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Final Report Summary - HEADS-UP (The modulation of vestibular reflexes during self-generated head-neck movements)

Human upright posture of both the head and body is regulated by the central nervous system’s (CNS) ability to integrate multiple sensory feedback signals and generate appropriate motor (i.e. muscle) commands. A key feature of this sensory integration is the ability to differentiate externally imposed and self-generated head and body movements. Although both movement types are indistinguishable to the vestibular sensors they induce very different motor responses. During externally imposed head movements, the vestibular signals are transmitted to motoneurons and elicit vestibular reflexes for gaze and posture maintenance. In the case of self-generated movements vestibular signals are suppressed at the earliest stage of vestibular processing, since any self-generated vestibular response would theoretically oppose the intended movement. However, our understanding of how vestibular suppression affects the resultant motor output (i.e. muscle activation) and vestibular reflexes during self-generated movements remains incomplete. The primary objective of the HEADS-UP project is to establish the interaction between vestibular suppression mechanisms and vestibular evoked responses during motor control activities involving self-motion.

The following outcomes were achieved throughout the duration of this project:
- Whole body rotation experiments showed that natural vestibular stimulation due to head motion modulates (decreases) the electrically evoked vestibulocollic reflex. Three sources facilitating this subaddative mechanism were identified: 1) the motoneuron, 2) the vestibular afferents, or 3) the vestibular nuclei. Control experiments were performed to eliminate the first and second possibility, and a numerical model was developed to confirm that modulation likely occurs at the nuclei. This demonstrates nonlinear processing of vestibular information in humans.
- Head-neck experiments showed that the electrically evoked vestibulocollic reflex is suppressed during both active and passive head movements. This revealed that the vestibular system can separate the reafferent activity during self-generated head movements from the exafferent signal generated by electrical stimulation to generate vestibulocollic reflex responses specific to the exafferent signal.
- Standing balance experiments showed that when the relationship between balancing motor commands and associated vestibular sensory feedback is reversed, the direction of the compensatory ankle response is also reversed. This implies that the nervous system re-associates new relationships between sensory signals and motor commands related to maintaining balance.
- Walking experiments showed that independent vestibular modulation of muscle activity from each limb occurs rapidly at the onset of split-belt walking, over a shorter time course relative to the characteristic split-belt error-correction mechanisms (i.e. muscle activity and kinematics) associated with locomotor adaptation. This indicates that that the nervous system rapidly modulates the vestibular influence of each limb separately through processes involving on-going sensory feedback loops.
- Afferent recordings obtained in collaboration with partners demonstrated that all afferents are affected by the electrical stimulus, thus ending the ongoing debate within the literature as to which afferent type responds to electrical currents. To complement this data, experiments were performed to compare the dynamic properties of the electrically and motion evoked vestibulocollic reflexes in humans. These results characterize the motor output responses in neck muscles during vestibular afferent activity during electrical vestibular stimulation.
- Standing balance experiments were performed to demonstrate that the vestibular control of posture can be engaged in the absence of head motion provided at least two other sensory modalities match normal balancing behaviour.
- Whole body motion experiments showed that the vestibulo-ocular reflex (VOR) is modulated by asking subjects to close their eyes. This was an unexpected finding and is contrary to what is assumed in the literature.
- Neck motor unit recordings were performed to demonstrate that the vestibular system can contribute to neck muscle activity well beyond any expected frequency (up to 150 Hz). This data was compared to afferent recordings obtained from collaborators confirming that the responses were of a vestibular origin.
- Eye movement experiments were performed to provide an assessment of using coupled electrical vestibular stimulation on oculomotor control. These results demonstrate that subjects can recalibrate an artificial electrical stimulus to be interpreted as a reafferent signal when given a reliable visual sensory signal.

These results provide fundamental insight into the vestibular sensorimotor processing that is required for everyday activities such as standing balance, head-neck movements and oculomotor control in humans. In particular, the insight provided by the vestibular afferent recordings during electrical stimulation will form a basis for future studies in fundamental and clinical studies. The research results of HEADS-UP facilitated the launch of two new projects aimed at understanding how zero-gravity conditions influence standing balance and how internal models of vestibular motor control are formed.

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