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Flocculectomy and unit activity in the vestibular nuclei during visual-vestibular interactions.

Activity of neurons in the vestibular nuclei of alert monkeys was recorded extracellularly after total unilateral and bilateral flocculectomy and partial paraflocculectomy. Type 1 horizontal cells that were encountered after flocculectomy responded to visual and vestibular stimuli and to conflict stimulation, i.e., to rotation in a subject-stationary visual surround, as do vestibular neurons in the normal animal. The major difference between neurons in the normal and lesioned animals was that more time was needed to reach steady state firing levels during optokinetic stimulation at a constant velocity after operation. As shown previously (Waespe et al. 1983) the longer time course is related to increased initial retinal slip velocities that occur after flocculectomy as a result of an inability to change eye velocity rapidly in response to visual stimulation. It does not signify a change in the dynamics of neurons in the vestibular nuclei that mediate the vestibulo-ocular reflex (VOR). The similarity in modulation of horizontal Type 1 vestibular neurons in normal and flocculectomized monkeys makes it unlikely that floccular Purkinje cells suppress the horizontal VOR in the monkey during conflicting visual and vestibular stimuli by inhibiting or disfacilitating secondary or tertiary vestibular neurons. This is consistent with earlier findings that indicate that visual-oculomotor pathways responsible for ocular pursuit or for rapid changes in OKN do not go through the vestibular nuclei. Rather the point of interaction of the flocculus output with the VOR appears to be external to the vestibular nuclei. There was a close correspondence between the slow phase velocity of nystagmus and unit activity in the vestibular nuclei under a wide variety of test conditions after flocculectomy. This is consistent with the postulate that frequencies of vestibular nuclei neurons represent a summation of activity in direct vestibulo-oculomotor pathways and indirect pathways that include the velocity storage mechanism. These are the major remaining sources of activity that generate slow phases of nystagmus after the direct visual-oculomotor pathways have been partially interrupted by flocculectomy (Waespe et al. 1983). Horizontal Type 1 neurons which responded to vestibular and optokinetic stimulation with increases in frequency above 1 spike/s/degree/s were rarely encountered after flocculectomy. These cells were present on the normal side in a monkey after unilateral flocculectomy. We infer that vestibular nuclei neurons that project mossy fibers to the flocculus are inactivated or disappear as a result of surgical ablation of their axons. This could also contribute to the reduced gain of vestibular nystagmus, OKAN and off-vertical nystagmus that was observed in some of the animals after lesion.

Animals↗

Canal-neck interaction in vestibular nuclear neurons of the cat.

The convergence and interaction of horizontal semicircular canal and neck proprioceptive inputs were studied in neurons of the caudal two thirds of the vestibular nuclear complex. Extracellular neuron activity was recorded under muscle relaxation and slight anesthesia in chronically prepared cats. The following stimulations were applied: horizontal rotations of (a) the whole body (labyrinth stimulation), (b) the trunk vs. the stationary head (neck stimulation), and (c) the head vs. the stationary trunk (combined labyrinth and neck stimulation). Of 152 neurons investigated, 83 (55%) showed convergence of the two inputs. In about half of these neurons, the neck input was very weak and hardly affected the labyrinthine response during head rotation. Judged from the response pattern, several of these neurons presumably were related to vestibulo-oculomotor function (i.e., vestibular nystagmus). In the other half (i.e., 27% of all neurons), sensitivity of the two inputs was similar. Both labyrinthine and neck responses contained a dynamic ("velocity") component; neck responses of more than half of these neurons had, in addition, a static ("position") component. The dynamic components were either "antagonistic" or "synergistic" as to their convergence during head rotation. When applying this combined stimulation, the dynamic components summed linearly, yielding subtration in case of antagonistic convergence and addition in case of synergistic convergence. In contrast, the static components of the neck responses remained largely unchanged during head rotation. However, the static head-to-trunk deflection determined the tonic discharge level in such neurons and thus facilitated or disfacilitated the dynamic responses to superimposed labyrinth stimulation. We suggest that the two patterns of labyrinthine neck interaction observed in vestibular nuclear neurons, i.e., subtration and addition, may be involved in the postural control of the trunk and head, respectively. In contrast, interference of the neck input with vestibulo-oculomotor function appears to be almost negligible in the intact cat.

Animals↗

Arthrokinetic nystagmus and ego-motion sensation.

A compelling illusion of body rotation and nystagmus can be induced when the horizontally extended arm of a stationary subject is passively rotated about a vertical axis in the shoulder joint. Lateral nystagmus with the fast phase beating in the opposite direction to the arm movement was found consistently; the mean slow phase velocity increased with increasing actual arm velocity and reached about 15 degrees/sec; the mean position of the eyes was deviated towards the fast phase as in optokinetic nystagmus, and the nystagmus continued after the cessation of stimulation (arthrokinetic after-nystagmus). The existence of an arthrokinetic circularvection and nystagmus indicates a convergence of vestibular and somatosensory afferents from joint receptors. It is concluded that information about joint movements plays an important role within the multisensory processes of self-motion perception.

Adult↗

Judgment and control of velocity in rapid voluntary movements.

Control of velocity in rapid flexion movements of the interphalangeal joint of the thumb was investigated by examining movement trajectories and patterns of activity in the extensor pollicis longus (EPL) and flexor pollicis longus (FPL) muscles. Although velocity was controlled with considerable accuracy, it was not sensed with the same precision. Consistent errors were made when subjects attempted to match the peak velocities under conditions in which the relationship between muscle activity and joint acceleration had been altered, i.e. changing the angle from which movement was initiated or varying the load. Rather than relying on afferent feedback from peripheral sensory receptors for information about velocity during rapid movements, it is suggested that subjects were more likely to base their judgment of velocity on sensations evoked by the voluntary motor command.

Adult↗

Arm movement performance during reversible basal ganglia lesions in the monkey.

Arm motor performance of eight Cebus monkeys was examined during reversible cooling in the ventral lateral region of the putamen and globus pallidus (primarily the external segment), where neurons discharging during arm movements have been found (DeLong 1972). When attempting to hold a handle stationary during basal ganglia cooling, all monkeys developed flexion at the wrist and some developed a slow flexion drift of the arm at the elbow. The prominence of wrist flexion emphasizes that the basal ganglia may normally influence distal musculature. During basal ganglia cooling an increase in segmental stretch reflexes (15-30 ms) was sometimes observed following arm perturbations, but no consistent increase occurred in the later EMG responses (30-95 ms) in contrast to results obtained in Parkinsonian patients (Tatton and Lee 1975). No major changes were observed in the time of onset of the earliest EMG activity in the agonist muscle in a simple reaction time elbow movement task during basal ganglia cooling. Basal ganglia lesions produced major disorders in both flexion and extension movements including slowing of movements and rebound of the arm towards its initial position after onset of movement. These disorders were accompanied by an increase in tonic activity of both flexors and extensors while holding and by increased levels of cocontraction of agonists and antagonists during attempted movements. It is suggested that this basal ganglia disorder is due to a failure to achieve the correct balance of activity between agonists and antagonists that is appropriate for a particular motor act.

Animals↗

The placing reaction in the standing cat: a model for the study of posture and movement.

By measuring the forces applied by each limb supporting the weight of the standing quadruped (cat), before and during elicitation of the placing reaction, it was possible to examine quantitatively and qualitatively the postural events which preceded and accompanied forelimb displacement. The findings are summarized as follows: 1. Postural adjustment consists of a shift from quadrupedal stance to a tripodal stance to permit withdrawal of weight from one forelimb without loss of equilibrium. The animal's weight is not equally distributed between the three supporting limbs but the majority of the weight is supported by the diagonally opposing limb pair. 2. During the isometric phase of the placing reaction, the animal's projected center of gravity moves contralaterally, across the diagonal line between the contralateral forepaw and the ipsilateral hindpaw, and comes to rest within the triangular zone outlined by the three supporting limbs. 3. The diagonal supporting stance is a maneuver of an anticipatory nature which precedes and accompanies the placing reaction. 4. The force changes exhibited by each limb to bring the animal to the stereotyped diagonal supporting stance illustrated that the way to achieve this is consistent within a given animal, but differs from one animal to another. The pattern in the same animal is generally symmetrical when lifting the right or left forepaw. 5. The data from the cat are compared to observations in other quadrupeds and man.

Animals↗

European vestibular experiments on the Spacelab-1 mission: 4. Thresholds of perception of whole-body linear oscillation.

Thresholds for the detection of linear oscillatory motion at 0.3 Hz in the X, Y and Z body axes were determined during the flight of Spacelab-1 and on the ground pre- and post-flight, using the method of limits with a single staircase procedure. Pre-flight, Z axis thresholds (mean 0.077 ms-2) were significantly higher than X and Y thresholds (mean 0.029 ms-2). Measures obtained on three crew members in-flight exhibited thresholds greater, by a factor of 1.5-4.3, than those obtained pre-flight. Post-flight, two crew members had significantly elevated X and Y axis thresholds whereas the other two crew members had lowered thresholds in X, Y and Z axes. In general, thresholds had returned to pre-flight levels by the second post-flight day. A possible explanation for these somewhat disparate responses is presented.

Acceleration↗

M.I.T./Canadian vestibular experiments on the Spacelab-1 mission: 2. Visual vestibular tilt interaction in weightlessness.

Adaptation to weightlessness includes the substitution of other sensory signals for the no longer appropriate graviceptor information concerning static spatial orientation. Visual-vestibular interaction producing roll circularvection was studied in weightlessness to assess the influence of otolith cues on spatial orientation. Preliminary results from four subjects tested on Spacelab-1 indicate that visual orientation effects were stronger in weightlessness than pre-flight. The rod and frame test of visual field dependence showed a weak post-flight increase in visual influence. Localized tactile cues applied to the feet in space reduced subjective vection strength.

Adaptation, Physiological↗

M.I.T./Canadian vestibular experiments on the Spacelab-1 mission: 6. Vestibular reactions to lateral acceleration following ten days of weightlessness.

Tests of otolith function were performed pre-flight and post-flight on the science crew of the first Spacelab Mission with a rail-mounted linear acceleration sled. Four tests were performed using horizontal lateral (y-axis) acceleration: perception of linear motion, a closed loop nulling task, dynamic ocular torsion, and lateral eye deviations. The motion perception test measured the time to detect the onset and direction of near threshold accelerations. Post-flight measures of threshold and velocity constant obtained during the days immediately following the mission showed no consistent pattern of change among the four crewmen compared to their pre-flight baseline other than an increased variability of response. In the closed loop nulling task, crewmen controlled the motion of the sled and attempted to null a computer-generated random disturbance motion. When performed in the light, no difference in ability was noted between pre-flight and post-flight. In the dark, however, two of the four crewmen exhibited somewhat enhanced performance post-flight. Dynamic ocular torsion was measured in response to sinusoidal lateral acceleration which produces a gravitionertial stimulus equivalent to lateral head tilt without rotational movement of the head. Results available for two crewmen suggest a decreased amplitude of sinusoidal ocular torsion when measured on the day of landing (R+0) and an increasing amplitude when measured during the week following the mission.

Acceleration↗

Vestibulo-spinal response modification as determined with the H-reflex during the Spacelab-1 flight.

Our laboratory at the Johnson Space Center has employed the H-reflex recorded from the soleus muscle as a method of monosynaptic reflex testing in conjunction with vertical linear acceleration to assess modification of utriculo-saccular function induced through prolonged exposure to microgravity. It was hypothesized that exposure to free fall would reduce the necessity for postural reflexes in the major leg muscles, and that postural modification would reflect a change, not in the peripheral vestibular organs, but more centrally. This postural adjustment would reflect a sensory motor rearrangement where otolith receptor input was reinterpreted to provide an environmentally appropriate response. In addition to the H-reflex (which was the only inflight measurement), vestibulo-spinal EMG from the gastrocnemius, and self-motion reports were obtained in response to a sudden earth vertical fall. Preflight, inflight and postflight motion sickness reports were also recorded, and related to the H-reflex data. The results indicated that early inflight H-reflex amplitude was similar to that recorded preflight, but that measurements obtained later in the flight (day seven) did not show a change in potentiation as a function of the different drop to shock intervals. Immediate postflight H-reflex response in three of the four astronauts tested showed a rebound effect. Postflight gastrocnemius EMG in response to the sudden fall did not show a significant change from preflight values. However, one crewman who was tested early postflight did show an increase in EMG activity in response to the sudden fall. This immediate postflight effect returned to baseline rapidly. Self-motion perception obtained inflight suggested that the early inflight drops were perceived like those preflight. Drops later inflight were described as sudden, fast, hard and translational in nature. Immediately postflight the drops were perceived like those late inflight, and the astronauts said that they did not feel as though they were falling, rather the floor came up to meet them. Post hoc peak H-reflex amplitude, both preflight and postflight was related to inflight space motion sickness.

Humans↗

Visual influence on postural control in the cat.

The influence of horizontal optokinetic stimulation on posture and postural readjustments, induced by horizontal rotation of a turntable, were studied in the cat. Optokinetic stimulations at constant velocities lead to modifications of posture depending on the velocity of the stimulus. However, habituation as well as interindividual variability of these postural responses make difficult a systematic and quantitative approach to the phenomenon. Optokinetic stimulations at sinusoidal velocities induced reproductible postural responses, whose phase and gain were studied at different velocities and frequencies of stimulation. At low frequencies (from 0.05 Hz to 0.2 Hz) the postural responses tend to lead the position of the optokinetic stimulus while a lag appears at higher frequencies (up to 1 Hz). In these conditions the gain increases and seems to depend on the performances of the simultaneously elicited oculomotor response. Induced postural readjustments are also modulated by the relative velocity of the visual stimulation with respect to the cat. A given visual input is more effective on an induced postural readjustment than on the posture of a static animal, especially at low frequencies (from 0.05 Hz to 0.3 Hz). These data extend to the cat the strong visual component of the postural control system previously described in other species.

Animals↗

Visual and vestibular contributions to prelanding EMG during jump-downs in cats.

Prelanding EMG responses in elbow flexors and extensors were assessed during landing from jump-downs (0.6, 0.8, and 1.0 m) in normal blindfolded cats and labyrinthectomized cats with and without vision occluded. Jump-down conditions determined the strategy of response elicited in the normal cat. When the height could be anticipated by the blindfolded animals, a response typical of a jump in the presence of visual cues occurred; extensor activity began an average of 73 +/- 12 ms before landing, while flexor activity was minimal. When the animal was 'tricked' by an unexpected change in jump height, it displayed a pattern of EMG activity appropriate for the jump height just previously experienced, not for the actual height. If the jump height was uncertain, the cat commonly exhibited continuous extensor activity that began soon (100-150 ms) after both forepaws left the platform. In the presence of visual cues, labyrinthectomized cats were able to execute jump-downs at 0.6 m. Onset of extensor EMG activity was normal during the first postoperative jumps, although the typical two-burst pattern was absent, and average prelanding extensor IEMG was less than that of the control jumps. In addition, landing was usually awkward, as the forelimbs collapsed and the ventral surface of the trunk contacted the landing pad. During subsequent sessions, the two-burst pattern reappeared, average prelanding extensor IEMG increased, and flight position improved, so that landing occurred without the forelimbs collapsing. Without visual cues, the labyrinthectomized cats were unable to execute a jump-down. These results suggest that visual input may normally regulate timing of the extensor prelanding motor program; however, without visual input, prelanding responses can be preprogrammed. When visual input is present, vestibular input during the flight phase may be primarily manifested as gain in extensor activity rather than in the temporal sequencing. When visual input is absent and jump height is uncertain, vestibular input may become more influential in determining the pattern of prelanding activity.

Animals↗

Effects of early visual and complex stimulation on learning, brain biochemistry, and electrophysiology.

A complex stimulation regimen (visual, auditory, and somesthetic-kinesthetic with forced movements, 30 times for 30 min each within 14 days) increased significantly the amplitudes of visual cortical evoked potentials (EPs) in adult rats if applied during the second postnatal fortnight. The EP increase after stimulation during the first 14 days after birth was not significant. Visual stimulation alone was compared with complex stimulation (visual plus forced movements) during the 2nd postnatal fortnight. More specific local changes in the visual cortex were revealed in brain biochemistry (lower DNA concentration, more RNA and protein per cell) and cortical electrogenesis (enhanced visual EPs) after visual stimulation alone, whereas complex stimulation induced more diffuse changes and rather profoundly influenced higher nervous functions (viz., memory retrieval - improved 24-h). Involvement of both specific and nonspecific mechanisms in the aftereffects of early stimulation is indicated.

Animals↗

Sigma-movement and optokinetic nystagmus elicited by stroboscopically illuminated stereopatterns.

Sigma-movement is an apparent movement seen when a stationary periodic visual pattern of the period PS is illuminated stroboscopically at the flash frequency fS and smooth gaze pursuit eye movements are performed across the pattern at an angular velocity Ve = PS X fS deg X S-1. Sigma-movement leads to an optokinetic nystagmus (Sigma OKN) which in turn sustains Sigma-movement perception. (1) Sigma-movement was also seen in an apparent three-dimensional periodic stripe pattern generated by two periodic monocular stimulus patterns with a certain degree of horizontal binocular disparity. (2) Sigma-movement perception and Sigma-OKN were also elicited by a stroboscopically illuminated, stationary, random dot stereostripe pattern. The periodicity PS of this pattern is generated on the cyclopean retina (Julesz 1971). The equation described above was also valid. When the time delay delta t between left eye and right eye flashes was varied, the apparent depth of the random dot stereostripe pattern decreased with increasing delta t, but the Sigma-effects were not affected. (3) Sigma-movement illusion and Sigma-pursuit movements can also be induced when real three-dimensional objects composed of periodic components are stroboscopically illuminated and adequate gaze or eye pursuit movements are induced. Sigma-movement is related to gaze movement and is therefore elicitable by eye, head or body movements. (4) Sigma-movement is presumably caused by the interaction of efference copy signals (generated in a cortical gaze pursuit system) and afferent visual signals. The present data indicate that neuronal mechanisms for this interaction are located--at least in part--at or beyond the level of binocular fusion and stereopsis.

Adult↗

Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography.

The characteristics of vibration-induced illusory joint movements were studied in healthy human subjects. Unseen by the subject, constant frequency vibration trains applied to the distal tendon of the Triceps or Biceps induced an almost constant velocity illusory movement of the elbow whose direction corresponded to that of a joint rotation stretching the vibrated muscle. Vibration trains of the same duration and frequency applied alternatively to the Biceps and Triceps evoked alternating flexion-extension illusory movements. During successive application of vibration trains at frequencies from 10 to 120 Hz, the perceived velocity of the illustory movements increased progressively from 10 to 70-80 Hz, then decreased from 80 to 120 Hz. The maximal perceived velocity was three times higher during alternating vibration of the Biceps and Triceps than during single muscle stimulation. Unit activity from 15 muscle spindle primary endings and five secondary endings located in Tibialis anterior and Extensor digitorum longus muscles were recorded using microneurography in order to study their responses to tendon vibration and passive and active movements of the ankle. Primary endings were all activated by low amplitude tendon vibration (0.2-0.5 mm) previously used to induce illusory movements of the elbow. The discharge of some was phase-locked with the vibration cycle up to 120 Hz, while others responded one-to-one to the vibration cycle up to 30-50 Hz, then fired in a sub-harmonic manner at higher frequencies. Secondary endings were much less sensitive to low amplitude tendon vibration. Primary and secondary ending responses to ramp and sinusoidal movements of the ankle joint were compared. During the movement, the primary ending discharge frequency was almost constant, while the secondary ending activity progressively increased. During ankle movements the primary ending discharge appeared mainly related to velocity, while some secondary activities seemed related to both movement velocity and joint angle position. Muscle spindle sensory ending responses to active and passive ankle movements stretching the receptor-bearing muscle (plantar flexion) were qualitatively and quantitatively similar. During passive reverse movements (dorsiflexion) most of the sensory endings stopped firing when their muscle shortened. Active muscle shortening (isotonic contraction) modulated differently the muscle spindle sensory ending discharge, which could stop completely, decrease or some times increase during active ankle dorsiflexion. During isometric contraction most of the muscle spindle sensory endings were activated. The characteristics of the vibration-induced illusory movements and the muscle spindle responses to tendon vibration and to active and passive joint movements strengthened the possibility of the contribution of primary endings to kinesthesia, as suggested by several previous works...

Adolescent↗

Perceptual and motor effects of agonist-antagonist muscle vibration in man.

Perceptual and motor effects of vibration applied simultaneously to the distal tendons of the Biceps and Triceps muscles, in isometric conditions and without sight of the stimulated arm, have been studied in human volunteers. Motor effects, measured by surface EMG, are inexistent when the flexor and extensor muscles are simultaneously vibrated at the same frequency. However, EMG activity appears in the muscle being vibrated at the lower frequency when simultaneous vibration is applied at different frequencies. The sensations felt by the subjects were reproduced by the nonvibrated arm and recorded by a goniometer. The studies show that the velocity and the amplitude of the ilusory movement is related to the difference in vibration frequency applied to the two muscles. The direction of movement felt (flexion or extension) is that produced by shortening of the muscle being vibrated at the lower frequency. When the two vibration frequencies are the same, there is either no sensation of movement, or a sensation of very slow movement. These results support the notion that the sensation of movement at a joint may be derived from a central processing of the proprioceptive inflow data obtained from flexor and extensor muscles. This interpretation may also be valid for the results obtained earlier by vibration of a single muscle. Furthermore, it is coherent with data on spindle afferent fibres obtained by microneurography in man during passive or active movements.

Adult↗

Purkinje cell activity in the primate flocculus during optokinetic stimulation, smooth pursuit eye movements and VOR-suppression.

Purkinje cell (PC) activity in the flocculus of trained monkeys was recorded during: 1) Vestibular stimulation in darkness. 2) Suppression of the vestibulo-ocular reflex (VOR-supp) by fixation of a small light spot stationary with respect to the monkey. 3) Visual-vestibular conflict (i.e. the visual surround moves together with the monkey during vestibular stimulation), which leads to attenuation or suppression of vestibular nystagmus. 4) Smooth pursuit eye movements. 5) Optokinetic nystagmus (OKN). 6) Suppression of nystagmus during optokinetic stimulation (OKN-supp) by fixation of a small light spot; whereby stimulus velocity corresponds then to image slip velocity. Results were obtained from PCs, which were activated with VOR-supp during rotation to the ipsilateral side. The same PCs were also modulated during smooth pursuit and visual-vestibular conflict. No tonic modulation during constant velocity OKN occurred with slow-phase nystagmus velocities below 40-60 deg/s. Tonic responses were only seen at higher nystagmus velocities. Transient activity changes appeared at the beginning and end of optokinetic stimulation. PCs were not modulated by image slip velocity during OKN-supp. The results show that in primates the same population of floccular PCs is involved in different mechanisms of visual-vestibular interaction and that smooth pursuit and certain components of OKN slow-phase velocity share the same neural pathway. It is argued that the activity of these neurons can neither be related strictly to gaze, eye or image slip velocity; instead, their activity pattern can be best interpreted by assuming a modulation, which is complementary to that of central vestibular neurons of the vestibular nuclei, in the control of slow eye movements.

Animals↗