L. Borel

Sensory strategies in human postural control before and after unilateral vestibular neurotomy

Abstract Vestibular inputs tonically activate the antigravitative leg muscles during normal standing in humans, and visual information and proprioceptive inputs from the legs are very sensitive sensory loops for body sway control. This study investigated the postural control in a homogeneous population of 50 unilateral vestibular-deficient patients (Ménière’s disease patients). It analyzed the postural deficits of the patients before and after surgical treatment (unilateral vestibular neurotomy) of their diseases and it focused on the visual contribution to the fine regulation of body sway. Static posturographic recordings on a stable force-plate were done with patients with eyes open (EO) and eyes closed (EC). Body sway and visual stabilization of posture were evaluated by computing sway area with and without vision and by calculating the percentage difference of sway between EC and EO conditions. Ménière’s patients were examined when asymptomatic, 1 day before unilateral vestibular neurotomy, and during the time-course of recovery (1 week, 2 weeks, 1 month, 3 months, and 1 year). Data from the patients were compared with those recorded in 26 healthy, age- and sex-matched participants. Patients before neurotomy exhibited significantly greater sway area than controls with both EO (+52%) and EC (+93%). Healthy participants and Ménière’s patients, however, displayed two different behaviors with EC. In both populations, 54% of the subjects significantly increased their body sway upon eye closure, whereas 46% exhibited no change or significantly swayed less without vision. This was statistically confirmed by the cluster analysis, which clearly split the controls and the patients into two well-identified subgroups, relying heavily on vision (visual strategy, V) or not (non-visual strategy, NV). The percentage difference of sway averaged +36.7%±10.9% and –6.2%±16.5% for the V and NV controls, respectively; +45.9%±16.8% and –4.2%±14.9% for the V and NV patients, respectively. These two distinct V and NV strategies seemed consistent over time in individual subjects. Body sway area was strongly increased in all patients with EO early after neurotomy (1 and 2 weeks) and regained preoperative values later on. In contrast, sway area as well as the percentage difference of sway were differently modified in the two subgroups of patients with EC during the early stage of recovery. The NV patients swayed more, whereas the V patients swayed less without vision. This surprising finding, indicating that patients switched strategies with respect to their preoperative behavior, was consistently observed in 45 out of the 50 Ménière’s patients during the whole postoperative period, up to 1 year. We concluded that there is a differential weighting of visual inputs for the fine regulation of posture in both healthy participants and Ménière’s patients before surgical treatment. This differential weighting was correlated neither with age or sex factors, nor with the clinical variables at our disposal in the patients. It can be accounted for by a different selection of sensory orientation references depending on the personal experience of the subjects, leading to a more or less heavy dependence on vision. The change of sensory strategy in the patients who had undergone neurotomy might reflect a reweighting of the visual and somatosensory cues controlling balance. Switching strategy by means of a new sensory selection of orientation references may be a fast adaptive response to the lesion-induced postural instability.

Walking performance of vestibular-defective patients before and after unilateral vestibular neurotomy

The present study investigated goal-directed linear locomotion in nine Menières patients before and after (1 week, 1 and 3 months) a curative unilateral vestibular neurotomy (UVN). Experiments were done using a 3D motion analysis system in subjects walking eyes open (EO) and eyes closed (EC) towards a real or memorized target, respectively. Locomotor pattern (velocity, step length, step frequency and walk ratio) and walking trajectory deviations were evaluated for normal and fast speeds of locomotion and compared to those recorded in 10 healthy subjects. Before UVN, patients showed no walking deviation but gait pattern changes characterized by slower walks compared to the controls, mainly due to step length and step frequency reductions for both visual conditions and locomotion speeds. In the acute stage after UVN, locomotor pattern impairments were significantly accentuated. On the other hand, patients showed strong walking deviations towards the lesioned side with EC. Opposite lateral deviation towards the intact side were observed with EO for normal speed only. Recovery from impaired locomotor pattern was achieved within 1 month for normal speed but remained uncompensated 3 months post-lesion for fast speed particularly in EC condition. Finally, the walking trajectory deviation towards the lesioned side in the dark was maintained up to 3 months after UVN. The results show that central processing of visual and vestibular cues contributes to an accurate locomotor pointing. They argue for an increased weight of visual reference frame on locomotor functions when vestibular function is unilaterally impaired.

Neuronal coding of linear motion in the vestibular nuclei of the alert cat

SummaryThe aim of the present study was to investigate some aspects of the central processing of otolith information during linear motion. For this purpose, the response characteristics of 69 vestibular nuclei units to sinusoidal otolith stimulation in the vertical Z axis were analysed in the alert cat. Among this population of neurons which responded to a 0.05 Hz, 290 mm translation, 47 units (70%) displayed a firing rate modulation which followed the input frequency (H1 units). The majority of these neurons exhibited an increase in discharge rate during upward displacement, with a response phase close to the motion velocity or slightly leading downward acceleration. The acceleration related units were divided into two groups according to whether they showed clear increases or only a slight change in discharge rate when the stimulus frequency was increased. The former group was characterized by an average −16.3 dB drop in gain (from 43.9±1.8 dB, S.D. to 27.6±7 dB, S.D.) within the 0.05 Hz–0.5 Hz frequency range, while the latter group displayed an average −31.2 dB gain attenuation (from 45.1±1.1 dB, S.D. to 13.9±0 dB) within the same decade. In contrast to differences in response gain, all the units tested exhibited a relatively stable phase lead of about 20° with respect to downward peak acceleration. Conversely, units whose response was close to motion velocity in the lower frequency range (0.05 Hz–0.10 Hz) displayed a strong phase lead of about 100° when the stimulus frequency was increased (up to 0.50 Hz). These neurons were thus characterized by an acceleration related response in the higher frequency range. At the same time, an average −24.8 dB gain attenuation (from 47.7±3.4 dB to 22.9±3.7 dB) was found in the 0.05 Hz–0.5 Hz decade. The remaining 22 neurons (30%) were called H2 units since they displayed a response waveform double that of the input frequency, a response already described during sinusoidal rotation. Unit discharge reached a peak approximately in phase with maximum upward and downward velocity. Asymmetrical change in unit firing rate about the resting discharge level and different dynamic behavior of the upward and downward response components were usually found. These response characteristics suggest that the H2 patterns are centrally constructed and could result from convergence of otolith afferents having opposite polarization vectors. Other evidence suggests that these units which behave like motion-detectors can exert an influence on the neck musculature. Our results corroborate, at least in part, the findings of previous studies on the dynamic responses properties of otolith-dependent central neurons during roll tilt, or pure linear acceleration in the horizontal plane.

Dental occlusion and postural control in adults

We studied the influence of a dental occlusion perturbation on postural control. The tests were performed in three dental occlusion conditions: (Rest Position: no dental contact, Maximal Intercuspal Occlusion: maximal dental contact, and Thwarted Laterality Occlusion: simulation of a dental malocclusion) and four postural conditions: static (stable platform) and dynamic (unstable platform), with eyes open and eyes closed. A decay of postural control was noted between the Rest Position and Thwarted Laterality Occlusion conditions with regard to average speed and power indexes in dynamic conditions and with eyes closed. However, the head position and stabilization were not different from those in the other experimental conditions, which means that the same functional goal was reached with an increase in the total energetic cost. This work shows that dental occlusion differently affects postural control, depending on the static or dynamic conditions. Indeed, dental occlusion impaired postural control only in dynamic postural conditions and in absence of visual cues. The sensory information linked to the dental occlusion comes into effect only during difficult postural tasks and its importance grows as the other sensory cues become scarce.

Tell Me Your Vestibular Deficit, and I’ll Tell You How You’ll Compensate

Most patients with unilateral vestibular loss exhibit a similar static and dynamic vestibular syndrome consisting of vestibulo‐ocular, posturolocomotor, and perceptive deficits. This vestibular syndrome recovers more or less completely and more or less rapidly over time. One open question is whether recovery mechanisms differ according to vestibular pathology and/or patients. It is reported here (1) data from three different cat models of unilateral vestibular loss reproducing vestibular pathology with sudden (unilateral vestibular neurectomy [UVN] model), gradual (unilateral labyrinthectomy [UL] model), or reversible (tetrodotoxine [TTX]) model) loss of vestibular function, and (2) clinical observations in a population of unilateral vestibular loss patients suffering the same pathology (Menières disease). Animal models show that time courses and mechanisms of recovery depend on the type of vestibular deafferentation, and clinical findings show that Menières patients compensate their postural and perceptive deficits using different vicarious processes. Taken together, results point to a more complex picture of compensation after unilateral vestibular loss, which cannot be reduced either to a common recovery mechanism or to a single process identical for all individuals. These findings should guide physiotherapists in treatment and rehabilitation for vestibular deficits.

Disturbance of contralateral unipedal postural control after stimulated and voluntary contractions of the ipsilateral limb.

One session of sustained unilateral voluntary muscular contractions increases central fatigue and induces a cross-over of fatigue of homologous contralateral muscles. It is not known, however, how this cross-transfer affects contralateral unipedal postural control. Moreover, contralateral neurophysiological effects differ between voluntary muscular contractions and electrically stimulated contractions. The aims of this study were thus to examine the effects of muscle fatigue on contralateral unipedal postural control and to compare the effects of stimulated and voluntary contractions. Fifteen subjects took part in the protocol. Fatigue of the ipsilateral quadriceps femoris was generated either by neuromuscular electrical stimulation (NMES) or by isometric voluntary muscular contraction (VOL). Postural control on the contralateral limb was measured before (PRE condition) and after the completion of the two fatiguing exercises (POST condition) using a force platform. We analyzed body sway area and the spectral power density given by the wavelet transform. In POST condition, postural control recorded in the unipedal stance on the contralateral limb was disturbed after NMES and VOL fatiguing exercises. In addition, postural control was similarly disturbed for both exercises. These results suggest that cross-over fatigue is able to disturb postural control after both stimulated and voluntary contractions.

How changes in vestibular and visual reference frames combine to modify body orientation in space.

The aim of this study was to analyse how changes in vestibular and visual reference frames combine to modify body orientation in space, and to determine the relationship between postural, oculomotor and perceptive parameters. Changes in vestibular and visual references were investigated by comparing controls and vestibular defective patients (Ménières patients tested before and one week after unilateral vestibular nerve section) under three visual contexts (light with and without vertical and horizontal coordinates, darkness). Unilateral vestibular loss was responsible for postural and perceptive deviations whose direction depended on the presence of visual reference frame. We suggest these changes vary according to the spatial reference frame patients are based on. Postural changes were related to perceptive modifications but not to eye cyclotorsion.

Posture and cognition in the elderly: interaction and contribution to the rehabilitation strategies.

In this paper we review the effects of aging on sensory systems and their impact on posture, balance and gait. We also address cognitive aging and attempt to specify which altered cognitive functions negatively impact balance and walking. The role of cognition in postural control is tested with dual-task experiments. This situation results in deleterious effects due to an attentional overload. Given the human cognitive system has limited capacities, we propose that simultaneously performing two tasks depends on the capacity of each individual to perform these tasks on a continuum between automatic execution to highly controlled performance. A level of maximum control exceeds the subjects attentional capacity, which makes it impossible to perform both tasks simultaneously. The subject therefore prioritizes one of the tasks. We use representative dual-task studies from the literature to illustrate the relationship between the different cognitive components and their impact on the control of posture and gait in elderly subjects with altered cognitive capacities and with elderly subjects who are fallers or who have altered sensory-motor capacities. Recently this postural-cognitive relationship was addressed with a new approach. We report how cognitive training can improve dual-task management and we attempt to define the cognitive mechanisms that may be responsible for better postural balance.

Stimulated and voluntary fatiguing contractions of quadriceps femoris differently disturb postural control

Muscle fatigue affects muscle strength and postural control. However, it is not known whether impaired postural control after fatiguing muscular exercise depends on the nature of the muscle contraction. To answer this question, the present study analyzes changes in postural control after two fatiguing exercises of equal duration and intensity but that induced different magnitudes of strength loss. The effects of fatiguing contractions of the femoris quadriceps were compared for voluntary muscular contraction (VOL) and neuromuscular electrical stimulation (ES) on muscle strength and postural control. Seventeen subjects completed these two fatiguing exercises. Maximal voluntary contraction (MVC) and postural control were recorded using an isokinetic dynamometer and a force platform that recorded the center of foot pressure. Recordings were performed before and after the completion of both fatiguing tasks. Results indicate that, after a fatiguing exercise, the ES exercise affected MVC more than the VOL exercise. Inversely, postural control was disturbed more after VOL exercise than after ES exercise. In conclusion, postural control disturbance is influenced by the nature of the muscular contraction (voluntary vs. non-voluntary) and the type of the motor unit solicited (tonic vs. phasic) rather than by the magnitude of strength loss.

Dynamic properties of the vertical otolith neck reflexes in the alert cat

SummaryElectromyographic activity of dorsal neck muscles elicited by sinusoidal vertical linear accelerations was studied in alert cats over a wide range of frequencies. Experiments were performed in headfixed cats and total darkness in order to activate selectively the otolith system. The polyunitary EMG activity was recorded from splenius capitis muscles in normal and labyrinthectomized cats during vertical translations varying from 0.05–1 Hz with a fixed 290 mm peak-to-peak amplitude. The corresponding accelerations ranged from 0.003–1.2 g. In normal cats, the results showed a bilateral and sinusoidal modulation of the EMG activity characterized by two typical EMG patterns depending on the stimulus frequency. In the low-frequency range (0.05–0.25 Hz), the neck muscles responses were composed of a second harmonic (frequency double that of the input signal: H2 responses). The H2 pattern was characterized by an increase in EMG activity during both the upward and downward parts of translation. These two components of the H2 response were closely related to the two peak velocities (+90° and −90°) of the animal motion. Only slight decreases in amplitude and shifts in phase were observed when increasing the frequency. In the higher frequency range (0.25–1 Hz), the neck muscles response was composed of a fundamental frequency corresponding to the input signal (H1 response). The H1 pattern was in phase with the peak of downward acceleration at 0.25 Hz. A phase lag (up to 45°) and a gain attenuation (16.5 dB) were observed when increasing the frequency. The two H1 and H2 EMG patterns were totally absent in bilateral vestibular neurectomized cats. In unilateral vestibular neurectomized cats, a strong drop in gain and phase advance was noted, which mainly affected the H1 pattern. The present results describe some characteristics of otolith-spinal reflexes acting on the head musculature during vertical motion. They are compared with the neuronal responses that we have recorded within the vestibular nuclei complex in the same experimental conditions. The functional role of the vertical otolithneck reflexes in stabilizing the head in space during many real-life situations is discussed.