The mechanosensory lateral line system: morphological, physiological, and behavioral study in pre- and post-metamorphic lampreys

Abstract

Lampreys are extant jawless vertebrates. The oldest lamprey-like fossil, which dates from approximately 360 million years ago, exhibits many external morphological similarities with modern lampreys. It is thought that lampreys have undergone very conservative evolutionary changes and therefore retain many ancestral characters. Studying lamprey sensory physiology may shed light on the phylogenetic development of various sensory systems in vertebrates. Electrophysiological and microscopic methods were used to investigate the morphology and physiology of the peripheral lateral line system of lampreys with special emphasis on the metamorphic changes. It was established that larval lampreys possess a functional mechanosensory lateral line system. Morphology of larval neuromasts was found to be similar to that of adults. Metamorphic transformations in the lateral line included functional and morphological changes. A general re-patterning of the system of neuromasts on the head and trunk was observed. It appears that three processes are involved in the re-patterning: an increase in neuromasts number, their re-distribution within the pit lines, and shifts of the pit lines relative to external features. Response of the trunk lateral line nerve (TLLN) fibers to vibrational stimulation was qualitatively similar in adults and larvae. Both showed two populations of neurons responding to opposite directions of water flow, with the response magnitude monotonically increasing with stimulus amplitude. At low frequencies, the phase lag of the response with respect to the stimulus maximum was approximately 220, and the gain depended approximately linearly on frequency, confirming the notion that superficial neuromasts are velocity detectors. The changes in phase lag with increasing stimulus frequency were steeper in larva suggesting slower conductance. The response of adults to different frequencies indicated a narrower range of frequency discrimination. The observed changes were hypothesized to be of preparatory nature, as the metamorphosis is in general, making this sensory system more suitable for the active life style of adult lampreys. In light of this hypothesis, the behavioral involvement of the lateral line in locomotion was investigated. It was found that the locomotion of lamprey in still water was not affected by blocking the lateral line. This may indicate that the intraspinal system of mechanoreceptors, so called 'edge' cells, is dominating locomotor feedback during such experimental conditions and is sufficient for normal locomotion. However, the question remains unanswered whether the movement-related feedback from the 'edge' cells is sufficient in complex flow conditions. It may very well be that the information provided by the lateral line in such demanding conditions is necessary for swimming. Thus the behavioral function of the lamprey lateral line remains unknown.