The orientation of the cervical vertebral column was studied by X-ray photography of the region containing the head and the neck in nine unrestrained species of vertebrates (man, monkey, cat, rabbit, guinea pig, rat, chicken, frog, lizard). In addition, the orientation of the horizontal semicircular canals was measured in four species using landmarks on the skull. In all vertebrates studied, with the exception of frog and lizard, the general orientation of the cervical vertebral column was vertical when animals were at rest, and not horizontal or oblique as suggested by the macroscopic appearance of the neck. The posture of the animal, whether lying, sitting or standing, had little effect on this general vertical orientation, although some variability was noticed depending on the species. This finding prompted the definition of a resting zone, where the cervical column can take any orientation within a narrow range around a mean position. The cervical vertebral column composes part of the S-shaped structure of the entire vertebral column, with one inflection around the cervico-thoracic (C7/Th1) junction. This feature is already noticable in the lizard. The vertical orientation of the cervical vertebral column is interpreted to provide a stable and energy saving balance of the head. Furthermore, when the head is lowered or raised, the atlanto-occipital and cervico-thoracic junctions are predominantly involved, while the entire cervical column largely preserves its intrinsic configuration. The curved configuration of the cervico-thoracic vertebral column embedded in long spring-like muscles is interpreted to function as a shock absorber. At rest, animals did not hold their heads with the horizontal canals oriented earth horizontally all the time, but often maintained them pitched up by ca. 5 deg, as has been reported for man. At other times, presumably when the vigilance level increased, the horizontal canals were brought into the earth horizontal plane. The vertical orientation of the cervical column results in a vertical positioning of the odontoid process of the axis (second cervical vertebra, C2), which thus provides the axis of rotation for yaw movements of the head. This axis corresponds to that of the horizontal semicircular canals. The vertical organization of the cervical vertebral column in birds and mammals, whether the animal is quadrupedal or bipedal, points to a common organizational principle for eye and head movement systems.(ABSTRACT TRUNCATED AT 400 WORDS)