Community Research and Development Information Service - CORDIS

FP7

HEADS-UP Report Summary

Project ID: 624158
Funded under: FP7-PEOPLE
Country: Netherlands

Periodic Report Summary 1 - HEADS-UP (The modulation of vestibular reflexes during self-generated head-neck movements)

Summary description of project objectives

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 commands. A key feature of this sensory integration is the ability to differentiate externally imposed and self-generated head 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 neck motor output (i.e. muscle activation) and vestibular reflexes during self-generated movements remains incomplete.
Two main ideas regarding the function of vestibular signals for neck muscle (vestibulocollic responses) control have emerged. The first stems from physiological studies, and states that vestibulocollic signals stabilize the head in space during body movements. However if vestibulocollic responses were to remain active during self-generated movement, it would oppose the intended motion. The second idea is based on engineering principles, and states that vestibulocollic responses dampens oscillations that arise as a result of the underdamped mechanics of the head/neck system. In this case however, complete cancellation of the vestibulocollic responses may lead to unwanted oscillatory behaviour during self-generated head movement. Therefore, the primary objective of the HEADS-UP project is to establish the interaction between vestibular suppression mechanisms and vestibulocollic responses during self-generated head movements. In this effort, period 1 of the project aimed to answer two questions in two separate work packages:
1. Are vestibulocollic responses modulated differentially during self-generated relative to externally imposed head movements (WPI)?
2. What is the effectiveness of vestibular suppression during self-generated head movements (WPII)?

Work performed

For this first 16 months of the project I carried out research on the contribution of vestibular signals on neck muscle activity during active head movements. The work was divided into two work packages each setup to answer the above research questions. For the completion of WPI, I carried out (1) programming of rotary chair robot, (2) programming of head perturbation robot, (3) experiments on the effect of head motion on electrically evoked vestibulocollic responses, (4) experiments comparing the effect of active versus passive head movements on electrically evoked vestibulocollic responses, (5) experiments comparing motion and electrically induced vestibulocollic responses, (6) experiments characterizing vestibulocollic responses in 16 neck muscles, (7) experiments characterizing the high frequency response of multi and single motor unit responses evoked by vestibular signals, and (8) analysis of afferent data from a collaborating institute. Some of the above tasks were additional to the originally proposed research but were essential in completing the research. For the completion of WPII, I carried out (1) programming of the head perturbation robot, and (2) experiments on the effectiveness of vestibular suppression during active head movements.

Description of the main results achieved so far

I have conducted experiments showing that natural vestibular stimulation due to head motion modulates (decreases) the electrically evoked vestibulocollic reflex. These results demonstrate that the vestibular evoked motor response in neck muscles is not a linear summation of the two inputs. I identified three potential physiological sources facilitating this subaddative mechanism: 1) the motoneuron, 2) the vestibular afferents, or 3) the vestibular nuclei. To eliminate the first possibility, I performed additional experiments at multiple frequencies and showed that the modulation does not vary with the motoneuron response properties at these frequencies (Forbes et al. 2015a). To eliminate the second possibility, I analyzed data collected from afferent studies (obtained through collaboration with the external vestibular expert) combining motion and electrical stimulation, and showed that afferent responses to electrical stimulation do no vary with simultaneous motion. Thus I conclude that the observed modulation occurs at the vestibular nuclei.
I then performed experiments to compare the differential effects of active and passive motion. Similar to the above result, the simultaneous presence of motion modulated the electrically evoked response; however, this modulation did not depend on the motion being either passive or active (Forbes et al. 2015b). 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. Thus the vestibulocollic reflex contributes to movement control even in conditions where its presence might counter the intended movement.
I also obtained exceptional insight into the firing behaviour of afferent responses through the collaborative work with the external vestibular experts. I visited their lab during their experiments and was given access to the data for analysis purposes. These results for the first time demonstrated that all afferents are affected by the stimulus, thus ending the ongoing debate within the literature as to which afferent type responds to electrical currents (Kwan et al. 2015). To compliment this data I conducted experiments to compare the dynamic properties of the electrically and motion evoked vestibulocollic reflexes. By combining these two sets of data I will construct a model to explain how vestibular afferent signals are summed to generate the electrically evoked response.
This led me to question whether the projections of vestibular afferent signals to neck muscles are related to the functionality of each neck muscle. I carried out experiments collecting EMG from 16 neck muscles during electrical stimulation. The data is still being collected but preliminary results indicate all neck muscles receive input from vestibular signals that is specific to the mechanical action of the muscle. Finally, I performed single motor unit recordings in neck muscles to confirm that the high frequencies observed during electrical stimulation are in fact evoked by stimulation of the vestibular organ and not a product of artifact noise from the stimulus. I found that vestibular inputs can generate muscle activity at frequencies well beyond what is considered functionally relevant for motor control.
I conducted preliminary experiments to determine whether vestibular reafference is calibrated by the central nervous system for head-neck control. In these experiments the electrical stimulation was driven by ongoing head movements. I found that subjects can recalibrate an artificial electrical stimulus to be interpreted as a reafferent signal for head-neck control. However, in the presence of substantial cutaneous inputs the necessity to recalibrate the signal diminishes.
I also conducted a series of experiments that have revealed a number of mechanisms involved in the vestibular control of posture: 1) that the properties of the mechanical system under control (i.e. stiffness, damping and inertia) modifies the vestibular control of posture, decreasing vestibular input to limb muscles as the difficulty of standing decreases, 2) that vestibular signals for posture control undergo a transformation to respond only to the component of an electrically evoked vestibular error that is co-axial with the direction of control (Forbes et al. 2015c), and 3) 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 (Shepherd et al. 2015). These results also support predictions I published during the outgoing phase of the IOF regarding the differences between the vestibular control of neck muscles and lower limb muscles (Forbes et al. 2015d).

Expected final results

The objective of the proposed research is to establish the interaction between vestibular suppression mechanisms and vestibulocollic reflexes (VCR) during self-generated head movements. The outcome of this research will provide insight into the interaction between vestibular suppression and reflexes by directly quantifying the modulation of VCR. These findings may relate to the known difficulties faced by people with vestibular or neck movement disorders (approx. 35% of people 40 years or older), such as age related dizziness and cervical dystonia, when performing such tasks as gaze adjustments and navigation.
The proposed research provides – to my knowledge for the first time – a direct assessment of vestibular reflex processing of externally imposed and self-generated head movements in humans. These results demonstrate that the brain treats the electrically generated stimulus separate from our desired movements and allows VCRs to contribute to head-neck control during active motion. The experimental protocols make novel use of a one-of-a-kind robotic manipulator, a unique experimental approach that has never been applied to the head-neck. This customized robot has the potential to be expanded to additional research applications such as patient rehabilitation, gaze control and motion sickness. Using intramuscular EMG, I have studied deep muscles only hypothesized to be strongly influenced by the vestibular organ and that are critical for our ability to orient, move and interact with our environment. The versatility of intramuscular EMG allowed me to study both multiple and single motor unit activity and has provide additional insight into the vestibular control of muscles.

Forbes PA, Siegmund GP, Schouten AC, and Blouin JS. Central and peripheral afferent processing of natural and artificial vestibular inputs. In: Canadian Association for Neuroscience Conference. Vancouver, BC: 2015a.
Forbes PA, Fice JB, Schouten AC, Siegmund GP, and Blouin JS. Suppression of vestibulocollic reflexes during head movements. In: Canadian Association for Neuroscience Conference. Vancouver, BC: 2015b.
Forbes PA, Luu BL, Van der Loos HF, Croft EA, Inglis JT, and Blouin JS. Spatial transformation of the vestibular control of standing in humans. In: Society for Neuroscience Conference. Chicago, IL: 2015c.
Forbes PA, Siegmund GP, Schouten AC, and Blouin JS. Task, muscle and frequency dependent vestibular control of posture. Frontiers in integrative neuroscience 8: 94, 2015d.
Kwan A, Mitchell DE, Forbes PA, Blouin JS, and Cullen KE. Galvanic vestibular stimulation: Recording afferents during transmastoid stimulation. In: Society for Neuroscience Conference. Chicago, IL: 2015.
Shepherd M, Forbes PA, and Blouin JS. Intersensory vestibular control of standing balance. In: Canadian Association for Neuroscience Conference. Vancouver, BC: 2015.

Contact

Lily Tunggal, (Contract manager)
Tel.: +31 152788684
E-mail

Subjects

Life Sciences
Record Number: 184136 / Last updated on: 2016-06-08
Information source: SESAM