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Journal of Experimental Biology, Vol 198, Issue 12 2581-2591, Copyright © 1995 by Company of Biologists

JOURNAL ARTICLES

Initiation of locomotion by lateral line photoreceptors in lamprey: behavioural and neurophysiological studies

T Deliagina, , F N, M Gonzalez, H Ehrsson, G Orlovsky and S Grillner

The lateral line system of lampreys includes photoreceptors distributed in the skin of the tail region. These are innervated by the trunk lateral line nerves, and the afferents terminate bilaterally in the medial octavolateral nucleus, crossing the midline through the cerebellar commissure. Stimulation of the dermal photoreceptors by tail illumination initiates locomotion. The present study was performed to characterize the response to illumination in larval and adult lampreys in detail and to elucidate the neuronal pathways responsible for the activation of locomotion. In both larval and adult quiescent lampreys, the response to unilateral illumination of the tail was found to consist of an initial turn followed by rectilinear swimming. The sign and magnitude of the turning angle were not correlated with the laterality of the optic stimulus. In mechanically restrained lampreys, spinalized at the level of segments 15&shy;20, tail illumination evoked a complex motor response in the rostral part of the body, with switches between different patterns of coordination (turns in different directions, locomotion, and turns combined with locomotion). Thus, the response to tail illumination is not a simple reflex, but includes a behavioural choice. Reticulospinal neurones play a crucial role in the initiation of locomotion in lampreys. The response to unilateral tail illumination in rhombencephalic reticular cells was studied with extracellular single-unit recordings. It was found that neurones in the middle and posterior rhombencephalic reticular nuclei were activated bilaterally. Tonic activity or slow bursts (<0.5 Hz) were evoked, in some cases lasting up to 60 s after the stimulation. The response remained bilateral after transection of one lateral line nerve and the cerebellar commissure. Afferents from one side can thus activate reticulospinal cells on both sides through a pathway outside the cerebellar commissure. This bilateral activation of reticulospinal neurones is presumably responsible for the activation of spinal locomotor networks, without any directional bias to the left or the right side, and for the rectilinear swimming observed in behavioural experiments. In the caudal part of the termination area of the lateral line nerve afferents, neurones with contralateral projections were retrogradely stained with horseradish peroxidase. These neurones appear to be likely candidates for mediating the contralateral effects of the lateral line fibres.

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