Relationships between neck muscle electromyography and three-dimensional head kinematics during centrally induced torsional head perturbations

Abstract

The relationship between neck muscle electromyography (EMG) and torsional head rotation (about the nasooccipital axis) is difficult to assess during normal gaze behaviors with the head upright. Here, we induced acute head tilts similar to cervical dystonia (torticollis) in two monkeys by electrically stimulating 20 interstitial nucleus of Cajal (INC) sites or inactivating 19 INC sites by injection of muscimol. Animals engaged in a simple gaze fixation task while we recorded three-dimensional head kinematics and intramuscular EMG from six bilateral neck muscle pairs. We used a cross-validation-based stepwise regression to quantitatively examine the relationships between neck EMG and torsional head kinematics under three conditions: 1) unilateral INC stimulation (where the head rotated torsionally toward the side of stimulation); 2) corrective poststimulation movements (where the head returned toward upright); and 3) unilateral INC inactivation (where the head tilted toward the opposite side of inactivation). Our cross-validated results of corrective movements were slightly better than those obtained during unperturbed gaze movements and showed many more torsional terms, mostly related to velocity, although some orientation and acceleration terms were retained. In addition, several simplifying principles were identified. First, bilateral muscle pairs showed similar, but opposite EMG-torsional coupling terms, i.e., a change in torsional kinematics was associated with increased muscle activity on one side and decreased activity on the other side. s, whenever torsional terms were retained in a given muscle, they were independent of the inputs we tested, i.e., INC stimulation vs. corrective motion vs. INC inactivation, and left vs. right INC data. These findings suggest that, despite the complexity of the head-neck system, the brain can use a single, bilaterally coupled inverse model for torsional head control that is valid across different behaviors and movement directions. Combined with our previous data, these new data provide the terms for a more complete three-dimensional model of EMG: head rotation coupling for the muscles and gaze behaviors that we recorded.