a function of movement direction. During movement along the maximum sensitivity direction, the dynamics of all central otolith neurons differed significantly from those observed for the primary afferent population. Specifically at low frequencies (相似文献   

Static and dynamic discharge properties of vestibular-nerve afferents in the mouse are affected by core body temperature

The goal of this study was to determine the effect of changes in core body temperature on the resting discharge rate and sensitivity of vestibular-nerve afferents. Extracellular recordings were made from vestibular-nerve afferents innervating the semicircular canals in anesthetized C57BL/6 mice maintained at a core body temperature of either 30–32°C (T ₃₁) or 35–37°C (T ₃₆). The resting rates of regular (CV* < 0.1) and irregular afferents (CV* > 0.1) were lower at T ₃₁ than at T ₃₆. Sensitivity and phase were compared for rotations ranging from 0.1 to 12 Hz by calculating coefficients of a transfer function, $ g \cdot t_{c} s \cdot ( {t_{z} s + 1} )/( {t_{c} s + 1}) $ , for each afferent. The sensitivity (g) increased with CV* and with higher core body temperature. The value of the coefficient representing the low-frequency dynamics (t _c) varied inversely with CV* but did not change with core body temperature. The high-frequency dynamics represented by t _z increased with CV* and decreased with higher core body temperature. These findings indicate that changes in temperature have effects on the static and dynamic properties of vestibular-nerve afferents.     

Influence of surgical plugging on horizontal semicircular canal mechanics and afferent response dynamics.

Mechanical occlusion of one or more of the semicircular canals is a surgical procedure performed clinically to treat certain vestibular disorders and used experimentally to assess individual contributions of separate canals and/or otoliths to vestibular neural pathways. The present experiments were designed to determine if semicircular canal afferent nerve modulation to angular head acceleration is blocked by occlusion of the endolymphatic duct, and if not, what mechanism(s) might account for a persistent afferent response. The perilymphatic space was opened to gain acute access to the horizontal canal (HC) in the oyster toadfish, Opsanus tau. Firing rate responses of HC afferents to sinusoidal whole-body rotation were recorded in the unoccluded control condition, during the process of duct occlusion, and in the plugged condition. The results show that complete occlusion of the duct did not block horizontal canal sensitivity; individual afferents often exhibited a robust firing rate modulation in response to whole-body rotation in the plugged condition. At high stimulus frequencies (about >8 Hz) the average sensitivity (afferent gain; spikes/s per degrees /s of head velocity) in the plugged condition was nearly equal to that observed for unoccluded controls in the same animals. At low stimulus frequencies (about <0.1 Hz), the average sensitivity in the plugged condition was attenuated by more than two orders of magnitude relative to unoccluded controls. The peak afferent firing rate for sinusoidal stimuli was phase advanced approximately 90 degrees in plugged canals relative to their control counterparts for stimulus frequencies approximately 0.1-2 Hz. Data indicate that afferents normally sensitive to angular velocity in the control condition became sensitive to angular acceleration in the plugged condition, whereas afferents sensitive to angular acceleration in the control condition became sensitive to the derivative of acceleration or angular jerk in the plugged condition. At higher frequencies (>8 Hz), the phase of afferents in the plugged condition became nearly equal, on average, to that observed in controls. A three-dimensional biomechanical model of the HC was developed to interpret the residual response in the plugged condition. Labyrinthine fluids were modeled as incompressible and Newtonian; the membranous duct, osseous canal and temporal bone were modeled as visco-elastic materials. The predicted attenuation and phase shift in cupular responses were in close agreement with the observed changes in afferent response dynamics after canal plugging. The model attributes the response of plugged canals to labyrinthine fluid pressure gradients that lead to membranous duct deformation, a spatial redistribution of labyrinthine fluids and cupular displacement. Validity of the model was established through its ability to predict: the relationship between plugged canal responses and unoccluded controls (present study), the relationship between afferent responses recorded during mechanical indentation of the membranous duct and physiological head rotation, the magnitude and phase of endolymphatic pressure generated during HC duct indentation, and previous model results for cupular gain and phase in the rigid-duct case. The same model was adjusted to conform to the morphology of the squirrel monkey and of the human to investigate the possible influence of canal plugging in primates. Membranous duct stiffness and perilymphatic cavity stiffness were identified as the most salient model parameters. Simulations indicate that canal plugging may be the most effective in relatively small species having small labyrinths, stiff round windows, and stiff bony perilymphatic enclosures.     

Responses of irregularly discharging chinchilla semicircular canal vestibular-nerve afferents during high-frequency head rotations

Mammalian vestibular-nerve afferents innervating the semicircular canals have been divided into groups according to their discharge regularity, gain at 2-Hz rotational stimulation, and morphology. Low-gain irregular afferents terminate in calyx endings in the central crista, high-gain irregular afferents synapse more peripherally in dimorphic (bouton and calyx) endings, and regular afferents terminate in the peripheral zone as bouton-only and dimorphic endings. The response dynamics of these three groups have been described only up to 4 Hz in previous studies. Reported here are responses of chinchilla semicircular canal vestibular-nerve afferents to rotational stimuli at frequencies up to 16 Hz. The sensitivity of all afferents increased with increasing frequency with the sensitivity of low-gain irregular afferents increasing the most and matching the high-gain irregular afferents at 16 Hz. All afferents increased their phase lead with respect to stimulus velocity at higher frequencies with the highest leads in low-gain irregular afferents and the lowest in regular afferents. No attenuation of sensitivity or shift in phase consistent with the presence of a high-frequency pole over the range tested was noted. Responses were best fit with a torsion-pendulum model combined with a lead operator (tau(HF1)s + 1)(tau(HF2)s + 1). The discharge regularity of individual afferents was correlated to the value of each afferent's lead operator time constants. These findings suggest that low-gain irregular afferents are well suited for encoding the onset of rapid head movements, a property that would be advantageous for initiation of reflexes with short latency such as the vestibulo-ocular reflex.     

Prototype Neural Semicircular Canal Prosthesis using Patterned Electrical Stimulation

The design of a prototype semicircular canal prosthesis is presented along with preliminary results. This device measures angular velocity of the head (±500°/s) using a piezoelectric vibrating gyroscope. With a digital filter this velocity is filtered to match the dynamic characteristics of the semicircular canals, which are the physiological rotation sensors of the vestibular system. This digitally filtered signal is used to modulate the pulse rate of electrical stimulation. The pulse rate is varied between 50 and 250 Hz via a sigmoidal lookup table relating pulse rate to angular velocity; the steady-state rate is 150 Hz. A current source utilizes these timing pulses to deliver charge balanced, cathodic-first, biphasic, current pulses to the nerves innervating the semicircular canal via platinum electrodes. Power is supplied via lithium batteries. dc/dc converters are used to generate regulated ±5 V supplies from the batteries. All of the components are contained in a small, lightweight, Nylon box measuring roughly 43 mm×31 mm×25 mm, which can be mounted on the top of an animal's head. This device has been tested in guinea pigs having surgically implanted platinum electrodes, and the results show that the prosthesis can provide a rotational cue to the nervous system. © 2000 Biomedical Engineering Society. PAC00: 4366Ts, 8719Nn, 8719La, 8780Xa     

Responses of pigeon horizontal semicircular canal afferent fibers. I. Step, trapezoid, and low-frequency sinusoid mechanical and rotational stimulation

1. The horizontal semicircular canals of anesthetized (barbiturate/ketamine) pigeons were stimulated by rotational and by mechanical stimulation. 2. The mechanical stimulation consisted of making a small (less than 1 mm) fistula in the lateral part of the bony horizontal semicircular canal and, after inserting a probe coupled to a piezoelectric micropusher through the fistula, providing controlled indentation of the exposed membranous horizontal semicircular duct. 3. Extracellular action potentials from single horizontal semicircular canal primary afferent (HCA) fibers were recorded during sinusoidal rotational and during step, ramp, and sinusoidal mechanical stimulation. 4. The mean spontaneous discharge rate of 160 horizontal canal afferents was 86 +/- 4 (SE) spikes/s. This rate was not significantly different from that reported previously for pigeon HCA fibers recorded with the horizontal canal intact (i.e., no fistula introduced). 5. Sinusoidal mechanical indentation of the horizontal semicircular duct produced clearly entrained action potentials on 36 HCA fibers for a range of peak displacements from +/- 0.5 to +/- 30 microns. Action potentials were never modulated on afferents (n greater than 100) identified as innervating the anterior and posterior semicircular canals or the otolith organs during mechanical stimulation of the horizontal semicircular canal, even for displacements as large as 30 microns. 6. Intensity functions relating peak firing frequency (spikes per second) and peak probe displacement (micrometers) for 1.0-Hz sinusoidal mechanical stimulation were linear over the range 1.0-5.0 microns. The most sensitive units (6/36, 17%) showed response saturation as the stimulus magnitude was extended to 7 microns and beyond. 7. In 15 of 36 units, both mechanical and rotational sinusoidal stimulation (1.0 Hz) were applied to the same unit. The duct indentation magnitudes were 1.0, 2.5, 5.0, and 7.0 microns and the rotational velocities were 5, 10, and 20 deg/s. The constant of proportionality found to equate the peak response produced by rotational to that elicited by mechanical stimulation was 7.0 deg.sec-1/1.0 microns. 8. Bode plots and best-fit transfer functions of the frequency response (0.05-10.0 Hz) of 14 HCAs exposed to both mechanical and rotational stimulation were nearly identical. 9. Parameters for best-fit transfer functions, responses to step, and trapezoidal duct displacements were in excellent agreement with previous rotational studies carried out using the pigeon. 10. Although the mechanisms by which focal identation of the horizontal membranous duct produce responses have not yet been determined, primary afferent responses using this method of stimulation are directly comparable with rotatory stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)     

Bone conducted vibration selectively activates irregular primary otolithic vestibular neurons in the guinea pig

The main objective of this study was to determine whether bone-conducted vibration (BCV) is equally effective in activating both semicircular canal and otolith afferents in the guinea pig or whether there is preferential activation of one of these classes of vestibular afferents. To answer this question a large number (346) of single primary vestibular neurons were recorded extracellularly in anesthetized guinea pigs and were identified by their location in the vestibular nerve and classed as regular or irregular on the basis of the variability of their spontaneous discharge. If a neuron responded to angular acceleration it was classed as a semicircular canal neuron, if it responded to maintained roll or pitch tilts it was classified as an otolith neuron. Each neuron was then tested by BCV stimuli—either clicks, continuous pure tones (200–1,500 Hz) or short tone bursts (500 Hz lasting 7 ms)—delivered by a B-71 clinical bone-conduction oscillator cemented to the guinea pig's skull. All stimulus intensities were referred to that animal's own auditory brainstem response (ABR) threshold to BCV clicks, and the maximum intensity used was within the animal's physiological range and was usually around 70 dB above BCV threshold. In addition two sensitive single axis linear accelerometers cemented to the skull gave absolute values of the stimulus acceleration in the rostro-caudal direction. The criterion for a neuron being classed as activated was an audible, stimulus-locked increase in firing rate (a 10% change was easily detectable) in response to the BCV stimulus. At the stimulus levels used in this study, semicircular canal neurons, both regular and irregular, were insensitive to BCV stimuli and very few responded: only nine of 189 semicircular canal neurons tested (4.7%) showed a detectable increase in firing in response to BCV stimuli up to the maximum 2 V peak-to-peak level we delivered to the B-71 oscillator (which produced a peak-to-peak skull acceleration of around 6–8 g and was usually around 60–70 dB above the animal's own ABR threshold for BCV clicks). Regular otolithic afferents likewise had a poor response; only 14 of 99 tested (14.1%) showed any increase in firing rate up to the maximum BCV stimulus level. However, most irregular otolithic afferents (82.8%) showed a clear increase in firing rate in response to BCV stimuli: of the 58 irregular otolith neurons tested, 48 were activated, with some being activated at very low intensities (only about 10 dB above the animal's ABR threshold to BCV clicks). Most of the activated otolith afferents were in the superior division of the vestibular nerve and were probably utricular afferents. That was confirmed by evidence using juxtacellular injection of neurobiotin near BCV activated neurons to trace their site of origin to the utricular macula. We conclude there is a very clear preference for irregular otolith afferents to be activated selectively by BCV stimuli at low stimulus levels and that BCV stimuli activate some utricular irregular afferent neurons. The BCV generates compressional and shear waves, which travel through the skull and constitute head accelerations, which are sufficient to stimulate the most sensitive otolithic receptor cells.     

Low-frequency physiological activation of the vestibular utricle causes biphasic modulation of skin sympathetic nerve activity in humans

We have previously shown that sinusoidal galvanic vestibular stimulation, a means of selectively modulating vestibular afferent activity, can cause partial entrainment of sympathetic outflow to muscle and skin in human subjects. However, it influences the firing of afferents from the entire vestibular apparatus, including the semicircular canals. Here, we tested the hypothesis that selective stimulation of one set of otolithic organs—those located in the utricle, which are sensitive to displacement in the horizontal axis—could entrain sympathetic nerve activity. Skin sympathetic nerve activity (SSNA) was recorded via tungsten microelectrodes inserted into cutaneous fascicles of the common peroneal nerve in 10 awake subjects, seated (head vertical, eyes closed) on a motorised platform. Slow sinusoidal accelerations–decelerations (~4 mG) were applied in the X (antero-posterior) or Y (medio-lateral) direction at 0.08 Hz; composite movements in both directions were also applied. Subjects either reported feeling a vague sense of movement (with no sense of direction) or no movement at all. Nevertheless, cross-correlation analysis revealed a marked entrainment of SSNA for all types of movements: vestibular modulation was 97 ± 3 % for movements in the X axis and 91 ± 5 % for displacements in the Y axis. For each sinusoidal cycle, there were two major peaks of modulation—one associated with acceleration as the platform moved forward or to the side, and one associated with acceleration in the opposite direction. We interpret these observations as reflecting inertial displacement of the stereocilia within the utricle during acceleration, which causes a robust vestibulosympathetic reflex.     

Neural basis for eye velocity generation in the vestibular nuclei of alert monkeys during off-vertical axis rotation

Summary Activity of vestibular only (VO) and vestibular plus saccade (VPS) units was recorded in the rostral part of the medial vestibular nucleus and caudal part of the superior vestibular nucleus of alert rhesus monkeys. By estimating the null axes of recorded units (n = 79), the optimal plane of activation was approximately the mean plane of reciprocal semicircular canals, i.e., lateral canals, left anterior-right posterior (LARP) canals or right anterior-left posterior (RALP) canals. All units were excited by rotation in a direction that excited a corresponding ipsilateral semicircular canal. Thus, they all displayed a type I response. With the animal upright, there were rapid changes in firing rates of both VO and VPS units in response to steps of angular velocity about a vertical axis. The units were bidirectionally activated during vestibular nystagmus (VN), horizontal optokinetic nystagmus (OKN), optokinetic afternystagmus (OKAN) and off-vertical axis rotation (OVAR). The rising and falling time constants of the responses to rotation indicated that they were closely linked to velocity storage. There were differences between VPS and VO neurons in that activity of VO units followed the expected time course in response to a stimulus even during periods of drowsiness, when eye volocity was reduced. Firing rates of VPS units, on the other hand, were significantly reduced in the drowsy state. Lateral canal-related units had average firing rates that were linearly related to the bias or steady state level of horizontal eye velocity during OVAR over a range of ±60 deg/s. These units could be further divided into two classes according to whether they were modulated during OVAR. Non-modulated units (n = 5) were VO types and all modulated units (n = 5) were VPS types. There was no significant difference between the bias level sensitivities relative to eye velocity of the units with and without modulation (P>0.05). The modulated units had no sustained change in firing rate in response to static head tilts and their phases relative to head position varied from unit to unit. The phase did not appear to be linked to the modulation of horizontal eye velocity during OVAR. The sensitivities of unit activity to eye velocity were similar during all stimulus modalities despite the different gains of eye velocity vs stimulus velocity during VN, OKN and OVAR. Therefore, VO and VPS units are likely to carry an eye velocity signal related to velocity storage. For example, when unit sensitivities were related to head or surround velocity, sensitivity relative to OVAR was less than for VN or OKN. Firing rates of both vertical canal-related VO and VPS units (n= 19) were strongly modulated during OVAR, although they did not show changes in discharge rate during static head tilts relative to the spatial vertical up to a maximal 25 deg. In some cases the amplitude of the modulation increased with increases in head velocity and eye velocity. Average activity of vertical canal-related units was linearly related to steady state horizontal eye velocity in the ipsilateral direction during OVAR. The mean sensitivities of RALP units were not significantly different from those of LARP neurons (P>0.05). Together, their mean sensitivity during OVAR about a subject yaw axis was 0.34 (imp/s)/(deg/s) relative to horizontal eye velocity. This could be explained as a contribution of the vertical canals to horizontal eye velocity due to their orientation in the head. During OVAR to the ipsilateral side, the bias level of neuronal activity decreased and saturated. For steps of rotation about a vertical axis with the animal upright, the firing rates of RALP and LARP units were linearly related to stimulus velocity and eye velocity. Contralateral rotation excited the units reflecting the orientation of the semicircular canals relative to the yaw axis of rotation. RALP and LARP units also responded during horizontal optokinetic stimulation producing both OKN and OKAN. All the vertical canal units had dynamic characteristics closely related to velocity storage. Their response characteristics were consistent with the model that they contribute to horizontal slow phase velocity as part of a three-dimensional system based on a semicircular canal frame of reference. Otolith-related units (n= 5) in the vestibular nuclei showed no evidence of velocity storage and were modulated in accordance with head position during OVAR. Mean amplitude of the modulation of activity during OVAR at a 20 deg tilt and 60 deg/s rotational velocity was 24 imp/s. The data indicate that the vestibular nuclei contain the requisite signals to generate horizontal eye velocity during OVAR. VO and VPS units probably contribute to the bias or velocity storage component while otolith units mainly contribute to the oscillations in eye velocity by generating gravity dependent eye position changes during OVAR. In addition to the velocity storage component of horizontal eye velocity, the vertical VO neurons also have oscillations in their discharge patterns probably related to the vertical component of eye movements generated by the velocity storage integrator.     

人内耳半规管嵴顶时间常数的定量分析

目的 通过数值仿真和实验定量探究人内耳前庭半规管中的嵴顶时间常数,明确半规管编码角运动的时间过程。方法 建立人双耳半规管数值模型,通过流固耦合数值模拟嵴顶的生物力学响应,进而计算嵴顶的力学松弛时间常数。同时,对志愿者进行前庭眼反射实验,根据志愿者的眼震慢相角速度计算嵴顶的时间常数。结果 通过人内耳半规管数值模型计算得出的嵴顶力学松弛时间常数为3.75 s。通过实验测量得出平均嵴顶时间常数约为4.86 s。数值模型和实验中的结果近似保持一致。结论 人内耳前庭半规管中的嵴顶时间常数大约为4.86 s,反映了嵴顶力学松弛和半规管传入神经适应性的联合作用效果,体现了半规管编码角运动的时间过程。     

Spatial and temporal properties of eye movements produced by electrical stimulation of semicircular canal afferents

To investigate the characteristics of eye movements produced by electrical stimulation of semicircular canal afferents, we studied the spatial and temporal features of eye movements elicited by short-term lateral canal stimulation in two squirrel monkeys with plugged lateral canals, with the head upright or statically tilted in the roll plane. The electrically induced vestibuloocular reflex (eVOR) evoked with the head upright decayed more quickly than the stimulation signal provided by the electrode, demonstrating an absence of the classic velocity storage effect that improves the dynamics of the low-frequency VOR. When stimulation was provided with the head tilted in roll, however, the eVOR decayed more rapidly than when the head was upright, and a cross-coupled vertical response developed that shifted the eye's rotational axis toward alignment with gravity. These results demonstrate that rotational information provided by electrical stimulation of canal afferents interacts with otolith inputs (or other graviceptive cues) in a qualitatively normal manner, a process that is thought to be mediated by the velocity storage network. The observed interaction between the eVOR and graviceptive cues is of critical importance for the development of a functionally useful vestibular prosthesis. Furthermore, the presence of gravity-dependent effects (dumping, spatial orientation) despite an absence of low-frequency augmentation of the eVOR has not been previously described in any experimental preparation.