Callum J. Osler

Postural threat differentially affects the feedforward and feedback components of the vestibular-evoked balance response

Circumstances may render the consequence of falling quite severe, thus maximising the motivation to control postural sway. This commonly occurs when exposed to height and may result from the interaction of many factors, including fear, arousal, sensory information and perception. Here, we examined human vestibular‐evoked balance responses during exposure to a highly threatening postural context. Nine subjects stood with eyes closed on a narrow walkway elevated 3.85 m above ground level. This evoked an altered psycho‐physiological state, demonstrated by a twofold increase in skin conductance. Balance responses were then evoked by galvanic vestibular stimulation. The sway response, which comprised a whole‐body lean in the direction of the edge of the walkway, was significantly and substantially attenuated after ~800 ms. This demonstrates that a strong reason to modify the balance control strategy was created and subjects were highly motivated to minimise sway. Despite this, the initial response remained unchanged. This suggests little effect on the feedforward settings of the nervous system responsible for coupling pure vestibular input to functional motor output. The much stronger, later effect can be attributed to an integration of balance‐relevant sensory feedback once the body was in motion. These results demonstrate that the feedforward and feedback components of a vestibular‐evoked balance response are differently affected by postural threat. Although a fear of falling has previously been linked with instability and even falling itself, our findings suggest that this relationship is not attributable to changes in the feedforward vestibular control of balance.

Galvanic Vestibular Stimulation Produces Sensations of Rotation Consistent with Activation of Semicircular Canal Afferents

Galvanic Vestibular Stimulation (GVS) is a simple method for evoking sensations of movement (Fitzpatrick and Day, 2004). It involves passing small currents, typically <5 mA, across the mastoid processes. A recent article by Cohen et al. (2012) discussed the mechanism of action of GVS. The authors concluded that although GVS excites both otolith and semicircular canal afferents, only otolith-related behavioral responses are induced. Specifically, it was stated that human subjects “…do not experience sensations of rotation and do not display ocular nystagmus, which would occur if the semicircular canals were continuously stimulated.” However, a growing body of evidence from perceptual, oculomotor, and whole-body experiments confirms that GVS does indeed produce sensations of rotation consistent with canal stimulation. Fitzpatrick et al. (2002) investigated the effect of binaural bipolar GVS upon the ability of supine subjects to report rotation around a vertical axis. When stimulation was applied concurrently with real rotation, subjects reported lesser, or greater movement depending on stimulus polarity. To minimize activation of the otoliths, the axis of (real) rotation was collinear with the midline between the ears. However, even when this axis was altered to produce a combination of translation and rotation, it did not change the effect of GVS upon perception. This suggests that GVS primarily influences the sensation of rotation, not translation. In a similar experiment, Day and Fitzpatrick (2005) determined the precise axis of this “virtual” rotation vector. Seated subjects adopted different head pitches while being spun on a rotary chair. Again, when GVS was applied, sensations of rotation could be increased or decreased in a polarity-dependent fashion. Maximal effects occurred when the naso-occipital axis was approximately co-linear with the axis of real rotation (i.e., with the head pitched fully up or down). With the head close to the neutral position, such that Reid’s plane was tilted 18.8° above horizontal (i.e., slight nose-up tilt), the effect of GVS upon rotation sensation was zero. This suggests that GVS evokes a sensation of head roll around a naso-occipital axis. Using a modeling approach, the authors elegantly demonstrated that this axis is a direct consequence of the anatomical orientation of the canals (Blanks et al., 1975). Based on the assumption that GVS modulates all vestibular afferents equally (Goldberg et al., 1984), they calculated the theoretical axis of head rotation when equal signals from all six canals are combined. It transpires that the resulting axis is naso-occipital, and elevated 16.4° relative to Reid’s plane. This tallies remarkably well with the data gained from the chair rotation experiment. Evoked eye movements corroborate these data. Many studies have described a torsional eye movement response to GVS (Schneider et al., 2000, 2002; Jahn et al., 2003; MacDougall et al., 2005). This consists not only of a fixed offset of eye position as one might expect from pure otolith activation, but contains alternating fast and slow phases, consistent with a canal-evoked nystagmus caused by head roll. Schneider et al. (2002) compared the ocular response to GVS with that caused by head roll. They found that GVS produced essentially the same eye movement as pure head rotation; i.e., torsional offset accompanied by nystagmus. This raises the possibility that both characteristics of the GVS-evoked eye movement can be explained entirely on the basis of rotation. Galvanic Vestibular Stimulation-evoked body movements agree with the perception and eye movement data. With the head tilted up or down GVS evokes locomotor turning (Fitzpatrick et al., 2006), and in standing subjects it induces vertical torque reactions (Reynolds, 2011). In the absence of somatosensory information GVS evokes a continuous body tilt response for the duration of the stimulus, rather than merely a fixed offset of body position (Day and Cole, 2002). Furthermore, prolonged stimuli evoke oscillating “nodding” lateral head responses, akin to ocular nystagmus (Wardman et al., 2003). These movements are consistent with a counteractive response to a sensation of continuous rotation, and cannot be readily attributed to sensations of tilt or linear acceleration. Nevertheless, the possibility of an otolith-based response has not been definitively excluded. Cathers et al. (2005) examined the effect of head pitch on GVS-evoked balance responses. Robust sway responses were observed with the head upright, but with the head tilted down the main balance response was abolished, leaving only a small transient sway. This transient response can be explained as a reaction to a sense of inter-aural linear acceleration, suggesting it can be attributed to otolith stimulation. However, a recent study examining the effect of head orientation on this response suggests it is not compatible with the anatomical properties of the otolith organs (Mian et al., 2010). This raises the possibility that weak trans-mastoidal current may also stimulate non-vestibular pathways to generate motor output. But regardless of the origin of the early transient response, it is dwarfed in magnitude by the later rotation-based movement consistent with canal stimulation. In summary, overwhelming evidence from perception, anatomy, modeling, oculomotor, and whole-body responses all converges toward the same conclusion: GVS is primarily interpreted by the brain as head roll, consistent with activation of semicircular canal afferents. Whether it also evokes sensations of tilt and/or linear acceleration, which would be indicative of otolith activation, is less certain (for a more comprehensive recent review, see St George and Fitzpatrick, 2011).

Mechanisms of interpersonal sway synchrony and stability

Here we explain the neural and mechanical mechanisms responsible for synchronizing sway and improving postural control during physical contact with another standing person. Postural control processes were modelled using an inverted pendulum under continuous feedback control. Interpersonal interactions were simulated either by coupling the sensory feedback loops or by physically coupling the pendulums with a damped spring. These simulations precisely recreated the timing and magnitude of sway interactions observed empirically. Effects of firmly grasping another persons shoulder were explained entirely by the mechanical linkage. This contrasted with light touch and/or visual contact, which were explained by a sensory weighting phenomenon; each persons estimate of upright was based on a weighted combination of veridical sensory feedback combined with a small contribution from their partner. Under these circumstances, the model predicted reductions in sway even without the need to distinguish between self and partner motion. Our findings explain the seemingly paradoxical observation that touching a swaying person can improve postural control.

Dynamic transformation of vestibular signals for orientation

The same pattern of vestibular afferent feedback may signify a loss of balance or a change in body orientation, depending upon the initial head posture. To resolve this ambiguity and generate an appropriate motor response, the CNS must transform vestibular information from a head-centred reference frame into relevant motor coordinates. But what if the reference frame is continuously moving? Here, we ask if this neural transformation process is continuously updated during a voluntary change in head posture. Galvanic vestibular stimulation (GVS) was used to induce a sensation of head roll motion in blindfolded subjects marching on the spot. When head orientation was fixed, this caused unconscious turning behaviour that was maximal during neck flexion, minimal with the head level and reversed direction with neck extension. Subjects were then asked to produce a continuous voluntary change in head pitch, while GVS was applied. As the neck moved from full flexion into extension, turn velocity was continuously modulated and even reversed direction, reflecting the pattern observed during the head-fixed condition. Hence, an identical vestibular input resulted in motor output which was dynamically modulated by changes in head pitch. However, response magnitude was significantly reduced, suggesting possible suppression of vestibular input during voluntary head movement. Nevertheless, these results show that the CNS continuously reinterprets vestibular exafference to account for ongoing voluntary changes in head posture. This may explain why the head can be moved freely without losing the sense of balance and orientation.

Increased gravitational force reveals the mechanical, resonant nature of physiological tremor

Physiological hand tremor has a clear peak between 6 and 12 Hz, which has been attributed to both neural and resonant causes. A reduction in tremor frequency produced by adding an inertial mass to the limb has usually been taken as a method to identify the resonant component. However, adding mass to a limb also inevitably increases the muscular force required to maintain the limbs position against gravity, so ambiguous results have been reported. Here we measure hand tremor at different levels of gravitational field strength using a human centrifuge, thereby increasing the required muscular force to preserve limb position without changing the limbs inertia. By comparing the effect of added mass (inertia + force) versus solely added force upon hand acceleration, we conclude that tremor frequency can be almost completely explained by a resonant mechanical system.