Neural mechanisms for the visual control of spatial orientation and locomotion : electrophysiological and behavioural studies of the supraspinal control of posture and steering in the lamprey central nervous system, with reference to visuo-motor mechanisms

Abstract

Neural mechanisms for the supraspinal control of posture and steering, in particular visuo-motor control and visuo-vestibular interaction in postural control, were investigated, using the lamprey as a model system. Behavioural experiments on intact and chronically lesioned animals, intra- and extracellular recordings in vitro and retrograde staining of neurons with horseradish peroxidase were utilized.

Lampreys actively stabilize their orientation in the vertical planes. The roll control system normally stabilizes a dorsal-side-up orientation of the animal, whereas the pitch control system can stabilize different angles of upward/downward swimming. Turns upwards and downwards are performed by a dorsiflexion or ventroflexion of the body, respectively. Lateral movements of the ventroflexed tail region is presumably an important mechanism for corrective roll turns. Vestibular input plays a crucial role for the stabilization of orientation: unilaterally labyrinthectomized animals roll continuously towards the lesioned side, whereas bilaterally labyrinthectomized animals turn continuously in all directions. Illumination of one eye evoked a horizontal turning movement away from light (negative phototaxis) and a dorsal light response, that is a roll tilt of the whole animal towards the light. The responses were seen both in quiescent animals, attached with their sucker mouths, and during locomotion. The visuo-motor pathways mediating the responses were investigated by chronic lesions. The contralateral pretectal region was found to play a major role for both dorsal light response and negative phototaxis, whereas bilateral ablation of tectum enhanced the responses. The crossed pretecto-reticular projection is crucial for dorsal light response, whereas the non-crossed projection is most important for negative phototaxis.

At a rostral spinal level, fibres for yaw turns and negative phototaxis course mainly in the lateral columns, whereas fibres for roll control and dorsal light response travel mainly more medially. Neural correlates of the dorsal light response were investigated by recording visual and vestibular responses in reticulospinal neurons, which form the major descending motor control system in lamprey. In the absence of visual stimulation, vestibular input induced an approximately equal activation of reticulospinal cells on the left and right side in the dorsal-side-up orientation (the set-point of the system). Any asymmetry in the reticulospinal activity will evoke a correcting roll turn, tending to restore the orientation with symmetrical activity.

Vestibular responses were strongly affected by the visual stimulation. Optic nerve stimulation potentiated ipsilateral vestibular responses and depressed contralateral responses, so that the set-point was shifted towards the stimulated side. The potentiation induced by optic nerve stimulation could last up to 2 hours. Intracellular recordings showed that around 50% of the studied reticulospinal neurons were potentiated. A likely mechanism for the long-lasting potentiation is increased excitability in visuo-vestibular interneurons projecting to the reticulospinal cells. Lampreys have lateral line skin photoreceptors in the tail. Tail illumination evoked locomotion without any preferential orientation relative to the source of light. Extracellular recordings in a semi-intact preparation showed that tail illumination activates reticulospinal cells bilaterally, which presumably in turn activates the spinal networks for locomotion. The bilateral activation presumably occurred due to bilateral projections both of the primary lateral line afferents and of secondary sensory neurons in the octavolateral area. Candidate neurons of the latter type were characterized morphologically after retrograde staining with HRP.