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.