Orienting head movements resulting from electrical microstimulation of the brainstem tegmentum in the barn owl

The size and direction of orienting movements are represented systematically as a motor map in the optic tectum of the barn owl (du Lac and Knudsen, 1990). The optic tectum projects to several distinct regions in the medial brainstem tegmentum, which in turn project to the spinal cord (Masino and Knudsen, 1992). This study explores the hypothesis that a fundamental transformation in the neural representation of orienting movements takes place in the brainstem tegmentum. Head movements evoked by electrical microstimulation in the brainstem tegmentum of the alert barn owl were cataloged and the sites of stimulation were reconstructed histologically. Movements elicited from the brainstem tegmentum were categorized into one of six different classes: saccadic head rotations, head translations, facial movements, vocalizations, limb movements, and twitches. Saccadic head rotations could be further subdivided into two general categories: fixed-direction saccades and goal-directed saccades. Fixed-direction saccades, those whose direction was independent of initial head position, were elicited from the midbrain tegmentum. Goal-directed saccades, those whose direction changed with initial head position, were elicited from the central rhombencephalic reticular formation and from the efferent pathway of the cerebellum. Particular attention was paid to sites from which fixed-direction saccadic movements were elicited, as these movements appeared to represent components of orienting movements. Microstimulation in the medial midbrain tegmentum elicited fixed-direction saccades in one of six directions: rightward, leftward, upward, downward, clockwise roll, and counterclockwise roll. Stimulation in and around the interstitial nucleus of Cajal (InC; a complete list of anatomical abbreviations is given in the Appendix) produced ipsiversive horizontal saccades. Stimulation in the ventral InC and near the dorsal and medial edges of the red nucleus produced upward saccades. Stimulation in the reticular formation near the lateral edge of the red nucleus produced downward saccades. Stimulation in the ventromedial central gray produced ipsiversive roll saccades. The metrics and kinetics of fixed-direction saccades, but not their directions, could be influenced by stimulation parameters. As such, direction was an invariant property of the circuits being activated, whereas movement latency, duration, velocity, and size each demonstrated dependencies on stimulus amplitude, frequency, and duration. The data demonstrate directly that at the level of the midbrain tegmentum there exists a three-dimensional Cartesian representation of head-orienting movements such that horizontal, vertical, and roll components of movement are encoded by anatomically distinct neural circuits.(ABSTRACT TRUNCATED AT 400 WORDS)