Spatial orientation of extraocular muscle EMG responses to tilt in the rabbit during postnatal development

Unanaesthetized pigmented rabbits 2-45 days of age were gradually tilted (15 degrees steps) over 360 degrees around three orthogonal body axes. The multiunit electromyogram activity of superior rectus (SR) and superior oblique (SO) extraocular muscles was recorded with chronically implanted pairs of fine wire electrodes after each tilt step. The integrated EMG activity of the extraocular muscles in response to static tilt stimulation was trigonometrically related to tilt angle in all age groups. Each eye muscle was characterized by a typical locus of tilt positions which resulted in maximum integrated EMG activity. This locus was described by a vector of tonic vestibular activation (TVA) within the head coordinate system. The orientation of these TVA vectors within the coordinate system of the rabbit's head and, therefore, the coordination of tonic eye muscle activation in response to the position of the animal in the gravitational field did not change with postnatal age in the rabbit. Therefore, eye muscles are already capable of responding to static vestibular stimulation for the stabilization of gaze when visual information becomes available to the rabbit pups. The EMG responses to static tilt stimulation were principally determined by the scalar product of the gravity vector and the muscle's TVA vector. The response of the extraocular muscles to this effective gravitational stimulus was unchanged during the postnatal development of the rabbit: excitatory stimuli resulted in an approximately linear increase of the integrated EMG activity, inhibitory stimuli resulted in a smaller decrease to a minimum value. The correlation between the effective strength of excitatory gravity stimuli and the EMG activity of the extraocular muscles increased significantly at the time of postnatal eye opening. Since the strongest responses of SR and SO to static tilt were observed in intermediate roll-pitch positions that correspond closely to the planes of the vertical semicircular canals, a common reference frame for the cooperation of maculo-ocular and ampullo-ocular reactions is suggested.