Analysis of different forms of locomotor behavior in lamprey

Sammanfattning: The ability to locomote, that is move actively in space, is characteristic of the animal kingdom. Many species are capable of different forms of locomotion. They include forward and backward locomotion, fast and slow progression, etc. A general goal of this study was, by comparing three different forms of locomotion observed in the lamprey (a lower vertebrate), to estimate the similarities and distinctions of their control mechanisms. The main and well studied form of locomotion in the lamprey is fast forward swimming (FFS) based on periodical waves of lateral body flexion propagating from head to tail. The lamprey is also capable of two other forms of undulatory locomotion, slow forward swimming (SFS) and slow backward swimming (SBS). In the present study, it was shown that continuous tactile stimulation of a large area in the middle part of the body evokes SFS. By contrast, continuous tactile stimulation of a large area in the head or gill region causes SBS. Lesions of afferent inputs showed that sensory information critical for elicitation of SFS is transmitted through the dorsal roots in the middle part of the spinal cord. By contrast, sensory signals that induce SBS are transmitted not only through the dorsal roots in the gill region of the spinal cord but also through afferents of the lateral line nerves and trigeminal nerves. In the present study, the kinematical and electromyographic patterns of SFS and SBS were characterized and then compared with those of FFS. During SBS, the waves of lateral body undulations propagated from tail to head. The EMG bursts on the two sides alternated, and the EMG in more caudal segments led in phase the EMG in more rostral segments. During SFS, the waves of lateral body undulations propagated from head to tail. The EMG bursts on the two sides alternated, and the EMG in more rostral segments led in phase the EMG in more caudal segments. The most striking feature of SFS was non-uniformity of the shape and speed of locomotor waves propagating along the body: in the vicinity of the site of stimulation, the waves slowed down, and the body curvature increased several-fold due to the enhanced muscle activity. It was found that SFS and SBS have some important features in common. In both forms of slow swimming, the cycle duration was similar, and it was much longer than the cycle duration of FFS. Besides that, both SFS and SBS had a lower speed of progression and larger amplitude of head and tail excursions as compared to FFS. Another characteristic feature of both modes of slow swimming was the lack of stabilization of the body orientation in space, which differed from the very efficient stabilization of orientation during FFS. Taken together, these characteristic features of SFS and SBS suggest that these two modes of locomotion are not effective for long distance migrations. Instead, SFS and SBS can be used for escape and withdrawal behavior. Persistence of SFS and SBS after different lesions of the spinal cord suggests that the ascending and descending pathways, necessary for initiation of SBS and SFS, are dispersed over the cross-section of the spinal cord. A complete transection of the spinal cord did not abolish the generation of SBS rostral to the lesion, suggesting that SBS can be initiated from different levels of the spinal cord. Role of the spinal cord and the brainstem in generation of different forms of undulatory locomotion is discussed.