Self-Motion Misperception Induced by Neck Muscle Fatigue

The effect of neck muscle fatigue induced by prolonged isometric contraction of the neck extensor muscles on self-motion perception was studied. The magnitude of self-motion perception was assessed by evaluating the tracking of a remembered earth-fixed visual target during passive symmetric and asymmetric sinusoidal horizontal body rotation. The trunk was rotated on a stationary head for examining the role of neck proprioception and the whole-body for that of the vestibular system. To induce neck extensor muscle fatigue, participants held their head extended against a load for several minutes. Perceptual responses were examined before and during neck muscle fatigue. It was found that the perception of the movement was diminished by neck muscle fatigue as shown by a reduction of the amplitude of the tracking during trunk rotation. This suggests that fatigue affects the motion perception when the neck proprioceptive system was activated by the rotation. This effect has been observed only during slow rotation, while the responses remained unmodified during fast rotation. In contrast, neck muscle fatigue did not affect the tracking when rotation activated only the vestibular system. Furthermore, neck muscle fatigue abolished the effect of tonic head deviation on perceptual responses to whole-body rotation. Therefore, neck muscle fatigue alters the self-motion perception reducing the ability of the proprioceptive system to signal slow trunk rotations and the position of the head relative to the trunk during body movements.

Asymmetrical sinusoidal whole-body rotation sequences with half-cycles at different velocities induce self-motion misperception. This is due to an adaptive process of the vestibular system that progressively reduces the perception of slow motion and increases that of fast motion. It was found that perceptual responses were conditioned by four previous cycles of asymmetric rotation in the dark, as the perception of self-motion during slow and fast rotations remained altered for several minutes. Surprisingly, this conditioned misperception remained even when asymmetric stimulation was performed in the light, a state in which vision completely cancels out the perceptual error. This suggests that vision is unable to cancel the misadaptation in the vestibular system but corrects it downstream in the central perceptual processing. Interestingly, the internal vestibular perceptual misperception can be cancelled by a sequence of asymmetric rotations with fast/slow half-cycles in a direction opposite to that of the conditioning asymmetric rotations.

The vestibular signal of head motion in space must be complemented by a neck signal of the trunk-to-head excursion in order to provide the individual with information on trunk motion in space. This consideration led us to study psychophysically the role of vestibular-neck interaction for human self-motion perception. Subjects (Ss) were presented with passive horizontal rotations of their trunk and/or head (sinusoidal rotations, f = 0.025 - 0.4 Hz) in the dark for vestibular and neck stimulation, as well as for combinations of both. Ss' perception was evaluated in terms of gain (veridical perception of stimulus magnitude, G = 1), phase, and detection threshold. (1) Perception of trunk rotation in space. During vestibular stimulation (whole-body rotation) and neck stimulation (trunk rotation with the head kept stationary) the frequency-transfer characteristics underlying this perception were very similar. The gain fell short; it was only about 0.7 at 0.4 and 0.2 Hz stimulus frequency and was further attenuated with decreasing frequency. In contrast, the phase was close to that of actual trunk position. The gain attenuation was found to be a function of the peak angular velocity of the stimulus, a fact, which we related to a 'velocity threshold' of the order of 1 deg/s. During the various vestibular-neck combinations used, Ss' perception was again erroneous, reflecting essentially the sum of its two non-ideal constituents. However, there was one noticeable exception; during the combination 'head rotation on stationary trunk', Ss veridically perceived their trunk as stationary (compatible with the notion that the sum yielded 'zero'). (2) Perception of head rotation in space. During vestibular stimulation, Ss' estimates showed the same non-ideal gain-vs.-frequency characteristics as described above for the trunk. Neck stimulation induced an illusion as if the head had been rotated in space. This neck contribution was such that, when it was combined with its vestibular counterpart during head rotation on stationary trunk, the perception became almost veridical. On closer inspection, however, this neck contribution was found to reflect the sum of two components; one was the non-ideal neck signal contributing to the perception of 'trunk in space', the other was an almost ideal neck signal of head-on-trunk rotation. (3) The results could be described by a simple model. In this model, the erroneous vestibular signal 'head in space' is primarily used to create an internal representation of 'trunk in space'.(ABSTRACT TRUNCATED AT 400 WORDS)

A recent study has shown that fatigue of the posterior neck muscles, induced by prolonged isometric contractions, causes self-motion misperception. The present study investigates whether focal vibration of the posterior neck muscles can prevent or abolish it. Self-motion perception was assessed by analyzing the tracking of a ground-fixed visual target during passive sinusoidal horizontal trunk rotation, both symmetric and asymmetric, with a stationary head. After prolonged isometric contractions that induced posterior neck muscle fatigue, perceptual responses to symmetric sinusoidal trunk rotation showed a decrease in gain at lower rotation velocities, and an increase in the final position error (FPE). The changes in gain and FPE were completely prevented by prior high-frequency vibration (100Hz for 3min) of the posterior neck muscles, whereas they were eliminated when the vibration was applied after the fatigue-induced deficit had already occurred. We suggest that the focal vibration activating the neck muscle proprioception may inhibit fatigue signals, possibly through a gate control mechanism. Furthermore, the persistence of the vibratory effects was examined by testing the perceptual gain and the FPE after prolonged vibratory application (three separate sessions of ten minutes each, at 1min rest intervals). It was found that the effects of fatigue on the FPE was eliminated even one week after vibration. This finding suggests that the focal vibratory procedure may be useful to attenuate the impact of fatigue on self-motion perception, potentially preventing deterioration of balance and orientation abilities.

A recent study has shown that fatigue of the posterior neck muscles, induced by prolonged isometric contractions, causes self-motion misperception. The present study investigates whether focal vibration of the posterior neck muscles can prevent it. Self-motion perception was assessed by analyzing the tracking of a ground-fixed visual target during passive sinusoidal horizontal trunk rotation, both symmetric and asymmetric, with a stationary head. After prolonged isometric contractions that induced posterior neck muscle fatigue, perceptual responses to symmetric sinusoidal trunk rotation showed a decrease in gain at lower rotation velocities, and an increase in the final position error (FPE). The changes in gain and FPE were completely prevented by prior high-frequency vibration (100 Hz for 3 minutes) of the posterior neck muscles, whereas they were eliminated when the vibration was applied after the fatigue-induced deficit had already occurred. We suggest that the focal vibration activating the neck muscle proprioception may inhibit fatigue signals, possibly through a gate control mechanism. Furthermore, the persistence of the vibratory effects was examined by testing the perceptual gain and the FPE after prolonged vibratory application (three separate sessions of ten minutes each). It was found that the effects of fatigue on the FPE was eliminated even one week after vibration. This finding suggests that the focal vibratory procedure may be useful to attenuate the impact of fatigue on self-motion perception, potentially preventing deterioration of balance and orientation abilities.

It is still an enigma how human subjects combine visual and vestibular inputs for their self-motion perception. Visual cues have the benefit of high spatial resolution but entail the danger of self motion illusions. We performed psychophysical experiments (verbal estimates as well as pointer indications of perceived self-motion in space) in normal subjects (Ns) and patients with loss of vestibular function (Ps). Subjects were presented with horizontal sinusoidal rotations of an optokinetic pattern (OKP) alone (visual stimulus; 0.025-3.2 Hz; displacement amplitude, 8 degrees) or in combinations with rotations of a Bárány chair (vestibular stimulus; 0.025-0.4 Hz; +/- 8 degrees). We found that specific instructions to the subjects created different perceptual states in which their self-motion perception essentially reflected three processing steps during pure visual stimulation: i) When Ns were primed by a procedure based on induced motion and then they estimated perceived self-rotation upon pure optokinetic stimulation (circular vection, CV), the CV has a gain close to unity up to frequencies of almost 0.8 Hz, followed by a sharp decrease at higher frequencies (i.e., characteristics resembling those of the optokinetic reflex, OKR, and of smooth pursuit, SP). ii) When Ns were instructed to "stare through" the optokinetic pattern, CV was absent at high frequency, but increasingly developed as frequency was decreased below 0.1 Hz. iii) When Ns "looked at" the optokinetic pattern (accurately tracked it with their eyes) CV was usually absent, even at low frequency. CV in Ps showed similar dynamics as in Ns in condition i), independently of the instruction. During vestibular stimulation, self-motion perception in Ns fell from a maximum at 0.4 Hz to zero at 0.025 Hz. When vestibular stimulation was combined with visual stimulation while Ns "stared through" OKP, perception at low frequencies became modulated in magnitude. When Ns "looked" at OKP, this modulation was reduced, apart from the synergistic stimulus combination (OKP stationary) where magnitude was similar as during "staring". The obtained gain and phase curves of the perception were incompatible with linear systems prediction. We therefore describe the present findings by a non-linear dynamic model in which the visual input is processed in three steps: i) It shows dynamics similar to those of OKR and SP; ii) it is shaped to complement the vestibular dynamics and is fused with a vestibular signal by linear summation; and iii) it can be suppressed by a visual-vestibular conflict mechanism when the visual scene is moving in space. Finally, an important element of the model is a velocity threshold of about 1.2 degrees/s which is instrumental in maintaining perceptual stability and in explaining the observed dynamics of perception. We conclude from the experimental and theoretical evidence that self-motion perception normally is related to the visual scene as a reference, while the vestibular input is used to check the kinematic state of the scene; if the scene appears to move, the visual signal becomes suppressed and perception is based on the vestibular cue.

Chronic loss of vestibular function modifies the role of neck afferents in human perception of self-motion. We characterized this change by comparing the self-motion perception of patients with chronic vestibular loss (Ps) to that of normal subjects (Ns). Stimuli consisted of sinusoidal horizontal rotations (0.025-0.4 Hz) of the trunk relative to the head (neck stimulation) and/or of the head in space (vestibular stimulation). Perception of head rotation relative to the trunk, of trunk rotation in space, or of head rotation in space was assessed in terms of gain and phase (veridical perception, G = 1 and phi = 0 degree) as well as detection threshold using a pointing procedure. (1) Perception of head rotation relative to the trunk (neck proprioception). Ps' detection threshold of head-to-trunk rotation was normal (i.e. similar to that of Ns) across all frequencies tested. Also, with peak angular velocities above 5 degrees/s, the gain of their perception was approximately normal. When peak velocity was decreased below this value, however, either by lowering stimulus frequency with peak displacement kept constant (+/- 8 degrees) or by decreasing peak displacement at constant frequency (0.05 Hz), the gain increased above unity, unlike in Ns. In contrast, the phase remained normal (approximately 0 degree). (2) Perception of trunk rotation in space. Ps perceived their trunks as stationary during neck stimulation and all vestibular-neck combinations at medium to low frequencies. At 0.4 Hz, however, Ps consistently perceived the trunk rotation, conceivably due to somatosensory self-motion cues arising from high body acceleration. In contrast, Ns perceive a trunk-in-space rotation with the neck stimulation and most of the stimulus combinations across the whole frequency range tested. Ns perceived their trunks as stationary only during head rotation on the stationary trunk (presumed to reflect a mutual cancellation of neck and vestibular signals). (3) Perception of head rotation in space. In Ps, unlike Ns, this perception always resembled that of head rotation relative to the trunk. (4) When Ps were presented with a visual or somatosensory space reference (not motion cues), their perception of trunk and head rotation in space became approximately normal. (5) We suggest that there are basically two changes in the neck-induced self-motion perception associated with chronic vestibular loss. First, neck proprioception shows a non-linear gain that overemphasizes low stimulus velocities, for unknown reasons.(ABSTRACT TRUNCATED AT 400 WORDS)

This study aimed to test the role of the otolithic system in self-motion perception by examining adaptive responses to asymmetric off-axis vertical rotation. Self-movement perception was examined after a conditioning procedure consisting of prolonged asymmetric sinusoidal yaw rotation of the head on a stationary body with hemicycle faster than the other hemicycle. This asymmetric velocity rotation results in a cumulative error in spatial self-motion perception in the upright position that persists over time. Head yaw rotation conditioning was performed in different head positions: in the upright position to activate semicircular canals and in the supine and prone positions to activate both semicircular canals and otoliths with the phase of otolithic stimulation reversed with respect to activation of the semicircular canals. The asymmetric conditioning influenced the cumulative error induced by four asymmetric cycles of whole-body vertical axis yaw rotation. The magnitude of this error depended on the orientation of the head during the conditioning. The error increased by 50% after upright position conditioning, by 100% in the supine position, and decreased by 30% in the prone position. The enhancement and reduction of the perceptual error are attributed to otolithic modulation because of gravity influence of the otoliths during the conditioning procedure in supine and prone positions. These findings indicate that asymmetric velocity otolithic activation induces adaptive perceptual errors such as those induced by semicircular canals alone, and this adaptation may be useful in testing dynamic otolithic perceptual responses under different conditions of vestibular dysfunction.

Convergence of vestibular and proprioceptive signals in the cerebellar nodulus/uvula enhances the encoding of self-motion in primates.

Self-motion perception was studied in patients with unilateral vestibular lesions (UVL) due to acute vestibular neuritis at 1 wk and 4, 8, and 12 mo after the acute episode. We assessed vestibularly mediated self-motion perception by measuring the error in reproducing the position of a remembered visual target at the end of four cycles of asymmetric whole-body rotation. The oscillatory stimulus consists of a slow (0.09 Hz) and a fast (0.38 Hz) half cycle. A large error was present in UVL patients when the slow half cycle was delivered toward the lesion side, but minimal toward the healthy side. This asymmetry diminished over time, but it remained abnormally large at 12 mo. In contrast, vestibulo-ocular reflex responses showed a large direction-dependent error only initially, then they normalized. Normalization also occurred for conventional reflex vestibular measures (caloric tests, subjective visual vertical, and head shaking nystagmus) and for perceptual function during symmetric rotation. Vestibular-related handicap, measured with the Dizziness Handicap Inventory (DHI) at 12 mo correlated with self-motion perception asymmetry but not with abnormalities in vestibulo-ocular function. We conclude that 1) a persistent self-motion perceptual bias is revealed by asymmetric rotation in UVLs despite vestibulo-ocular function becoming symmetric over time, 2) this dissociation is caused by differential perceptual-reflex adaptation to high- and low-frequency rotations when these are combined as with our asymmetric stimulus, 3) the findings imply differential central compensation for vestibuloperceptual and vestibulo-ocular reflex functions, and 4) self-motion perception disruption may mediate long-term vestibular-related handicap in UVL patients.NEW & NOTEWORTHY A novel vestibular stimulus, combining asymmetric slow and fast sinusoidal half cycles, revealed persistent vestibuloperceptual dysfunction in unilateral vestibular lesion (UVL) patients. The compensation of motion perception after UVL was slower than that of vestibulo-ocular reflex. Perceptual but not vestibulo-ocular reflex deficits correlated with dizziness-related handicap.

Vestibular functions are known to show some deterioration with age. Vestibular deterioration is often thought to be compensated for by an increase in neck proprioceptive gain. We studied this presumed compensatory mechanism by measuring psychophysical responses to vestibular (horizontal canal), neck and combined stimuli in 50 healthy human subjects as a function of age (range 15-76 years). After passive horizontal rotations of head and/or trunk (torso) in complete darkness (dominant frequencies 0.05, 0.1, and 0.4 Hz), subjects readjusted a visual target to its remembered prerotational location in space. (1) Vestibular-only stimulus(whole-body rotation); subjects' responses were shifted towards postrotatory body position, this only slightly at 0.4 Hz and pronounced at 0.1 and 0.05 Hz. These errors reflect the known physiological drop of vestibular gain at low rotational frequency. They exhibited a slight but significant increase with age. (2) Neck-only stimulus(trunk rotated, head stationary); the responses showed errors similar to those upon vestibular stimulation (with offset towards postrotatory trunk position) and this again slightly more with increasing age. (3) Vestibular-neck stimulus combinationduring head rotation on stationary trunk; the errors were close to zero, independent of stimulus frequency and the subjects' age. (4) Opposite stimulus combination(trunk rotated in the same direction as the head, but with double amplitude); the errors were clearly enhanced, essentially reflecting the sum of those with vestibular-only and neck-only stimulation. Taken together, we find a parallel increase in neck- and vestibular-related errors with age, in seeming contrast to previous studies. We explain our and the previous findings by a vestibular-neck interaction model in which two different neck signals are involved. One neck signal is used, in combination with the vestibular signal, for estimating trunk-in-space rotation. It is internally shaped to always match the vestibular signal, so that these two signals cancel each other out when summed during head rotation on stationary trunk. Because of this matching, perceived trunk stationariness during head rotation on the stationary trunk is independent of vestibular deterioration (related to stimulus frequency, age, ototoxic medication, etc.). The other neck proprioceptive signal, coding head-on-trunk rotation, is superimposed on the estimate of trunk-in-space rotation, thereby yielding a notion of head-in-space. This neck signal remains essentially unchanged with vestibular deterioration. Generally, we hold that the transformation of the vestibular signal from the head down to the trunk proceeds further to include the hip and the legs as well as the haptically perceived body support surface; by this, subjects yield a notion of support kinematics in space. As a consequence, spatial orientation is impaired by chronic vestibular deterioration only to the extent that the body support is moving in space, while it is unimpaired (determined by proprioception alone) during body motion with respect to a stationary support.

Reaching for an object while simultaneously rotating induces Coriolis and centrifugal inertial forces on the arm that require compensatory actions to maintain accuracy. We investigated whether the nervous system uses vestibular signals of head rotation to predict inertial forces. Human subjects reached in darkness to a remembered target 33 cm distant. Subjects were stationary, but experienced a strong vestibular rotation signal. We achieved this by rotating subjects at 360 degrees /s in yaw for 2 min and then stopping, and subjects reached during the 'post-rotary' period when the deceleration is interpreted by the vestibular system as a rotation in the opposite direction. Arm trajectories were straight in control trials without a rotary stimulus. With vestibular stimulation, trajectory curvature increased an average of 3 cm in the direction of the vestibular stimulation (e.g., to the right for a rightward yaw stimulus). Vestibular-induced curvature returned rapidly to normal, with an average time constant of 6 s. Movements also became longer as the vestibular stimulus diminished, and returned towards normal length with an average time constant of 5.6 s. In a second experiment we compared reaching with preferred and non-preferred hands, and found that they were similarly affected by vestibular stimulation. The reach curvatures were in the expected direction if the nervous system anticipated and attempted to counteract the presence of Coriolis forces based on the vestibular signals. Similarly, the shorter reaches may have occurred because the nervous system was attempting to compensate for an expected centrifugal force. Since vestibular stimulation also alters the perceived location of targets, vestibular signals probably influence all stages of the sensorimotor pathway transforming the desired goal of a reach into specific motor-unit innervation.

1. The activity of 113 Y group neurons was recorded extracellularly in 5 alert squirrel monkeys. Sixty-two cells were recorded in naive animals, and 51 cells were recorded after adaptation of the vestibuloocular reflex (VOR) with the use of telescopic lenses. The animals were lying on their right side, so that head rotation was in the vertical (pitch) plane and optokinetic stimulation elicited vertical eye movement. The responses of most cells, as well as the concurrent eye movement, were studied during 1) the VOR, elicited in darkness or in light by sinusoidal head rotation, 2) visual following, elicited by sinusoidal rotation of a full-field optokinetic drum around the stationary animal, and 3) paradigms of visual-vestibular interaction, elicited by combined sinusoidal vestibular and optokinetic stimulation. Stimulation parameters for both head and drum velocity were usually 0.5 Hz, 35 degrees/s peak velocity. 2. Y group cells respond vigorously during visual following and during suppression of the VOR (produced by in-phase rotation of the head and the optokinetic drum); the response is approximately in-phase with eye velocity during visual following, and approximately in-phase with head velocity during suppression of the VOR. During the VOR in darkness, Y cells usually exhibit only slight modulation. The results suggest a linear interaction of visual following and vestibular signals on Y cells during vertical visual-vestibular interaction. Taking into account the excitatory projection of Y cells to superior rectus and inferior oblique motoneurons, a causal role of the Y group in rapid modification of VOR gain during visual-vestibular interaction is suggested. 3. Nine Y neurons from two animals were recorded continuously, for periods ranging from 30 min to 5 h, while the VOR was being adapted to higher or lower gain. Progressive changes of the gain of the VOR in darkness were evident after approximately 30 min from the initiation of head rotation under visual-vestibular mismatch. Consistent changes of the gain and/or phase of the neuronal response during the VOR in darkness were noted in all cases. The phase of the neuronal response gradually approximated head velocity phase during adaptation of the VOR to low gain, increases in the neuronal gain thereafter ensued; the opposite changes were observed during adaptation of the VOR to high gain. 4. Sixteen Y cells were recorded from 1 animal chronically adapted to high VOR gain with the use of magnifying lenses, and 35 cells were recorded from 2 animals chronically adapted to low VOR gain with the use of miniaturizing lenses.(ABSTRACT TRUNCATED AT 400 WORDS)

Human self-motion perception during translatory vestibular and proprioceptive stimulation

Neural Representation of Orientation Relative to Gravity in the Macaque Cerebellum