Patterns of neck muscle activation in cats during reflex and voluntary head movements

Summary When the head rotates, vestibulocollic reflexes counteract the rotation by causing contraction of the neck muscles that pull against the imposed motion. With voluntary head rotations, these same muscles contract and assist the movement of the head. The purpose of this study was to determine if an infinite variety of muscle activation patterns are available to generate a particular head movement, or if the CNS selects a consistent and unique muscle pattern for the same head movement whether performed in a voluntary or reflex mode. The relationship of neck muscle activity to reflex and voluntary head movements was examined by recording intramuscular EMG activity from six neck muscles in three alert cats during sinusoidal head rotations about 24 vertical and horizontal axes. The cats were trained to voluntarily follow a water spout with their heads. Vestibulocollic reflex (VCR) responses were recorded in the same cats by rotating them in an equivalent set of planes with the head stabilized to the trunk so that only the vestibular labyrinths were stimulated. Gain and phase of the EMG responses were calculated, and data analyzed to determine the directions of rotation for which specific muscles produced their greatest EMG output. Each muscle exhibited preferential activation for a unique direction of rotation, and weak responses during rotations orthogonal to that preferred direction. The direction of maximal activation could differ for reflex and voluntary responses. Also, the best excitation of the muscle was not always in the direction that would produce a maximum mechanical advantage for the muscle based on its line of pull. The results of this study suggest that a unique pattern of activity is selected for VCR and tracking responses in any one animal. Patterns for the two behaviors differ, indicating that the CNS can generate movements in the same direction using different muscle patterns.     

Updating visual space during passive and voluntary head-in-space movements

The accuracy of our spatially oriented behaviors largely depends on the precision of monitoring the change in body position with respect to space during self-motion. We investigated observers’ capacity to determine, before and after head rotations about the yaw axis, the position of a memorized earth-fixed visual target positioned 21° laterally. The subjects (n=6) showed small errors (mean=–0.6°) and little variability (mean=0.9°) in determining the position of an extinguished visual-target position when the head (and gaze) remained in a straight-ahead position. This accuracy was preserved when subjects voluntary rotated the head by various magnitudes in the direction of the memorized visual target (head rotations ranged between 5° and 60°). However, when the chair on which the subjects were seated was unexpectedly rotated about the yaw axis in the direction of the target (chair rotations ranged between 6° and 36°) during the head-on-trunk rotations, the performance was markedly decreased, both in terms of spatial precision (mean error=5.6°) and variability (mean=5.7°). A control experiment showed that the prior knowledge of chair rotation occurrence had no effect on the perceived target position after head-trunk movements. Updating an earth-fixed target position during head-on-trunk rotations could be achieved through both cervical and vestibular signals processing, but, in the present experiment, the vestibular output was the only signal that had the potentiality to contribute to accurate coding of the target position after simultaneous head and trunk movements. Our results therefore suggest that the vestibular output is a noisy signal for the central nervous signal to update the visual space during head-in-space motion. Received: 2 June 1997 / Accepted: 16 March 1998     

Vestibuloocular reflex dynamics during high-frequency and high-acceleration rotations of the head on body in rhesus monkey

For frequencies >10 Hz, the vestibuloocular reflex (VOR) has been primarily investigated during passive rotations of the head on the body in humans. These prior studies suggest that eye movements lag head movements, as predicted by a 7-ms delay in the VOR reflex pathways. However, Minor and colleagues recently applied whole-body rotations of frequencies < or =15 Hz in monkeys and found that eye movements were nearly in phase with head motion across all frequencies. The goal of the present study was to determine whether VOR response dynamics actually differ significantly for whole-body versus head-on-body rotations. To address this question, we evaluated the gain and phase of the VOR induced by high-frequency oscillations of the head on the body in monkeys by directly measuring both head and eye movements using the magnetic search coil technique. A torque motor was used to rotate the heads of three Rhesus monkeys over the frequency range 5-25 Hz. Peak head velocity was held constant, first at +/-50 degrees /s and then +/-100 degrees /s. The VOR was found to be essentially compensatory across all frequencies; gains were near unity (1.1 at 5 Hz vs. 1.2 at 25 Hz), and phase lag increased only slightly with frequency (from 2 degrees at 5 Hz to 11 degrees at 25 Hz, a marked contrast to the 63 degrees lag at 25 Hz predicted by a 7-ms VOR latency). Furthermore, VOR response dynamics were comparable in darkness and when viewing a target and did not vary with peak velocity. Although monkeys offered less resistance to the initial cycles of applied head motion, the gain and phase of the VOR did not vary for early versus late cycles, suggesting that an efference copy of the motor command to the neck musculature did not alter VOR response dynamics. In addition, VOR dynamics were also probed by applying transient head perturbations with much greater accelerations (peak acceleration >15,000 degrees /s(2)) than have been previously employed. The VOR latency was between 5 and 6 ms, and mean gain was close to unity for two of the three animals tested. A simple linear model well described the VOR responses elicited by sinusoidal and transient head on body rotations. We conclude that the VOR is compensatory over a wide frequency range in monkeys and has similar response dynamics during passive rotation of the head on body as during passive rotation of the whole body in space.     

Kinetic analysis of arm reaching movements during voluntary and passive rotation of the torso

Reaching movements made to targets during exposure to passive constant velocity rotation show significant endpoint errors. By contrast, reaching movements made during voluntary rotation of the torso are accurate. In both cases, as a consequence of the simultaneous motion of the arm and the torso, Coriolis forces are generated on the arm tending to deflect its path. Our goal in the present paper was to determine whether during voluntary torso rotations arm movement accuracy is preserved by feed forward compensations for self-generated Coriolis forces. To test this hypothesis we analyzed and quantified the contribution of torso rotation and translation to arm dynamics and compared the kinematics and kinetics of pointing movements during voluntary and passive torso rotation. Coriolis torques at the shoulder increase nearly sixfold in voluntary turn and reach movements relative to reaches made without torso rotation, yet are equally accurate. Coriolis torques during voluntary turn and reach movements are more than double those produced by reaching movements during passive body rotation at 60°/s. Nevertheless, the endpoints of the reaches made during voluntary rotation are not deviated, but those of reaches made during passive rotation are deviated in the direction of the Coriolis forces generated during the movements. We conclude that there is anticipatory pre-programmed compensation for self-generated Coriolis forces during voluntary torso rotation contingent on intended torso motion and arm trajectory.     

Stretch reflex modulation during imposed static and dynamic hip movements in standing humans

The purpose of this study was to investigate the effects of hip proprioceptors on soleus stretch reflex excitability in standing humans. A custom-made device to stretch the ankle extensors was mounted on the lower leg portion of a gait orthosis and was used to elicit stretch reflex responses while standing. Six subjects with motor complete spinal cord injury (SCI) and six spinal intact subjects were placed in the orthosis, and stretch reflex responses were elicited when static and/or dynamic hip joint angle changes were imposed. We found that static hip extension significantly enhanced the stretch reflex responses as compared to the neutral position and the hip flexion position only in the SCI group. The EMG magnitude induced by hip extension was 142 ± 16.6% greater than that induced by the neutral position. When the leg was dynamically swung, the reflex responses also changed with the phase of the hip angle in the SCI group; in particular, the reflex amplitude was enhanced with hip extension and in the transition phase from flexion to extension. Although the magnitude of the changes was less than that in the SCI group, a similar type of modulation was found in the normal group. Given the fact that the persons with SCI had lost the neural connection between higher nervous center and the paralyzed lower limb muscles, the mechanism underlying the present results can be attributed to the peripheral afferent input due to the hip angle changes. We concluded that hip mediated afferent input has a significant influence on the excitability modulation of the soleus stretch reflex pathway. Such neural modulation may play a role in the mechanism responsible for the phase-dependent modulation of the stretch reflex while walking.     

Signal processing in the vestibular system during active versus passive head movements

In everyday life, vestibular receptors are activated by both self-generated and externally applied head movements. Traditionally, it has been assumed that the vestibular system reliably encodes head-in-space motion throughout our daily activities and that subsequent processing by upstream cerebellar and cortical pathways is required to transform this information into the reference frames required for voluntary behaviors. However, recent studies have radically changed the way we view the vestibular system. In particular, the results of recent single-unit studies in head-unrestrained monkeys have shown that the vestibular system provides the CNS with more than an estimate of head motion. This review first considers how head-in-space velocity is processed at the level of the vestibular afferents and vestibular nuclei during active versus passive head movements. While vestibular information appears to be similarly processed by vestibular afferents during passive and active motion, it is differentially processed at the level of the vestibular nuclei. For example, one class of neurons in vestibular nuclei, which receives direct inputs from semicircular canal afferents, is substantially less responsive to active head movements than to passively applied head rotations. The projection patterns of these neurons strongly suggest that they are involved in generating head-stabilization responses as well as shaping vestibular information for the computation of spatial orientation. In contrast, a second class of neurons in the vestibular nuclei that mediate the vestibuloocular reflex process vestibular information in a manner that depends principally on the subject's current gaze strategy rather than whether the head movement was self-generated or externally applied. The implications of these results are then discussed in relation to the status of vestibular reflexes (i.e., the vestibuloocular, vestibulocollic, and cervicoocular reflexes) and implications for higher-level processing of vestibular information during active head movements.     

Vestibuloocular reflex inhibition and gaze saccade control characteristics during eye-head orientation in humans

1. In natural conditions, gaze (i.e., eye + head) orientation is a complex behavior involving simultaneously the eye and head motor systems. Thus one of the key problems of gaze control is whether or not the vestibuloocular reflex (VOR) elicited by head rotation and saccadic eye movement linearly add. 2. Kinematics of human gaze saccades within the oculomotor range (OMR) were quantified under different conditions of head motion. Saccades were visually triggered while the head was fixed or passively moving at a constant velocity (200 deg/s) either in the same direction as, or opposite to, the saccade. Active eye-head coordination was also studied in a session in which subjects were trained to actively rotate their head at a nearly constant velocity during the saccade and, in another session, during natural gaze responses. 3. When the head was passively rotated toward the visual target, both maximum and mean gaze velocities increased with respect to control responses with the head fixed; these effects increased with gaze saccade amplitude. In addition, saccade duration was reduced so that corresponding gaze accuracy, although poorer than for control responses, was not dramatically affected by head motion. 4. The same effects on gaze velocity were present during active head motion when a constant head velocity was maintained throughout saccade duration, and gaze saccades were as accurate as with the head fixed. 5. During natural gaze responses, an increased gaze velocity and a decreased saccade duration with respect to control responses became significant only for gaze displacement larger than 30 degrees, due to the negligible contribution of head motion for smaller responses. 6. When the head was passively rotated in the opposite direction to target step, gaze saccades were slower than those obtained with the head fixed; but their average accuracy was still maintained. 7. These results confirm a VOR inhibition during saccadic eye movements within the OMR. This inhibition, present in all 16 subjects studied, ranged from 40 to 96% (for a 40 degree target step) between subjects and increased almost linearly with target step amplitude. Furthermore, the systematic difference between instantaneous VOR gain estimated at the time of maximum gaze velocity and mean VOR gain estimated over the whole saccadic duration indicates a decay of VOR inhibition during the ongoing saccade. 8. A simplified model is proposed with a varying VOR inhibition during the saccade. It suggests that VOR inhibition is not directly controlled by the saccadic pulse generator.(ABSTRACT TRUNCATED AT 400 WORDS)     

Vertical eye position-dependence of the human vestibuloocular reflex during passive and active yaw head rotations.

Vertical eye position-dependence of the human vestibuloocular reflex during passive and active yaw head rotations. The effect of vertical eye-in-head position on the compensatory eye rotation response to passive and active high acceleration yaw head rotations was examined in eight normal human subjects. The stimuli consisted of brief, low amplitude (15-25 degrees ), high acceleration (4,000-6,000 degrees /s2) yaw head rotations with respect to the trunk (peak velocity was 150-350 degrees /s). Eye and head rotations were recorded in three-dimensional space using the magnetic search coil technique. The input-output kinematics of the three-dimensional vestibuloocular reflex (VOR) were assessed by finding the difference between the inverted eye velocity vector and the head velocity vector (both referenced to a head-fixed coordinate system) as a time series. During passive head impulses, the head and eye velocity axes aligned well with each other for the first 47 ms after the onset of the stimulus, regardless of vertical eye-in-head position. After the initial 47-ms period, the degree of alignment of the eye and head velocity axes was modulated by vertical eye-in-head position. When fixation was on a target 20 degrees up, the eye and head velocity axes remained well aligned with each other. However, when fixation was on targets at 0 and 20 degrees down, the eye velocity axis tilted forward relative to the head velocity axis. During active head impulses, the axis tilt became apparent within 5 ms of the onset of the stimulus. When fixation was on a target at 0 degrees, the velocity axes remained well aligned with each other. When fixation was on a target 20 degrees up, the eye velocity axis tilted backward, when fixation was on a target 20 degrees down, the eye velocity axis tilted forward. The findings show that the VOR compensates very well for head motion in the early part of the response to unpredictable high acceleration stimuli-the eye position- dependence of the VOR does not become apparent until 47 ms after the onset of the stimulus. In contrast, the response to active high acceleration stimuli shows eye position-dependence from within 5 ms of the onset of the stimulus. A model using a VOR-Listing's law compromise strategy did not accurately predict the patterns observed in the data, raising questions about how the eye position-dependence of the VOR is generated. We suggest, in view of recent findings, that the phenomenon could arise due to the effects of fibromuscular pulleys on the functional pulling directions of the rectus muscles.     

Reciprocal Ia inhibition during voluntary movements in man

Summary Effects on the H-reflex of the triceps surae muscle from the volleys in the common peroneal nerve were investigated in normal human subjects at rest and during voluntary ankle movements. A depressive effect was revealed during active dorsiflexion but not at rest. Since this depression was evoked by volleys of low-threshold afferents and had a very short latency which suggests a disynaptic linkage, it was regarded as the reciprocal Ia inhibition. In an exceptional case, which showed an H-reflex in pretibial muscles at rest in spite of normal central nervous functions, reciprocal Ia inhibition of the triceps surae as well as pretibial motoneurones was observed in a resting state. It was stressed that there is a close parallelism between the excitability of a group of a-motoneurones and of interneurones which mediate Ia inhibition of the antagonists. Relying on recent observations from animal experiments neuronal mechanisms of the present observation were discussed.     

Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation.

1. Extracellular recordings were obtained from 124 Purkinje cells (P-cells) in the flocculus of alert monkeys. P-cell simple spike-firing rate was analyzed quantitatively during various combinations of smooth-pursuit eye movement and passive head rotation. 2. During sinusoidal smooth eye movements, 80% of the P-cells displayed increased firing rate during ipsilateral and 20% during contralateral eye movement. Over the frequency range 0.3--1.4 Hz, firing-rate modulation was proportional to and in phase with maximum eye velocity. During the steady state of triangle-wave tracking, firing rate increased monotonically as a function of eye velocity. Since firing rate was uncorrelated with retinal-error velocity, one component of P-cell firing rate was related to eye velocity. 3. During the transient phase of triangle-wave tracking, when an instantaneous change in the direction of target movement caused a large retinal-error velocity, 40% of the P-cells were related only to eye velocity. Sixty percent of the P-cells displayed an overshoot or undershoot in firing rate, indicating a relationship to either retinal-error velocity or eye acceleration as well as to eye velocity. 4. During the vestibuloocular reflex (VOR), evoked by head rotation in the dark, P-cell firing rate was only weakly modulated. In contrast, when the monkey suppressed the VOR by fixating a target that rotated with him, P-cell rate was deeply modulated. Since the modulation was proportional to and in phase with maximum head velocity, another component of P-cell firing rate was related to head velocity. 5. Of 36 P-cells tested, 35 displayed firing-rate modulation during both suppression of the VOR and smooth-pursuit eye movement. P-cells that reached peak firing rate during ipsilateral head rotation also reached peak firing rate during ipsilateral smooth eye rotation. Average population sensitivitites to head velocity and eye velocity were equal. In three conditions in which eye and head velocity were elicited simultaneously, P-cell firing rate could be predicted by the linear, vector addition of the separate eye and head velocity components of firing rate. Therefore, the relatively weak modulation of P-cell firing rate during the VOR in the dark can be accounted for by the cancellation of equal but opposite head and eye velocity components. 6. The connections of flocculus P-cells to interneurons in the brain stem VOR pathways have been established in other mammals. In the context of those connections, P-cell firing patterns were appropriate to facilitate the eye movements the monkey was required to make. We conclude that the flocculus is important for sustaining any smooth eye movements that are different from those evoked by head rotation in the dark. The eye velocity component may represent an efference copy signal that sustains ongoing eye velocity during smooth pursuit.     

Two kinematic synergies in voluntary whole-body movements during standing

We used a particular computational approach, the uncontrolled manifold hypothesis, to investigate joint angle covariation patterns during whole-body actions performed by standing persons. We hypothesized that two kinematic synergies accounted for the leg/trunk joint covariation across cycles during a rhythmic whole-body motion to stabilize two performance variables, the trunk orientation in the external space and the horizontal position of the center of mass (COM). Subjects stood on a force plate and performed whole-body rhythmic movements for 45 s under visual feedback on one of the four variables, the position of the center of pressure or the angle in one of the three joints (ankle, knee, or hip). The Fitts-like paradigm was used with two target amplitudes and six indices of difficulty (ID) for each of the four variables. This was done to explore the robustness of kinematic postural synergies. A speed-accuracy trade-off was observed in all feedback conditions such that the movement time scaled with ID and the scaling differed between the two movement amplitudes. Principal-component (PC) analysis showed the existence of a single PC in the joint space that accounted for over 95% of the joint angle variance. Analysis within the uncontrolled manifold hypothesis has shown that data distributions in the joint angle space were compatible with stabilization of both trunk orientation and COM location. We conclude that trunk orientation and the COM location are stabilized by co-varied changes of the major joint angles during whole-body movements. Despite the strong effects of movement amplitude and ID on performance, the structure of the joint variance showed only minor dependence on these task parameters. The two kinematic synergies (co-varied changes in the joint angles that stabilized the COM location and trunk orientation) have proven to be robust over a variety of tasks.     

Influence of long-latency reflex modulation on the performance of quick adjustment movements

The effect of long-latency reflex modulation on the performance of a quick adjustment movement following a muscle stretch was studied in 26 healthy male subjects. When the subjects felt a sudden angle displacement in the direction of a wrist extension they were required to make an adjustment movement by moving a handlebar, held in the hand, to align with a target position as quickly and as accurately as possible. The index of performance (adjustment time) was the time taken to move the handle to the target position from stretch onset. A DC torque motor was used to evoke electromyographic (EMG) reflex responses on a wrist flexor. Averaging of the rectified EMG, recorded from surface electrodes placed over the flexor, showed short- and long-latency reflexes (M1 and M2 components). For all subjects, the amplitudes of the reflex components decreased during the adjustment movement because the target position for this study was fixed to the extension side of the wrist joint. The decrease in the M2 component, which is considered to be a transcortical reflex, was significantly larger than the decrease in the M1 component, which is spinal reflex. The main finding was of a positive correlation between the length of adjustment time and the degree of reduction of M1 and M2 with the adjustment movement (r?=?0.602 for M1, P?r?=?0.850 for M2, P?r?=?0.577, P?r?=?0.603, P?相似文献   

Firing behavior of vestibular neurons during active and passive head movements: vestibulo-spinal and other non-eye-movement related neurons.

The firing behavior of 51 non-eye movement related central vestibular neurons that were sensitive to passive head rotation in the plane of the horizontal semicircular canal was studied in three squirrel monkeys whose heads were free to move in the horizontal plane. Unit sensitivity to active head movements during spontaneous gaze saccades was compared with sensitivity to passive head rotation. Most units (29/35 tested) were activated at monosynaptic latencies following electrical stimulation of the ipsilateral vestibular nerve. Nine were vestibulo-spinal units that were antidromically activated following electrical stimulation of the ventromedial funiculi of the spinal cord at C1. All of the units were less sensitive to active head movements than to passive whole body rotation. In the majority of cells (37/51, 73%), including all nine identified vestibulo-spinal units, the vestibular signals related to active head movements were canceled. The remaining units (n = 14, 27%) were sensitive to active head movements, but their responses were attenuated by 20-75%. Most units were nearly as sensitive to passive head-on-trunk rotation as they were to whole body rotation; this suggests that vestibular signals related to active head movements were cancelled primarily by subtraction of a head movement efference copy signal. The sensitivity of most units to passive whole body rotation was unchanged during gaze saccades. A fundamental feature of sensory processing is the ability to distinguish between self-generated and externally induced sensory events. Our observations suggest that the distinction is made at an early stage of processing in the vestibular system.     

Adjustment of saccade characteristics during head movements

Summary Saccade characteristics have been studied during coordinated eyehead movements in monkeys. Amplitude, duration, and peak velocity of saccades with head turning were compared with saccades executed while the head was artificially restrained. The results indicate that the saccade characteristics are modulated as a function of head movement, hence the gaze movement (eye+head) exactly matches saccades with head fixed. Saccade modulation is achieved by way of negative vestibulo-ocular feedback. The neck proprioceptors, because of their longer latency, are effective only if the head starts moving prior to the onset of saccade. It is concluded that saccades made with head turning are not ballistic movements because their trajectory is not entirely predetermined by a central command.     

Startle reflex modulation during exposure to pleasant and unpleasant odors

The eyeblink component of the startle response to acoustic probes was measured while subjects smelled pleasant odors, unpleasant odors, or no odor. Peak electromyogram (EMG) 20–90 ms after probe onset was greater during unpleasant than during no odor conditions; EMGs for pleasant odors did not differ from those for no odor. Base tension in orbicularis oculi muscles was also higher during unpleasant odors. The results for unpleasant odors parallel those found in previous studies that have used a variety of methods for producing negatively valenced experiences. The results for pleasant odors diverge from those of most previous studies, which have found startle attenuation during positively valenced experiences. However, the results may be compatible with the suggestion (Lang, Bradley, & Cuthbert, 1992) that the motivational state that modulates startle involves both valence and arousal. Pleasant odors may require appropriate contexts to produce the positive motivational state required for startle attenuation.     

Premotor cortex modulates somatosensory cortex during voluntary movements without proprioceptive feedback

Movement perception relies on sensory feedback, but the involvement of efference copies remains unclear. We investigated movements without proprioceptive feedback using ischemic nerve block during fMRI in healthy humans, and found preserved activation of the primary somatosensory cortex. This activation was associated with increased interaction with premotor cortex during voluntary movements, which demonstrates that perception of movements relies in part on predictions of sensory consequences of voluntary movements that are mediated by the premotor cortex.