End buds: non-ampullary electroreceptors in adult lampreys

Summary

Shared anatomical and physiological characters indicate that the low-frequency sensitive electrosensory system of lampreys is homologous with those of non-teleost fishes and amphibians. However, the ampullary electroreceptor organs which characterize all of these gnathostomes are not found in lampreys. Experimental anatomical and physiological studies reported here demonstrate that the epidermal end buds are the electroreceptors of adult lampreys.

End buds, consisting of both sensory and supporting cells, are goblet-shaped with the top (25–60 μm diameter) at the epidermal surface and the stem directed toward the dermis (Fig. 1A). Short lines or clusters of 2–8 end buds (Fig. 1B) are distributed over both trunk and head. Injections of horseradish peroxidase (HRP) into vitally-stained end buds labeled anterior lateral line afferents terminating in the ipsilateral dorsal nucleus (Fig. 2A) — the primary electrosensory nucleus of the lamprey medulla. Conversely, after HRP injection into the dorsal nucleus HRP-filled fibers and terminals were present on ipsilateral end buds (Fig. 2B).

End buds are usually not visible without staining. However, in adult sea lampreys the presence of end buds was histologically confirmed in skin patches containing the receptive fields of electroreceptor fibers recorded in the anterior lateral line nerve. Additionally, in the rare instance of two silver lampreys in which end buds were visible without staining, electrosensory activity indistinguishable from that of the primary electroreceptor afferents was recorded from the end bud surface (Figs. 3, 4).

End buds were initially characterized as chemoreceptors (Johnston 1902) but were later correctly advanced as lateralis receptors based on the presence of presynaptic dense bodies in the receptor cells (Whitear and Lane 1981). Unlike all other low-frequency electroreceptors, end buds lack canals. The receptor cells contact the epidermal surface and possess apical microvilli rather than the kinocilium of most gnathostomes with homologous electrosensory systems of the primitive (non-teleost) type.

Larval lampreys and newly transformed adults lack end buds although at least the latter are electroreceptive. End buds, therefore, may be the form taken by electroreceptors only in the final portion of a lamprey's life.