Mechanisms controlling human head stabilization. II. Head-neck characteristics during random rotations in the vertical plane

1. In this study we have tested the hypothesis that the mechanisms controlling stabilization of the head-neck motor system can vary with both the frequency and spatial orientation of an externally applied perturbation. Angular velocity of the head with respect to the trunk (neck) and myoelectric activity of two neck muscles (semispinalis capitis and sternocleidomastoid) were recorded in eight seated subjects during pseudorandom rotations of the trunk in the vertical (pitch) plane. Subjects were externally perturbed with a random sum-of-sines stimulus at frequencies ranging from 0.35 to 3.05 Hz. Four instructional sets were presented. Voluntary mechanisms were examined by having the subjects actively stabilize the head in the presence of visual feedback as the body was rotated (VS). Visual feedback was then removed, and the subjects attempted to stabilize the head in the dark as the body was rotated (NV). Reflex mechanisms were examined when subjects performed a mental arithmetic task during body rotations in the dark (MA). Finally, subjects performed a voluntary head tracking task while the body was kept stationary (VT). 2. In VS and NV, gains and phases of head velocity indicated good compensation for the perturbation at frequencies up to 2 Hz. Between 2 and 3 Hz, gains dropped slowly and then steeply descended above 3 Hz as phases became scattered. 3. In MA, gains were lower and exhibited more scatter than in VS and NV at frequencies <1 Hz. Phases around -180° indicated that compensatory activity was occurring even with these low gains. Between 1 and 2 Hz, response gains steeply ascended, implying that reflex mechanisms were becoming the predominant mechanism for compensation in this frequency range. Above 2 Hz, gains dropped off to 0.5 and lower, but phases remained close to -180°, suggesting that the reflex mechanisms were not dominant in this frequency range, but that they were still contributing toward compensation for the trunk perturbation. 4. Neck muscle electromyographic (EMG) responses were similar in VS, NV, and MA, demonstrating decreasing gains between 0.35 and 1.5 Hz, and then increasing beyond the previous high level of activation. This U-shaped response pattern implies an enhanced participation of neural mechanisms, probably of reflex origin, in the higher frequency range. 5. Patterns observed during external perturbations of the trunk were not apparent in the response dynamics of voluntary head tracking. In VT, subjects successfully tracked the stimulus only at the lowest frequencies of head movement. A gradual and consistent decline was exhibited as frequency increased. EMG activation continued throughout the frequency range, however, suggesting a continued effort to track the target. 6. A comparison of response dynamics revealed that the greatest distinction between responses to pseudorandom rotations in the horizontal and vertical planes existed at very low (<0.5 Hz) frequencies and at frequencies >2 Hz. Low-frequency differences reflected improved gains in the vertical plane. High-frequency differences reflected the presence of resonant oscillations in the horizontal but not in the vertical plane. Response dynamics at these frequencies might have been the result of a stiffer head-neck system in the vertical plane due to the combination of smaller rotational amplitudes and greater muscle moment arms than in the horizontal plane. 7. The results of this study suggest that head stabilizing mechanisms are related to both the frequency and orientation of an external perturbation. Neck reflexes exhibit a greater operational bandwidth in the vertical than in the horizontal plane and may function to damp mechanical resonance and free the voluntary mechanisms for producing an efficient time matched response to a continually changing environment.