Mechanisms controlling human head stabilization. I. Head-neck dynamics during random rotations in the horizontal plane

1. Potential mechanisms for controlling stabilization of the head and neck include voluntary movements, vestibular (VCR) and proprioceptive (CCR) neck reflexes, and system mechanics. In this study we have tested the hypothesis that the relative importance of those mechanisms in producing compensatory actions of the head-neck motor system depends on the frequency of an externally applied perturbation. Angular velocity of the head with respect to the trunk (neck) and myoelectric activity of three neck muscles were recorded in seven seated subjects during pseudorandom rotations of the trunk in the horizontal plane. Subjects were externally perturbed with a random sum-of sines stimulus at frequencies ranging from 0.185 to 4.11 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. Gains and phases of head velocity indicated good compensation to the stimulus in VS and NV at frequencies <1 Hz. Gains dropped and phases advanced between 1 and 2 Hz, suggesting interference between neural and mechanical components. Above 3 Hz, the gains of head velocity increased steeply and exceeded unity, suggesting the emergence of mechanical resonance. 3. At low frequencies (<1 Hz) during MA, gains were very low, and phases indicated that the head was moving with the trunk. A steady rise in gains and shift in phases toward a compensatory response were observed as frequency increased. Between 1 and 2 Hz, the response of the neck moved toward compensation as gains observed during voluntary stabilization decreased, suggesting that reflex mechanisms were becoming the predominant controller of compensatory processes at this frequency range. Around 3 Hz, mechanical resonance was observed. 4. In VS, NV, and MA, electromyographic (EMG) activity steadily decreased in gain up to 1 Hz, then continuously increased at frequencies >1 Hz. This implied sustained participation of neural mechanisms in the higher frequency range. Depending on the relative motion of the head with respect to space and to the trunk, either the vestibulocollic or cervicocollic (proprioceptive) reflex were assumed to be present in the EMG output. 5. The patterns observed in the neck responses secondary to trunk perturbations were not apparent in the response dynamics of voluntary head tracking. In VT, the most compensatory gains and phases of both head velocity and muscle EMG responses appeared at the lowest frequencies of head movement. Gains steadily declined, and phase lags increased as frequency increased. 6. We acknowledge that the contributions of the three mechanisms examined here cannot be completely separated by the paradigms used, but the data suggest that reflexes do participate in the stabilization process. Comparisons of the frequency responses of the cat and human showed that a model based on the passive mechanics of the cat's neck is applicable to these data even though experimental conditions were different. Evidence of a similar pattern of gains and phases in our data to that of the animal model allow us to conclude that the observed activity of the head with respect to the trunk in this series of experiments is indicative of a process of compensatory head stabilization as a consequence of trunk movements caused by external forces.