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

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.

Cross-validated models of the relationships between neck muscle electromyography and three-dimensional head kinematics during gaze behavior.

The object of this study was to model the relationship between neck electromyography (EMG) and three-dimensional (3-D) head kinematics during gaze behavior. In two monkeys, we recorded 3-D gaze, head orientation, and bilateral EMG activity in the sternocleidomastoid, splenius capitis, complexus, biventer cervicis, rectus capitis posterior major, and occipital capitis inferior muscles. Head-unrestrained animals fixated and made gaze saccades between targets within a 60° × 60° grid. We performed a stepwise regression in which polynomial model terms were retained/rejected based on their tendency to increase/decrease a cross-validation-based measure of model generalizability. This revealed several results that could not have been predicted from knowledge of musculoskeletal anatomy. During head holding, EMG activity in most muscles was related to horizontal head orientation, whereas fewer muscles correlated to vertical head orientation and none to small random variations in head torsion. A fourth-order polynomial model, with horizontal head orientation as the only independent variable, generalized nearly as well as higher order models. For head movements, we added time-varying linear and nonlinear perturbations in velocity and acceleration to the previously derived static (head holding) models. The static models still explained most of the EMG variance, but the additional motion terms, which included horizontal, vertical, and torsional contributions, significantly improved the results. Several coordinate systems were used for both static and dynamic analyses, with Fick coordinates showing a marginal (nonsignificant) advantage. Thus, during gaze fixations, recruitment within the neck muscles from which we recorded contributed primarily to position-dependent horizontal orientation terms in our data set, with more complex multidimensional contributions emerging during the head movements that accompany gaze shifts. These are crucial components of the late neuromuscular transformations in a complete model of 3-D head-neck system and should help constrain the study of premotor signals for head control during gaze behaviors.

Neck muscle synergies during stimulation and inactivation of the interstitial nucleus of Cajal (INC).

The interstitial nucleus of Cajal (INC) is thought to control torsional and vertical head posture. Unilateral microstimulation of the INC evokes torsional head rotation to positions that are maintained until stimulation offset. Unilateral INC inactivation evokes head position-holding deficits with the head tilted in the opposite direction. However, the underlying muscle synergies for these opposite behavioral effects are unknown. Here, we examined neck muscle activity in head-unrestrained monkeys before and during stimulation (50 muA, 200 ms, 300 Hz) and inactivation (injection of 0.3 mul of 0.05% muscimol) of the same INC sites. Three-dimensional eye and head movements were recorded simultaneously with electromyographic (EMG) activity in six bilateral neck muscles: sternocleidomastoid (SCM), splenius capitis (SP), rectus capitis posterior major (RCPmaj.), occipital capitis inferior (OCI), complexus (COM), and biventer cervicis (BC). INC stimulation evoked a phasic, short-latency ( approximately 5-10 ms) facilitation and later ( approximately 100-200 ms) a more tonic facilitation in the activity of ipsi-SCM, ipsi-SP, ipsi-COM, ipsi-BC, contra-RCPmaj., and contra-OCI. Unilateral INC inactivation led to an increase in the activity of contra-SCM, ipsi-SP, ipsi-RCPmaj., and ipsi-OCI and a decrease in the activity of contra-RCPmaj. and contra-OCI. Thus the influence of INC stimulation and inactivation were opposite on some muscles (i.e., contra-OCI and contra-RCPmaj.), but the comparative influences on other neck muscles were more variable. These results show that the relationship between the neck muscle responses during INC stimulation and inactivation is much more complex than the relationship between the overt behaviors.

Three-dimensional eye-head coordination after injection of muscimol into the interstitial nucleus of Cajal (INC).

The interstitial nucleus of Cajal (INC) is thought to be the "neural integrator" for torsional/vertical eye position and head posture. Here, we investigated the coordination of eye and head movements after reversible INC inactivation. Three-dimensional (3-D) eye-head movements were recorded in three head-unrestrained monkeys using search coils. INC sites were identified by unit recording/electrical stimulation and then reversibly inactivated by 0.3 mul of 0.05% muscimol injection into 26 INC sites. After muscimol injection, the eye and head 1) began to drift (an inability to maintain stable fixation) torsionally: clockwise (CW)/counterclockwise (CCW) after left/right INC inactivation respectively. 2) The eye and head tilted torsionally CW/CCW after left/right INC inactivation, respectively. Horizontal gaze/head drifts were inconsistently present and did not result in considerable position offsets. Vertical eye drift was dependent on both vertical eye position and the magnitude of the previous vertical saccade, as in head-fixed condition. This correlation was smaller for gaze and head drift, suggesting that the gaze and head deficits could not be explained by a first-order integrator model. Ocular counterroll (OC) was completely disrupted. The gain of torsional vestibuloocular reflex (VOR) during spontaneous eye and head movements was reduced by 22% in both CW/CCW directions after either left or right INC inactivation. Our results suggest a complex interdependence of eye and head deficits after INC inactivation during fixation, gaze shifts, and VOR. Some of our results resemble the symptoms of spasmodic torticollis (ST).