Activity of ventroposterior thalamus neurons during rotation and translation in the horizontal plane in the alert squirrel monkey

The firing behavior of 107 vestibular-sensitive neurons in the ventroposterior thalamus was studied in two alert squirrel monkeys during whole body rotation and translation in the horizontal plane. Vestibular-sensitive neurons were distributed primarily along the anterior and posterior borders of ventroposterior nuclei; three clusters of these neurons could be distinguished based on their location and inputs. Eighty-four neurons responded to rotation; 66 (78%) of them responded to rotation only and 18 (22%) to both rotation and translation. Forty-one neurons were sensitive to linear translation; 23 (56%) of them responded to translation only. The population rotational response to 0.5-Hz sinusoids with a peak velocity of 40 degrees /s showed a gain of 0.23 +/- 0.15 spike.s(-1).deg(-1).s(-1) and phase lagging behind the angular velocity by -9.3 +/- 34.1 degrees . Although rotational response amplitude increased with the stimulus velocity across the range 4-100 degrees /s, the rotational sensitivity decreased with and was inversely proportional to the stimulus velocity. The rotational response amplitude and sensitivity increased with the stimulus frequency across the range 0.2-4.0 Hz. The population response to sinusoidal translation at 0.5 Hz and 0.1 g amplitude had a gain of 111.3 +/- 53.7 spikes.s(-1).g(-1) and lagged behind stimulus acceleration by -71.9 +/- 42.6 degrees . Translational sensitivity decreased as acceleration increased and this was inversely proportional to the square root of the acceleration. Results of this study imply that changes in the discharge rate of vestibular-sensitive thalamic neurons can be approximated using power functions of the angular and linear velocity of spatial motion.     

The vestibular nerve of the chinchilla. IV. Discharge properties of utricular afferents

1. Extracellular recording techniques were used in the chinchilla to study the discharge properties of utricular afferents, including their discharge regularity, background discharge, and responses to both externally applied galvanic currents and centrifugal forces. 2. A normalized coefficient of variation (CV*), independent of discharge rate, was used to classify units as regularly (CV* less than 0.10), intermediate (0.10 less than or equal to CV* less than or equal to 0.20), or irregularly discharging (CV* greater than 0.20). In some circumstances, it was useful to recognize a group of very regularly discharging afferents (CV* less than 0.05). The CV* ranged from less than 0.020 to greater than 0.60. Regular units outnumbered irregular units by an approximate 3:1 ratio. The distribution of CV*s was bimodal: there was a major peak at CV* = 0.03 and a minor peak at CV* = 0.3. 3. Background rates were measured with the head in a horizontal position. Those of regular units usually fell between 40 and 80 spikes/s (mean: 54 spikes/s); those of irregular units were more broadly distributed (mean: 47 spikes/s). 4. Units were categorized in terms of the tilt directions resulting in increased discharge. There is a broad distribution of excitatory tilt directions with some units excited by ipsilateral rolls, others by contralateral rolls, some by nose-up pitches, and still others by nose-down pitches. In the chinchilla, there are almost equal numbers of units excited by ipsilateral or contralateral tilts. This is in contrast to previous findings in the cat and squirrel monkey, where the former units predominant by a 3:1 ratio. The difference can be related to the fact that the medial zone of the macula, where units excited by ipsilateral tilts reside, makes up a smaller proportion of the sensory epithelium in the chinchilla than in the monkey. 5. Galvanic sensitivity (beta *) and discharge regularity (CV*) were related by a power law, beta* = (CV*), with an exponent, b = 0.70. 6. Responses to sinusoidal centrifugal forces in the frequency range, f, between DC and 2 Hz were characterized by their gains (gf) and phases (phi f), taken with respect to peak linear force. Response linearity was studied by varying the amplitude of a 0.1-Hz sinusoid from 0.05 to 0.4 g. Nonlinear distortion was small (approximately 10%), as was the variation of gain (+/- 10%) and phase (+/- 5 degrees) with amplitude. 7. Response dynamics vary with discharge regularity. Very regular units are tonic. Their gains are typically 50 spikes.s-1/g and almost constant (+/- 10%) over the entire frequency range. Phases hover near zero with small (5 degrees) phase leads at low frequencies and slightly larger (10 degrees) phase lags at high frequencies. Irregular units are more phasic.(ABSTRACT TRUNCATED AT 400 WORDS)     

Neuronal activity related to vertical eye movement in the region of the interstitial nucleus of Cajal in alert cats

Summary (1) Discharge characteristics of neurons in the region of the interstitial nucleus of Cajal (INC) were studied in alert cats during spontaneous or visually induced eye movement and sinusoidal vertical (pitch) rotation. Activity of a majority of cells (n = 68) was closely related to vertical eye position with or without bursting activity during on-direction saccades. They were called vertical burst-tonic (n = 62) and tonic (n = 6) neurons. Mean discharge rates for individual cells when the eye was near the primary position ranged from 35 to 133 (mean 75) spikes/s with a coefficient of variation (CV) ranging from 0.04 to 0.29 (mean 0.15). Average rate position curves were linear for the great majority of these cells with a mean slope of 3.9 ± 1.2 SD spikes/s/deg. (2) The burst index was defined as the difference in discharge rate between maximal rate during an on-direction saccade and the tonic rate after the saccade. The values of mean burst index for individual cells ranged from 8 to 352 (mean 135) spikes/s. Tonic neurons had a burst index lower than 60 spikes/s and were distributed in the lower end of the continuous histogram, suggesting that burst-tonic and tonic neurons may be a continuous group with varying degrees of burst components. During off-direction saccades, a pause was not always observed, although discharge rate consistently decreased and pauses were seen when saccades were made further in the off-direction toward recruitment thresholds. Significant positive correlation was observed between average discharge rate during off- as well as on-direction saccades and tonic discharge rate after saccades for individual cells, which was not due to cats making saccades mainly from the primary position. (3) During pitch rotation at 0.11 Hz (±10 deg), burst-tonic and tonic neurons had mean phase lag and gain of 128 (±13 SD) deg and 4.2 (±1.7 SD) spikes/s/deg/s² relative to head acceleration. During pitch rotation of a wide frequency range (0.044–0.495 Hz), the values of phase lag were mostly constant (120–140 deg), while simultaneously recorded vertical VOR showed the mean phase lag of 178 deg. Vertical eye position sensitivity and pitch gain (re head position) showed significant positive correlation. (4) Comparison of the discharge characteristics of vertical burst-tonic and tonic neurons with those of secondary vestibulo-ocular neurons (Perlmutter et al. 1988) and extraocular motoneurons (Delgado-Garcia et al. 1986) in alert cats suggests that signals carried by burst-tonic and tonic neurons are partially processed signals in vertical VOR and saccades, and different from oculomotor signals. (5) The INC region also contained many cells that did not belong to the above groups but whose activity was clearly modulated by pitch rotation (called pitch cells for the present study, n = 44). Many (n = 23) showed some correlation with vestibular quick phases, and some (n = 12) with visually elicited eye movement, although they showed significantly lower and more irregular discharge rates than burst-tonic and tonic neurons (mean discharge rate when the eye was near the primary position 34, range 3–91, spikes/s; mean CV 0.61, range 0.15–1.7). During pitch rotation they showed the mean phase lag and gain of 119(±26 SD) deg and 3.2(±2.1 SD) spikes/s/deg/s². Some cells showed a much lower phase lag of about 90 deg. (6) More than half the burst-tonic, tonic and pitch cells tested were antidromically activated by stimuli applied to the ponto-medullary medial longitudinal fasciculus at the level of abducens nucleus, while none of them were activated from the inferior olive, suggesting that vertical eye position signals carried by some burst-tonic and tonic neurons are carried to the lower brainstem.     

Dynamics of maculo-ocular reflexes in the frog

Compensatory torsional and vertical eye movements were recorded in the frog during sinusoidal linear acceleration along the longitudinal and transverse body axes, respectively. Stimulus frequencies ranged between 0.1 and 1.0 Hz and peak accelerations from 0.01 g to 0.1 g corresponding to body tilts ranging from 0.57 to 5.7 degrees. In addition, static compensatory eye movements were studied during fore-and-aft and lateral body tilt over ranges of +/- 10 degrees. The evoked eye movements were generally quite small (+/- 0.5 degree). Dynamic gain (rotation of the eye/apparent rotation of gravity direction) was 0.10-0.20 at 0.1 Hz and decreased to about 0.05 at 1.0 Hz. The gain of vertical eye movements was somewhat higher than that of torsional eye movements. Phase lag relative to peak accelerations increased from about 10 degrees to about 45 degrees over the same frequency range. Static compensatory eye movements evoked by nose-up and ipsilateral side-up tilt were larger in amplitude than those evoked by nose-down and ipsilateral side-down tilt. Static gain (rotation of the eye/tilt of the whole body) was about 0.10 for vertical and about 0.06 for torsional eye movements. No consistent eye movements could be evoked by vertical sinusoidal accelerations (maximal modulation amplitudes +/- 0.025 g). The results indicate that, as in other vertebrates, maculo-ocular reflexes contribute to gaze stabilization in the frog mainly during low frequency and static head and body tilts.     

Contribution of oculomotor signals to the behavior of rabbit floccular Purkinje cells during reflex eye movements.

Alert pigmented rabbits were stimulated in 3 ways: (1) weak repetitive electrical stimulation (10-30 Hz) of an optic tract which induced nystagmic and after-nystagmic eye movements; (2) sinusoidal whole-body oscillation (5 degrees peak-to-peak, 0.1 Hz) which induced the horizontal vestibulo-ocular reflex (HVOR); (3) sinusoidal oscillation (2.5 degrees, 0.33 Hz) of a screen with a dot pattern which drove the horizontal optokinetic eye movement response (HOKR). Single units were recorded from Purkinje cells in the floccular H-zone where local stimulation caused a horizontal shift of the eyes. During slow phases of optic-tract-induced nystagmus and after-nystagmus, most of the H-zone Purkinje cells tested exhibited changes in discharges of simple spikes, an increase at a mean rate of 1.74 for ipsilaterally directed and 1.17 [spikes/s]/[deg/s] for contralaterally directed eye velocity. One-third of the H-zone Purkinje cells changed simple spike discharges depending on the eye position. During HVOR, most of the H-zone Purkinje cells exhibited a modulation of simple spike discharges 180 degrees out of phase to head velocity, the mean amplitude of modulation being 9.3% of the mean discharge rate. During HOKR, these cells also exhibited modulation by 13.8% in phase to screen velocity. No specific localization was found as to the relative intensities of these responses. It is estimated that an eye velocity component accounts for 18-20% and an eye position component for 5-14% of the responses of floccular H-zone Purkinje cells during HVOR and HOKR.     

Responses of vestibular nucleus neurons to tilt following chronic bilateral removal of vestibular inputs

Recordings were made from the vestibular nuclei of decerebrate cats that had undergone a combined bilateral labyrinthectomy and vestibular neurectomy 49-103 days previously and allowed to recover. Responses of neurons were recorded to tilts in multiple vertical planes at frequencies ranging from 0.05 to 1 Hz and amplitudes up to 15 degrees. Many spontaneously active neurons were present in the vestibular nuclei; the mean firing rate of these cells was 43 +/- 5 (SEM) spikes/s. The spontaneous firing of the neurons was irregular: the coefficient of variation was 0.86 +/- 0.14. The firing of 27% of the neurons was modulated by tilt. The plane of tilt that elicited the maximal response was typically within 25 degrees of pitch. The response gain was approximately 1 spikes/s/degree across stimulus frequencies. The response phase was near stimulus position at low frequencies, and lagged position slightly at higher frequencies (average of 35 +/- 9 degrees at 0.5 Hz). The source of the inputs eliciting modulation of vestibular nucleus activity during tilt in animals lacking vestibular inputs is unknown, but could include receptors in the trunk or limbs. These findings show that activation of vestibular nucleus neurons during vertical rotations is not exclusively the result of labyrinthine inputs, and suggest that limb and trunk inputs may play an important role in graviception and modulating vestibular-elicited reflexes.     

Responses of Renshaw cells coupled with hindlimb extensor motoneurons to sinusoidal stimulation of labyrinth receptors in the decerebrate cat

Contraction of ipsilateral limb extensors during side-down roll tilt of the head, leading to selective stimulation of labyrinth receptors, is attributed to an increased discharge of excitatory vestibulospinal (VS) neurons (alpha-responses) and a decreased discharge of medullary inhibitory reticulospinal (RS) neurons (beta-responses), both of which act on ipsilateral extensor motoneurons. Experiments were performed in decerebrate cats, with the de-efferented gastrocnemius-soleus (GS) muscle fixed at a constant length, to find out whether Renshaw (R) cells linked with GS motoneurons responded to labyrinth stimulation elicited by head rotation, while the neck had been bilaterally deafferented. We hoped in this way to clarify the role and the mechanism by which these inhibitory interneurons act on limb extensor motoneurons during the vestibular reflexes. 72.7% of the R-cells, disynaptically excited by group I volleys elicited by single shock stimulation of the GS nerve, weakly responded to head rotation at frequencies of 0.026-0.15 Hz and at a peak amplitude of 10 degrees. For the frequency of head rotation of 0.026 Hz, +/- 10 degrees C, most of the GS R-cells increased their firing rate during side-down head displacement (alpha-responses); some responses were related to head position, but others showed some phase lead or lag with respect to head position. The gain of the first harmonic of these unit responses was very low and corresponded on the average to 0.084 +/- 0.062, S.D. imp./s/deg, while the sensitivity corresponded to 2.14 +/- 2.35, S.D.%/deg (base frequency, 6.85 +/- 5.97, S.D. imp./s). These responses were attributed to the activity of VS neurons, the increased discharge of which during side-down head rotation exerts a weak excitatory influence on a limited number of GS motoneurons and, through their recurrent collaterals, on the related R-cells. The modulation of the firing rate of R-cells coupled with the GS motoneurons increased linearly by increasing the peak amplitude of displacement from 5 degrees to 20 degrees at the frequency of 0.026 Hz, so that the response gain remained almost unchanged. An increase in frequency of head rotation from 0.026 to 0.32 Hz at a fixed amplitude of 10 degrees, thus changing the maximal angular acceleration from 0.26 degrees/s2 to 41.7 degrees/s2, reversed the response pattern of R-cells reported above. The resulting beta-responses, which also showed some phase lead or lag with respect to head position, were attributed to vestibular activation of RS neurons.(ABSTRACT TRUNCATED AT 400 WORDS)     

Roll rotation cues influence roll tilt perception assayed using a somatosensory technique

We investigated how the nervous system processes ambiguous cues from the otolith organs by measuring roll tilt perception elicited by two motion paradigms. In one paradigm (tilt), eight subjects were sinusoidally tilted in roll with the axis of rotation near ear level. Stimulus frequencies ranged from 0.005 to 0.7 Hz, and the peak amplitude of tilt was 20 degrees . During this paradigm, subjects experienced a sinusoidal variation of interaural gravitational force with a peak of 0.34 g. The second motion paradigm (translation) was designed to yield the same sinusoidal variation in interaural force but did not include a roll canal cue. This was achieved by sinusoidally translating the subjects along their interaural axis. For the 0.7-Hz translation trial, the subjects were simply translated from side to side. A centrifuge was used for the 0.005- to 0.5-Hz translation trials; the subjects were rotated in yaw at 250 degrees /s for 5 min before initiating sinusoidal translations yielding an interaural otolith stimulus composed of both centrifugal and radial acceleration. Using a somatosensory task to measure roll tilt perception, we found substantial differences in tilt perception during the two motion paradigms. Because the primary difference between the two motion paradigms was the presence of roll canal cues during roll tilt trials, these perceptual differences suggest that canal cues influence tilt perception. Specifically, rotational cues provided by the semicircular canals help the CNS resolve ambiguous otolith cues during head tilt, yielding more accurate tilt perception.     

Effects of natural neck afferent stimulation on vestibulo-spinal neurons in the decerebrate cat

Summary The response patterns of antidromically identified vestibulo-spinal Deiters' neurons and other vestibular nuclear neurons to stimulation of neck receptors and horizontal semicircular canal receptors were investigated in precollicular decerebrate cats.The neck receptors were stimulated by sinusoidal oscillation (frequency 0.2 Hz and 10 ° amplitude) and trapezoidal movements of the cervical axis vertebrae in the horizontal plane, while the head was stereotaxically fixed in a prone position. The influence of horizontal semicircular canal receptors was examined by sinusoidal turntable oscillations (0.2 Hz, 10 °).Out of 151 antidromically driven Deiters' neurons, 16 units responded to neck rotation and 11 cells out of 148 Deiters' neurons were influenced by the horizontal semicircular canal receptors. Only 3 of these neurons were affected by convergent cervical and vestibular influences and revealed antagonistic response patterns. Neck-responsive units were found to be scattered throughout Deiters' nucleus, whereas semicircular-canal-influenced neurons were predominantly encountered in its rostro-ventral part.Altogether, 68 neck-responsive neurons in the vestibular nuclear complex were tested. These units showed a periodic, direction-specific modulation of the discharge rate in response to sinusoidal oscillation. Almost all responses were related to input angular velocity at 0.2 Hz with a mean gain of 1.15 imp/s per deg/s. During trapezoidal neck displacement, responsive units also exhibited tonical components in their discharge rates.These results suggest kinetic-static response characteristics of neck receptors. The cervico-vestibulo-spinal pathway may contribute to tonic neck reflexes; vestibular and neck reflexes may partially interact in Deiters' nucleus.Supported by Sonderforschungsbereich Hirnforschung und Sinnesphysiologie (SFB 70) der Deutschen Forschungsgemeinschaft     

Vertical eye position responses to steady-state sinusoidal fore–aft head translation in monkeys

A major function of the otolith organ is to detect linear acceleration generated by two different head conditions, dynamic linear translation and static tilt relative to gravity. To investigate these sensory functions of the otolith organ, we analyzed vertical eye position in response to steady-state sinusoidal fore–aft translation over a range of frequencies (0.5–4 Hz) and amplitudes (0.10–0.33 g) in three monkeys. Vertical vestibuloocular reflexes elicited by linear acceleration (LVORs) during sinusoidal fore–aft translation were divided into translational LVOR component and tilt LVOR component taking vertical gaze-dependent properties into account. Based on geometrical considerations, the translational LVOR component, but not the tilt LVOR component, depended on vertical gaze eccentricity. To quantify these two components, we used a V-shaped function model, plotting vertical eye sensitivities (deg/cm) against vertical gaze eccentricities (deg). The slope (deg/cm per degree) and intercept (sensitivity at zero gaze eccentricity) of this function approximately reflected the translational and tilt LVOR components, respectively. Our data show that the tilt LVOR component is independent of the reciprocal of the fixation distance (MA), whereas the translational LVOR component is almost linearly related to MA. The gain of the tilt LVOR component, characterized by low-pass dynamics, was greatest (0.36) at 0.5 Hz. Visual information clearly reduced the gain of the tilt LVOR component, by approximately 50%. There was no difference between the effects of large-field and small-spot stimuli. These findings demonstrate that steady-state sinusoidal fore–aft translation at lower frequencies stimulates the otolith organs and produces a pseudo-pitch tilt in cooperation with the gravito-inertial force and as a result elicits an ocular response equivalent to the tilt LVOR.     

Discharge patterns of levator palpebrae superioris motoneurons during vertical lid and eye movements in the monkey.

1. We recorded single-unit activity in the caudal central nucleus (CCN) of the oculomotor complex in monkeys trained to make vertical saccadic, smooth-pursuit, and fixation eye movements. We confirmed that our recordings were from motoneurons innervating the upper lid, because small lesions placed at the sites of responsive units were recovered among neurons labeled by horseradish peroxidase (HRP) injections into the levator palpebrae superioris muscle. 2. For fixations above a threshold lid position, levator motoneurons discharged at a steady rate, which increased linearly with upward lid position. The average position sensitivity during fixation was 2.9 spikes/s per deg, and the average lid motoneuron was recruited into steady firing when the eye was looking 10 degrees down. 3. During upward saccades, levator motoneurons discharged a burst of spikes that began, on average, 7.3 ms before the lid movement if the saccade started from a straight-ahead position; the lead time decreased considerably as the initial eye and lid positions shifted downward. The firing rate usually reached its peak (130-280 spikes/s) at the very onset of the burst and declined gradually during the course of the saccade. The steady rate associated with the new fixation position was reached about halfway during the saccade. All units exhibited a pause in firing during the initial half of large downward saccades; during small saccades, the pause was inconspicuous or absent. 4. During vertical sinusoidal smooth pursuit, levator motoneurons exhibited a sinusoidal modulation in firing rate, which led eye position by an average of 23 degrees at 0.3 Hz. The average velocity sensitivity calculated from such data was 0.63 spikes/s per deg/s. 5. Although they exhibit a number of qualitative similarities, the discharge patterns of levator motoneurons and superior rectus motoneurons differ in several respects. First, during a blink, when the lid undergoes a large depression but the eye exhibits only a brief transient displacement, levator motoneurons cease firing completely, whereas superior rectus motoneurons continue to discharge. Second, for all types of coordinated lid and eye movements, levator motoneurons discharge at lower firing rates than do superior rectus motoneurons. Third, during saccades, levator motoneurons have less conspicuous and shorter-lasting bursts and pauses than do motoneurons involved in rotating the eye. 6. During upward gaze, the qualitative similarity of their burst-tonic discharge patterns suggests that levator and superior rectus motoneurons receive input signals that originate from a common source, but that the signals are processed differently to deal with the different loads facing these muscles.(ABSTRACT TRUNCATED AT 400 WORDS)     

Processing of periodic whisker deflections by neurons in the ventroposterior medial and thalamic reticular nuclei

Rats employ rhythmic whisker movements to sample information in their sensory environment. To study frequency tuning and filtering characteristics of thalamic circuitry, we recorded single-unit responses of ventroposterior medial (VPm) and thalamic reticular (Rt) neurons to 1- to 40-Hz sinusoidal and pulsatile whisker deflection in lightly narcotized rats. Neuronal entrainment was assessed by a measure of the relative modulation (RM) of firing at the stimulus frequency given by the first harmonic (F1) of the cycle time histogram divided by the mean firing rate (F0). VPm signaling of both sinusoidal and periodic pulsatile whisker movements improved gradually over 1-16 and was maximal at 20-40 Hz. By contrast, the RM of Rt responses increased over 1-8 Hz, but deteriorated progressively over the 12- to 40-Hz range. In Rt, response adaptation occurred at lower stimulus frequencies and to a greater extent than in VPm. Within a train of high-frequency stimuli, Rt responses progressively decremented, possibly due to the accumulation of inhibition, whereas those of VPm neurons augmented. Mean firing rates in Rt increased 42 spikes/s over 1-40 Hz, providing tonic (low RM) inhibition during high-frequency stimulation that may enhance VPm signal-to-noise ratios. Consistent with this view, VPm mean firing rates increased only 13 spikes/s over 1-40 Hz, and inter-deflection activity was suppressed to a greater extent than stimulus-evoked responses. Rt inhibition is likely to act in concert with actions of neuromodulators in optimizing thalamic temporal signaling of high-frequency whisker movements.     

Yaw direction neurons in the cat inferior olive

1. Single units that responded to yaw rotation were recorded extracellularly in the caudal inferior olive (IO) of barbiturate-anesthetized cats. Of 276 neurons, 55 responded reliably to yaw, and extensive quantitative data were recorded from 25. 2. No yaw-sensitive IO neuron responded to somatosensory or auditory stimuli but two responded, though unreliably, to flash. 3. Yaw-sensitive IO cells fired at low (1-4 spikes/s), irregular rates during one direction of rotation. Though cells responded reliably during yaw, firing rates varied considerably from cycle to cycle. Rotation speed and acceleration were not represented in any cell's firing rate. 4. Eighty five percent (47/55) of yaw-sensitive cells fired during contralateral rotation, 9% (5/55) during ipsilateral rotation, and 6% (3/55) fired from late in the ipsilateral phase of a sinusoidal oscillation to the middle of the contralateral phase. 5. Responses were tested to 0.1-Hz sinusoidal yaw oscillations with a range of peak angular velocities (1-200 degrees/s). Thresholds were not sharp because of the cycle to cycle variability in response rates but were estimated using averaged responses. The peak rate of the most sensitive cell was driven to criterion (2 SD above spontaneous rate) by an oscillation with a peak velocity of 1 degrees/s. Other cells reached criterion between 5 and 50 degrees/s. 6. Sinusoidal oscillation at all frequencies tested (0.01-0.5 Hz) elicited approximately the same firing rates. Even at 0.01 Hz cells responded well. Responses lagged acceleration by approximately 25 degrees at 0.01 Hz and shifted to later parts of the cycle as frequency increased so that firing lagged acceleration by approximately 200 degrees at 0.5 Hz. 7. Histological reconstruction showed that yaw-sensitive neurons were recorded in olivary subnucleus beta (N beta), the dorsal cap of Kooy (DC), the posterior medial region of the medial accessory division of the inferior olive (MAO), and in the medial-lateral center of the caudal MAO. 8. Yaw-sensitive neurons in the inferior olive provide a signal to the cerebellum that indicates the direction of passive rotation over a wide range of velocity and acceleration. The signal from individual neurons does not reliably encode either rotation velocity or acceleration. Yaw-sensitive IO neurons are therefore unlike other central vestibular neurons but are similar to somatosensory IO cells which signal the presence, but not the intensity of a stimulus.     

Horizontal vestibuloocular reflex (VOR) head velocity estimation in Purkinje cell degeneration (pcd/pcd) mutant mice

The horizontal vestibuloocular reflex (VOR) of Purkinje cell degeneration (pcd/pcd) mutant mice, which lack a functional cerebellar cortex, was compared in darkness to that of wild-type animals during constant velocity yaw rotations about an earth-horizontal axis and during sinusoidal yaw rotations about an earth-vertical axis. Both wild-type and pcd/pcd mice showed a compensatory average VOR eye velocity, or bias, during constant velocity horizontal axis rotations, evidence of central neural processing of otolith afferent signals to create a signal proportional to head angular velocity. Eye velocity bias was greater in pcd/pcd mice than in wild-type mice at a low rotational velocity (32 degrees/s), but less at higher velocities (128 and 200 degrees/s). Lesion of the medial nodulus severely attenuated eye velocity bias in two wild-type mice, without attenuating VOR during sinusoidal vertical axis yaw rotations at 0.2 Hz. These results show that while head velocity estimation in mice, as in primates, depends on the cerebellum, pcd/pcd mutant mice develop velocity estimation without a functional cerebellar cortex. We conclude that neural circuits that exclude cerebellar cortex are capable of the signal processing necessary for head angular velocity estimation, but that these circuits are insufficient for normal estimation at high velocities.     

Discharge activity of spindle afferents from the gastrocnemius-soleus muscle during head rotation in the decerebrate cat

The activity of spindle afferents originating from both primary and secondary endings of the isometrically extended (6-8 mm) gastrocnemius-soleus (GS) muscle was recorded in precollicular decerebrate cats during sinusoidal head rotation about the longitudinal axis above a stationary body. In the first group of experiments to test the influence of vestibular volleys on fusimotor neurons, an acute bilateral neck deafferentation at C1-C3 was performed to eliminate possible influences arising from neck receptors; head rotation (0.026 Hz, +/- 15 degrees) induced a weak periodic rate modulation in 6/38 (15.8%) of the tested spindle afferents; the average response gain was 0.18 +/- 0.12, SD imp./s/deg (mean firing rate, 18.9 +/- 2.8 imp./s), and the average phase angle was -43.2 +/- 47.0 degrees, SD lag with respect to ipsilateral side-down displacement of the head (alpha-response pattern). In a second group of experiments head rotation studied after acute bilateral section of VIII cranial nerve, thereby stimulating only neck receptors, failed to influence in a reliable manner the firing rate of 38 additional spindle afferents. In a third group of experiments in which both VIII nerves and cervical dorsal roots were left intact, head rotation induced a response in 7/45 (15.6%) of the tested spindle afferents similar to that observed after cervical deafferentiation and thus depended on stimulation of labyrinth receptors alone. Over the examined frequency range of head rotation from 0.015 to 0.325 Hz (+/- 15 degrees), the response gain of spindle afferents was relatively stable during sinusoidal labyrinth stimulation. For most of the spindle afferents the phase angle of the response elicited at the lower frequencies was related to the direction of head orientation towards the ipsilateral sidedown, thus being attributed to labyrinth volleys originating from macular receptors; at 0325 Hz the stimulus was less effective and some units showed a phase advance relative to head position which was attributed to costimulation of canal receptors. Displacement of the muscle under study obtained by either rotation of the whole animal or body alone beneath a stationary head elicited a periodic modulation of spindle afferent discharge, independent of head orientation or type of preparation, in 51/73 (70%) of the muscle spindles tested; the average response gain was 0.20 +/- 0.19, SD imp./s/deg, and an average phase lead of +14.1 +/- 20.5 degrees, SD with respect to the peak of the ipsilateral side-down displacement of the body or of the animal was observed.(ABSTRACT TRUNCATED AT 400 WORDS)     

Activity of pursuit neurons in the caudal part of the frontal eye fields during static roll-tilt

The smooth-pursuit system and vestibular system interact to keep the retinal target image on the fovea during head and/or whole body movements. The caudal part of the frontal eye fields (FEF) in the fundus of arcuate sulcus contains pursuit neurons and the majority of them respond to vestibular stimulation induced by whole-body rotation, that activates primarily semi-circular canals, and by whole-body translation, that activates otoliths. To examine whether coordinate frames representing FEF pursuit signals are orbital or earth-vertical, we compared preferred directions during upright and static, whole-body roll-tilt in head- and trunk-restrained monkeys. Preferred directions (re monkeys’ head/trunk axis) of virtually all pursuit neurons tested (n = 21) were similar during upright and static whole-body roll-tilt. The slight shift of preferred directions of the majority of neurons could be accounted for by ocular counter-rolling. The mean (±SD) differences in preferred directions between upright and 40° right ear down and between upright and 40° left ear down were 6° (±6°) and 5° (±5°), respectively. Visual motion preferred directions were also similar in five pursuit neurons tested. To examine whether FEF pursuit neurons could signal static whole-body roll-tilt, we compared mean discharge rates of 29 neurons during fixation of a stationary spot while upright and during static, whole-body roll-tilt. Virtually all neurons tested (28/29) did not exhibit a significant difference in mean discharge rates between the two conditions. These results suggest that FEF pursuit neurons do not signal static roll-tilt and that they code pursuit signals in head/trunk-centered coordinates.     

High-frequency dynamics of regularly discharging canal afferents provide a linear signal for angular vestibuloocular reflexes.

Regularly discharging vestibular-nerve afferents innervating the semicircular canals were recorded extracellularly in anesthetized chinchillas undergoing high-frequency, high-velocity sinusoidal rotations. In the range from 2 to 20 Hz, with peak velocities of 151 degrees/s at 6 Hz and 52 degrees/s at 20 Hz, 67/70 (96%) maintained modulated discharge throughout the sinusoidal stimulus cycle without inhibitory cutoff or excitatory saturation. These afferents showed little harmonic distortion, no dependence of sensitivity on peak amplitude of stimulation, and no measurable half-cycle asymmetry. A transfer function fitting the data predicts no change in sensitivity (gain) of regularly discharging afferents over the frequencies tested but shows a phase lead with regard to head velocity increasing from 0 degrees at 2 Hz to 30 degrees at 20 Hz. These results indicate that regularly discharging afferents provide a plausible signal to drive the angular vestibuloocular reflex (VOR) even during high-frequency head motion but are not a likely source for nonlinearities present in the VOR.     

Responses of locus coeruleus and subcoeruleus neurons to sinusoidal stimulation of labyrinth receptors

In precollicular decerebrate cats the electrical activity of 141 individual neurons located in the locus coeruleus-complex, i.e. in the dorsal (n = 41) and ventral parts (n = 67) as well as in the locus subcoeruleus (n = 33), was recorded during sinusoidal tilt about the longitudinal axis of the whole animal, leading to stimulation of labyrinth receptors. Some of these neurons showed physiological characteristics attributed to the norepinephrine-containing locus coeruleus neurons, namely, (i) a slow and regular resting discharge, and (ii) a typical biphasic response to fore- and hindpaw compression consisting of short impulse bursts followed by a silent period, which has been attributed to recurrent and/or lateral inhibition of the norepinephrine-containing neurons. Furthermore, 16 out of the 141 neurons were activated antidromically by stimulation of the spinal cord at T12 and L1, thus being considered coeruleospinal or subcoeruleospinal neurons. A large number of tested neurons (80 out of 141, i.e. 56.7%) responded to animal rotation at the standard frequency of 0.15 Hz and at the peak amplitude of 10 degrees. However, the proportion of responsive neurons was higher in the locus subcoeruleus (72.7%) and the dorsal locus coeruleus (61.0%) than in the ventral locus coeruleus (46.3%). A periodic modulation of firing rate of the units was observed during the sinusoidal stimulus. In particular, 45 out of the 80 units (i.e. 56.2%) were excited during side-up and depressed during side-down tilt (beta-responses), whereas 20 of 80 units (i.e. 25.0%) showed the opposite behavior (alpha-responses). In both instances, the response peak occurred with an average phase lead of about + 18 degrees, with respect to the extreme side-up or side-down position of the animal; however, the response gain (imp./s per deg) was, on average, more than two-fold higher in the former than in the latter group. The remaining 15 units (i.e. 18.7%) showed a prominent phase shift of this response peak with respect to animal position. Similar results were obtained from the subpopulation of locus coeruleus-complex neurons which fired at a low rate (less than 5.0 imp./s), as well as for the antidromically identified coeruleospinal neurons. The response gain of locus coeruleus-complex neurons, including the coeruleospinal neurons, did not change when the peak amplitude of tilt was increased from 5 degrees to 20 degrees at the fixed frequency of 0.15 Hz. This indicates that the system was relatively linear with respect to the amplitude of displacement.(ABSTRACT TRUNCATED AT 400 WORDS)     

Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. II. Mossy fiber firing patterns during horizontal head rotation and eye movement.

1. Extracellular recordings were obtained from 113 mossu fibers (MFs) in the flocculus of alert monkeys trained to perform a visual tracking task during sinusoidal, horizontal head rotation. The analysis of MF discharge patterns was designed to allow quantitative comparison of the discharge properties of flocculus MFs with brain stem cell populations from which the MFs might originate and with flocculus Purkinje cells (P-cells). Based on their firing patterns, MFs were divided into two classes. Vestibular MFs discharged in relation to head velocity and, in some cases, also in relation to eye movement. Eye movement MFs discharged only in relation to one or more components of eye movement. 2. Vestibular MFs were subdivided into three classes. Vestibular-only MFs (n = 15) displayed a modulation in firing rate during head rotation but exhibited no relationship to spontaneous eye movements. Vestibular-plus-saccade MFs (n = 14) displayed a modulation in firing rate during head rotation that quantitatively resembled the modulation in vestibular-only MFs. In addition, a pause in firing rate interrupted the vestibular modulation during saccades in one or more directions. Vestibular-plus-position MFs (n = 4) exhibited steady firing rates that were linearly related to horizontal eye position in the absence of vestibular stimulation. Sinusoidal head rotation evoked a modulation ofiring rate above and below the firing rate set by the eye position. 3. during sinusoidal head rotation, vestibular MF firing rate led head velocity by an average of 24 degrees. The amplitude of MF firing-rate modulation increased as a function of the frequency of head rotation and, hence, maximum head velocity. Since these characteristics are similar to those displayed by P-cells during suppression of the VOR, vestibular MFs probably transmit the head velocity component of P-cell firing rate to the flocculus. Based on evidence from other mammals and a quantitative comparison of population discharge characteristics, it is likely that vestibular MFs originate from the vestibular nerve and from cells in the medial vestibular nucleus. 4. Based on their discharge patterns, eye movement MFs were also subdivided into three classes. Burst MFs (n = 14) emitted a high-frequency burst of spikes prior to and during saccades in one or more direction, but were silent during steady fixation. Burst-tonic MFs (n = 53) emitted a burst of spikes prior to saccades in a preferred ("on") direction, ceased firing during saccades in the opposite ("off") direction, and exhibited steady firing rates that increased as steady gaze shifted in the on direction. Tonic MFs (n = 13) displayed steady firing rates that increased as the position of steady gaze shifted in the on direction, and either paused or exhibited step changes in firing rate during saccades. 5. During steady fixation, 64% of tonic and burst-tonic MFs were recruited into maintained firing within +/- 10 degrees of the primary direction of gaze...     

Vertical eye movement-related secondary vestibular neurons ascending in medial longitudinal fasciculus in cat I. Firing properties and projection pathways

1. The firing characteristics and projection patterns of secondary vestibular nucleus neurons involved in the vertical vestibuloocular pathways were investigated in alert cats. Single-unit recordings were made in the medial longitudinal fasciculus (MLF) near the trochlear nucleus from axons that were monosynaptically activated after electrical stimulation of the vestibular nerve. In a total of 253 identified secondary neurons, 225 discharged in relation to vertical eye movements; 189 of these increased their firing rate for downward eye movements and 36 for upward movements. The activity of the remaining 28 axons was not related to eye movements when the head was still. 2. Virtually all of the secondary neurons with downward on-direction displayed tonic activity that was primarily related to steady eye position during fixation (DPV neurons). The slope of the relationship between firing rate and vertical eye position ranged from 1.2 to 9.1 (spikes/s)/deg with a mean of 3.2 (spikes/s)/deg. The regularity of firing was quantified by calculating the coefficient of variation (CV) of interspike intervals. A comparison of the CV in the population units indicated that DPV neurons could be classified as either regular or irregular neurons. There was a tendency for regular neurons to have higher firing rates and higher correlation coefficients for the rate-position relationships than irregular neurons. 3. During pitch rotation in the light, all the DPV neurons tested increased their firing rate with upward head rotation. Both the phase and the amplitude of the response indicated that DPV neurons discharged not only in relation to eye position but also in relation to head velocity, suggesting that they received monosynaptic input from the posterior semicircular canal. The gain and phase lag of the response relative to head velocity were measured at 0.5 Hz. The range of the gain was 1.1-5.1 (spikes/s)/(deg/s), and that of the phase lag was 18.3-62.4 degrees. There was a tendency for irregular DPV neurons to have a larger gain and smaller phase lag than regular DPV neurons. 4. Ascending and descending projection pathways were determined for 147 DPV axons. Of these, 69 ascended in the contralateral MLF with respect to their soma (crossed-DPV axons), and 78 in the ipsilateral MLF (uncrossed-DPV axons), as revealed by their monosynaptic activation from the contralateral or ipsilateral vestibular nerve. Stimulation of the caudal MLF at the level of the obex evoked direct responses caused by antidromic activation of descending collaterals in approximately 70% (49/69) of the crossed-DPV axons.(ABSTRACT TRUNCATED AT 400 WORDS)