Where's your head at? An illusion of head orientation which reveals dissociation of proprioceptive signals for balance versus perception

The vestibular apparatus provides signals of head motion that can be used to stabilise balance. Since it is locked within the skull, the information it provides must first be transformed from head to body-centred coordinates. This requires an accurate sense of head orientation. For example, if head motion is detected towards the left ear when standing face-forwards, the appropriate response would be a compensatory body sway in a rightward direction. But if the head is turned towards our right shoulder, the same pattern of vestibular feedback would now indicate forward body sway, with the appropriate response being directed backward. Any errors in the sensation of head orientation may cause the compensatory sway response to be oriented in the wrong direction, leading to postural instability. This head-to-feet coordinate transformation process has previously been demonstrated using electrical vestibular stimulation (EVS). EVS applies small currents to the mastoid processes that modulate activity in the vestibular nerve. This leads to a false sensation of head (and body) motion towards the cathode electrode that, in turn, leads to a compensatory sway response towards the anode (Fitzpatrick & Day, 2004). As the head is turned left or right, the direction of the evoked sway response rotates by an equal amount, staying fixed within head coordinates, always directed along an axis through the ears. In this issue of The Journal of Physiology, Dalton et al. (2017) describe an intriguing scenario in which this transformation process goes awry. Normally we have an accurate sensation of how the head is aligned with the body, but under special circumstances this can be distorted. The authors used a simple technique for evoking an illusion of head orientation (Gurfinkel et al. 1989). This involved maintaining a prolonged 90 deg leftward turn of the head for up to 15 min, with the head passively held in place and the eyes closed. This intervention caused the erroneous perception that the head was gradually drifting rightward towards the face-forwards position. As the illusion progressed in strength, the vestibular-evoked sway response was periodically probed using EVS stimuli. Initially the direction of the evoked ground reaction force vector was oriented towards the inter-aural axis, as per normal. As time progressed, however, it became skewed towards the direction of illusory head orientation. This demonstrates that the inaccuracy in head orientation sensation affected the transformation of vestibular information for balance. The authors then posed a simple question: what happens if the illusion is abolished? After 15 min, subjects were asked to open their eyes for 30s to allow for visual recalibration, while maintaining the head turned. As expected, this immediately abolished the head orientation illusion and subjects accurately reported the direction they were facing. One might expect the sway response to also return to normal in line with perception, but this was not the case. The direction of the EVS-evoked force vector was completely unaffected by the period of visual recalibration, and remained skewed towards the direction of the prior illusion. Hence, the estimate of head orientation used for balance control did not tally with perception. Thus it seems that the central nervous system can maintain two competing estimates of head orientation simultaneously. What is the mechanism underlying this dissociation? The illusion itself may be due to adaptation of peripheral receptors. Prolonged muscle stretch has been shown to modulate muscle spindle output, with concomitant effects upon joint angle perception (Gregory et al. 1988). The lack of any illusion following active neck rotation may be caused by differences in the mechanical state of the muscle, or is possibly due to alpha–gamma co-activation. Whatever the cause, the illusion was only observed following passive neck rotation. Since vestibulo-spinal neurons are strongly influenced by proprioceptive input from the neck muscles, any inaccuracy in these signals would also affect vestibulo-spinal output. Visual input, by comparison, exhibits a much weaker influence upon vestibulo-spinal neurons (Cullen, 2012). Hence, when it comes to transforming vestibular signals for motor output, the nervous system may have a built-in bias against visual information. Irrespective of the neural mechanisms involved in the dissociation, why would it occur from a teleological perspective? In particular, why would the balance system trust a proprioceptive estimate of head orientation when vision is screaming out that this estimate is bogus? Such behaviour seems maladaptive. Despite the fact that this study involved untrustworthy proprioception it may be that, under more natural circumstances, visual signals exhibit greater ambiguity. False perceptions of movement are readily evoked by moving visual stimuli. In contrast, as the authors point out, we do not normally experience prolonged periods of twisted neck postures. This suggests that the balance system need not adapt to such situations. However, there is an example to the contrary, namely sleep. When lying in bed our head may rest in a twisted position on the pillow for an extended period. Could the faulty transformation of vestibular signals reported by Dalton et al. partly explain the instability we experience when stumbling to the lavatory in the middle of the night?