Spatial orientation in the lamprey. I. Control of pitch and roll

Two major tasks must be fulfilled during locomotion: propulsion and spatial orientation. In the lamprey, the propulsive force is generated by laterally directed body undulations propagated from the rostral to the caudal end of the body. The neuronal networks underlying this basic locomotor pattern have been described in considerable detail. The present study was undertaken to provide the necessary behavioural background for parallel studies of the vestibular neuronal networks responsible for spatial orientation during locomotion. The following results were obtained. 1. The lamprey actively stabilized its pitch angle during swimming and usually kept a linear trajectory in the sagittal plane, despite large changes in the speed of swimming. During repeated tests, a certain preferred pitch angle could be maintained over a period of several minutes, even if the initial starting angle of the animal was changed considerably. 2. Two different strategies were observed for active turning in the downward direction: a smooth turn accomplished by weak ventral flexion of the whole body, and a sharp turn accomplished by localized ventral flexion of a region of the body just posterior to the gills. 3. The lampreys were oriented with the dorsal side up while swimming at any pitch angle. The control systems for pitch and roll can thus operate independently. When swimming, lampreys kept the tail region flexed somewhat ventrally. This body configuration will cause lateral movements of the tail to generate a torque that rotates the body around its longitudinal axis. This mechanism is presumably used to correct deviations from the dorsal-side-up orientation. After amputation of the dorsal and tail fins, lampreys maintained a proper spatial orientation during swimming. 4. After a unilateral labyrinthectomy, swimming lampreys continuously rolled towards the lesioned side. Unilaterally labyrinthectomized animals displayed a tonic twisting of the body into a helical shape. This presumably represents an additional strategy for performing roll turns. Bilaterally labyrinthectomized animals never maintained a linear trajectory in any plane, but turned continuously in all directions.