Reflex and mechanical contributions to head stabilization in alert cats

1. Five alert cats were tested for their responses to rotation in a device that allowed rotation of the head on the trunk about a vertical axis passing through the C₁-C₂ vertebral joint. Electrodes were implanted to record the horizontal and vertical electrooculogram and electromyographic (EMG) activity of the dorsal neck muscles splenius, biventer cervicus, and complexus. Head rotation and torque acting on the head were recorded in the horizontal plane during rotations in the 0.05-5.0 Hz frequency range. Responses were interpreted with reference to a closed-loop dynamic model of the head-neck system. 2. Whole-body rotation (WBR) with no neck movement elicited a vestibulocollic reflex (VCR). Neck muscle EMG lagged the sinusoidal platform rotation by ~120° at low frequencies, which represents a 60° lead relative to a perfectly compensatory 180° lag. This phase lead was related to the cumulative eye position of the accompanying horizontal vestibular nystagmus as reported by Vidal et al. Horizontal head torque exhibited a similar low-frequency behavior. At high frequencies, EMG exhibited a progressively increasing phase lead and gain increase typical of a second-order lead system as described in decerebrate cats. Torque, however, showed much less lead and gain increase, presumably because of the low-pass filter properties of the process coupling muscle excitation to torque. Head torque did exhibit a steep increase in gain with frequency and a phase approaching that of platform acceleration at high frequencies when weights were attached to the head to increase its moment of inertia. The same +40 dB/decade gain slope and phase approaching 0° was observed during WBR rotation of the anesthetized cat in which head inertia is the only factor contributing to the torque. This dynamic behavior was predicted by the inertial component of the model. In the alert unweighted cat, the inertial torque was smaller than VCR-generated torque at frequencies below 4 Hz. 3. Rotation of the neck with the head held fixed in space (HFS rotation) elicited a cervicocollic reflex (CCR). Neck EMG response was very similar to that observed during WBR, both in dynamic behavior and overall gain. Torque, however, was consistently greater than that generated by WBR and showed a steady increase of 8 dB/decade as frequency rose. The added torque can be attributed to the viscoelastic properties of neck muscles. 4. Driven rotation of the head on the fixed body elicited torques that could be closely approximated by a vector sum of torques observed during WBR and HFS rotations. These observations indicated that interactions of torques generated by VCR, CCR, and non-reflex mechanics under open-loop conditions can be treated as a simple linear summation. 5. Rotation of the cat with its head free to rotate about the C₁-C₂ axis was carried out under three conditions. With the animal anesthetized, the underdamped second-order behavior of the passive mechanical elements in the head-neck system was observed. Most noteworthy was the resonant peak at ~3 Hz, where gain had risen at 40 dB/decade to a value above 1.0 and where phase had shifted from 0 to -90° on its way to -180°. With the cat alert and its head weighted to increase its moment of inertia two- to fourfold, a similar resonant peak was observed at 2-3 Hz. Rather than falling at 40 dB/decade below the peak, however gain plateaued at 0.4-0.6 from 0.18-1.0 Hz, and phase remained at -180°. Analysis based on the model indicated that this low-frequency behavior resulted from interaction of the VCR with the CCR and neck viscoelasticity. When the added weights were removed, the plateau region extended from 0.18 to 3 Hz. Thus reflex-related forces dominate the closed-loop VCR behavior over this frequency range in the alert cat. 6. Terms in the model transfer function describing the closed-loop VCR operation were reflected in torque measurements made during WBR (inertial and VCR torques) and HFS rotation (viscous, elastic, and CCR torques). The hypothesis of linear interaction of torques incorporated in the model was tested by using these open-loop measurements to predict the closed-loop head movement responses. This prediction closely fitted the actual data for both normal and increased head inertia indicating that the form of the model is correct and that torques do, in fact, sum linearly to determine head rotation. 7. In conclusion, analysis of the alert cat's response to rotation in the context of a dynamic model of the head-neck system indicates that reflex forces dominate head stabilization up to 3-4 Hz, above which frequency head inertia and other mechanical properties become predominant.