Michel Guerraz

Ocular versus extraocular control of posture and equilibrium

Vision has been shown for almost a century to be heavily involved in postural control. However, the mechanism by which it operates is still an open debate. The purpose of this manuscript is to review the evidence supporting the view that there are two modes of visual detection of body sway: ocular and extraocular. The former is based on the characteristics of the visual flow (retinal slip), the second one is based on either the copy of the motor command (efference copy) or the extraocular muscle afferents (re-afferences) consecutive to eye movements. Results from the literature indicate that these two modes of visual detection of body sway are effective and can operate congruently. For sufficiently large body sway with respect to eye-target distance, the ocular and the extraocular perception systems could provide two sources of visual information about body displacements. However, the afferent system might remain the only one used for small lateral body sway.

Sensory interactions for human balance control revealed by galvanic vestibular stimulation.

Many types of sensory information are known to contribute to the human balance control process but little is known about how the different sensory channels interact. Here we consider the postural response to a perturbation delivered to the vestibular channel using galvanic vestibular stimulation. We show that the response is modified by the absence of information in the other sensory channels. Removal of somatosensory information leads to a massive increase in response size. Similarly, removal of visual information augments the response. Furthermore, the response size is graded according to the amount of visual information available. These effects occur through two processes. One that influences the developing response through feedback mechanisms and another that influences the initial response selection through gain changes. The latter is described as a competitive process that can be likened to a proportional representation voting system.

Feedforward versus feedback modulation of human vestibular‐evoked balance responses by visual self‐motion information

Visual information modulates the balance response evoked by a pure vestibular perturbation (galvanic vestibular stimulation, GVS). Here we investigate two competing hypotheses underlying this visual–vestibular interaction. One hypothesis assumes vision acts in a feedforward manner by altering the weight of the vestibular channel of balance control. The other assumes vision acts in a feedback manner through shifts in the retinal image produced by the primary response. In the first experiment we demonstrate a phenomenon that is predicted by both hypotheses: the GVS‐evoked balance response becomes progressively smaller as the amount of visual self‐motion information is increased. In the second experiment we independently vary the pre‐stimulus and post‐stimulus visual environments. The rationale is that feedback effects would depend only upon the post‐stimulus visual environment. Although the post‐stimulus visual environment did affect later parts of the response (after ∼400 ms), the pre‐stimulus visual environment had a strong influence on the size of the early part of the response. We conclude that both feedforward and feedback mechanisms act in concert to modulate the GVS‐evoked response. We suggest this dual interaction that we observe between visual and vestibular channels is likely to apply to all sensory channels that contribute to balance control.

Effect of Achilles tendon vibration on postural orientation

Vibration applied to the Achilles tendon is well known to induce in freely standing subjects a backward body displacement and in restrained subjects an illusory forward body tilt. The purpose of the present experiment was to evaluate the effect of Achilles tendon vibration (90Hz) on postural orientation in subjects free of equilibrium constraints. Subjects (n=12) were strapped on a backboard that could be rotated in the antero-posterior direction with the axis of rotation at the level of the ankles. They stood on a rigid horizontal floor with the soles of their feet parallel to the ground. They were initially positioned 7 degrees backward or forward or vertical and were required to adjust their body (the backboard) to the vertical orientation via a joystick. Firstly, results showed that in response to Achilles tendon vibration, subjects adjusted their body backward compared to the condition without vibration. This backward body adjustment likely cancel the appearance of an illusory forward body tilt. It was also observed that the vibratory stimulus applied to the Achilles tendon elicited in restrained standing subjects an increased EMG activity in both the gastrocnemius lateralis and the soleus muscles. Secondly, this vibration effect was more pronounced when passive displacement during the adjustment phase was congruent with the simulated elongation of calf muscles. These results indicated that the perception of body orientation is coherent with the postural response classically observed in freely standing subjects although the relationship between these two responses remains to be elucidated.

Expectation and the Vestibular Control of Balance

Recent experiments have shown that the visual channel of balance control is susceptible to cognitive influence. When a subject is aware that an upcoming visual disturbance is likely to arise from an external agent, that is, movement of the visual environment, rather than from self-motion, the whole-body response is suppressed. Here we ask whether this is a principle that generalizes to the vestibular channel of balance control. We studied the whole-body response to a pure vestibular perturbation produced by galvanic vestibular stimulation (GVS; 0.5 mA for 3 sec). In the first experiment, subjects stood with vision occluded while stimuli were delivered either by the subject himself (self-triggered) or by the experimenter. For the latter, the stimulus was delivered either without warning (unpredictable) or at a fixed interval following an auditory cue (predictable). Results showed that GVS evoked a whole-body response that was not affected by whether the stimulus was self-triggered, predictable, or unpredictable. The same results were obtained in a second experiment in which subjects had access to visual information during vestibular stimulation. We conclude that the vestibular-evoked balance response is automatic and immune to knowledge of the source of the perturbation and its timing. We suggest the reason for this difference between visual and vestibular channels stems from a difference in their natural abilities to signal self-motion. The vestibular system responds to acceleration of the head in space and therefore always signals self-motion. Visual flow, on the other hand, is ambiguous in that it signals object motion and eye motion, as well as self-motion.

Attenuation of the evoked responses with repeated exposure to proprioceptive disturbances is muscle specific

In response to repetitive proprioceptive disturbances (vibration) applied to postural muscles, the evoked response has been shown to decrease in amplitude within the first few trials. The present experiment investigated whether this attenuation of the response to vibration stimulation (90Hz, 5s) was muscle specific or would be transferred to the antagonist muscles. Sixteen participants stood upright with eyes closed. One half of the participants practiced 15 tibialis vibrations followed by 15 calf vibrations (TIB-CALF order), while the other half practiced the opposite order (CALF-TIB order). Antero-posterior trunk displacements were measured at the level of C7 and centre of foot pressure (COP). EMG activity of the tibialis anterior (TA) and gastrocnemius lateralis (GL) was also measured. Results showed that evoked postural responses as well as EMG activity decreased with practice when vibration was applied to either calf or tibialis muscles. However, such attenuation of the response appeared muscle specific since it did not generalise when the same vibration stimulus was later applied onto the antagonist muscles.

Corrigendum to “Mechanisms underlying visually induced body sway” [Neurosci. Lett. 443 (2008) 12–16]

Fig. 1. Mean lateral body translation (C7) in both headand earth-fixed foreground conditions over the 65 s of background motion. Upward deflections indicate translations in the direction of the moving background. Note the initially diverging postural response in the two conditions for the first few seconds. The inset shows the two conditions averaged together (excluding the initial 10 s as they are opposite in direction) fitted with an exponential of time constant =20 s.