The orientation of the cervical vertebral column in unrestrained awake animals. II. Movement strategies.

Previously we demonstrated a stereotyped resting posture of the head-neck arrangement in a number of vertebrates: the cervical vertebral column is oriented vertically to form one portion of the partial S-shaped configuration of the entire spine. The present investigation quantified the various strategies of head-neck movements employed by different mammalian species (human, monkeys, cats, rabbits and guinea pigs) using cineradiography. At rest, bipeds and quadrupeds hold their heads at the extreme point of flexion of the passive atlanto-occipital range of motion. In this posture, the horizontal semicircular canals are tilted upward from earth horizontal by 5 to 10 degrees and roughly parallel the plane determined by the two obliquus capitis posterior muscles. Furthermore, at this head position, the utricular maculae become oriented earth-horizontally. In quadrupedal animals, head-neck movements in the sagittal plane result from movement at the atlanto-occipital articulation (head/C1) and at the multi-articular cervico-thoracic junction (C6-Th3). Only very small flexion/extension movements occur within the body of the cervical vertebral column (C2-C5). Lowering the head from the resting position is only possible by flexion at the C6-Th3 vertebrae. Raising of gaze from the resting position is only possible by extension of the head at the atlanto-occipital articulation. By contrast, sagittal plane head movements in bipeds are largely confined to the cervico-thoracic junction. This is related to a significantly reduced range of motion of the atlanto-occipital articulation. In monkeys and humans, it range of motion is about 13 and 8-11 degrees, respectively, compared to 105 degrees in rabbits. Our cineradiographic data demonstrated different strategies for head movements in the sagittal plane between quadrupeds and bipeds. At one end of the spectrum, in the case of rabbits, there was no systematic relationship between head and neck orientation. Rabbits stabilized head posture by using the head-neck structure in a parallelogram fashion, which resulted in head posture being largely independent of cervical vertebral column orientation. In monkeys and humans, however, orientation of the head depended almost entirely on the orientation of the cervical vertebral column. In such case, head movements in the sagittal plane almost exclusively relied on the positioning of the cervico-thoracic junction. These different strategies again correlate with the different ranges of motion of the atlanto-occipital articulation. We suggest that vertebrates use mechanical constraints and preferred planes of action for head-neck movement control to simplify sensory-motor transformations subserving motor control and plasticity and to minimize neuronal operations.