Correlated studies of sense organs and nerves of the lateral-line in living frog tadpoles. II. The trophic influence of specific nerve supply as revealed by prolonged observations of denervated and reinnervated organs

1948 ◽  
Vol 82 (2) ◽  
pp. 277-320 ◽  
Author(s):  
Carl Caskey Speidel
1972 ◽  
Vol 57 (2) ◽  
pp. 435-448 ◽  
Author(s):  
B. L. ROBERTS ◽  
I. J. RUSSELL

1. The activity of efferent neurones innervating lateral-line organs on the body of dogfish was followed by recording from filaments of cranial nerve X in 41 decerebrate preparations. 2. The efferent nerves were not spontaneously active. 3. Tactile stimulation to the head and body, vestibular stimulation and noxious chemical stimulation were followed by activity of the efferent nerves. 4. In contrast, natural stimulation of lateral-line organs (water jets) did not reflexly evoke discharges from the efferent fibres. 5. Reflex efferent responses were still obtained to mechanical stimulation even after the lateral-line organs had been denervated. 6. Electrical stimulation of cranial nerves innervating lateral-lines organs was followed by reflex activity of the efferent fibres. But similar stimuli applied to other cranial nerves were equally effective in exciting the efferent system. 7. Vigorous movements of the fish, involving the white musculature, were preceded and accompanied by activity of the efferent fibres which persisted as long as the white muscle fibres were contracting. 8. Rhythmical swimming movements were accompanied by a few impulses in the efferent fibres grouped in bursts at the same frequency as the swimming movements. 9. It is concluded that the efferent neurones cannot contribute to a feedback regulatory system because they are not excited by natural stimulation of the lateral-line sense organs. The close correlation found between efferent activity and body movement suggests that the efferent system might operate in a protective manner to prevent the sense organs from being over-stimulated when the fish makes vigorous movements.


The recognition of the morphological and developmental relationship of the vertebrate auditory organ and the lateral-line system of fishes and aquatic Amphibia rests on the foundation of a large volume of com­ parative researches. The main outlines of this generalization were already laid down forty years ago, and Cole’s work on the cranial nerves and lateral sense organs of fishes (1898) contains a comprehensive treatment of the history of the subject. The acustico-lateral or neuromast system embraces, in addition to the labyrinth and the lateral-line canals, the pit organs found to a greater or less extent in most fishes, the vesicles of Torpedo , and the ampullary canal system of Selachians and Holocephali. Concerning these Cole wrote: “The history of our knowledge of the phylogeny of the sensory canals is coincident with three discoveries—the discovery that the‘mucus’ canals contain sense organs, the discovery of Savi’s vesicles, and the dis­covery of the ampullae of Lorenzini.... We now know that all three types belong to the lateral line system, and I shall suggest that they represent three stages in the development of a canal—the most superficial condition, represented by the pit organs and Savi’s vesicles; the full development, represented by the canal; and the intermediate type, forming neither a Savi vesicle nor yet a canal, represented by the ampullae of Lorenzini” (p. 187). This conception has remained valid to the present day. The ampullae of Lorenzini, with which I am here principally concerned, are briefly described in current text-books as transitional or specialized neuromasts, and the implication always is that structurally and functionally they do not differ significantly from the neuromasts of the lateral-line canals. For example, in their recent exhaustive treatise on the vertebrate nervous system Kappers, Huber and Crosby (1936) state with reference to the lateral-line canals, the Savi vesicles and the ampullae of Lorenzini: “thus in the various animals there is a transition between an open and a closed system for perceiving vibrations" (p. 438).


For a long time after their discovery in the seventeenth century the lateral-line canals of fishes were considered to be mucus-secreting organs. In 1850 Leydig described sense organs in the lateral-line canals, and this discovery stimulated a keen interest in the investigation of both the morphological and functional features of the lateral-line system. Morphological studies have yielded a thorough understanding of the structure of these organs (Ewart and Mitchell 1892; Cole 1896; Johnson 1917; von Woellwarth 1933). Physiological studies, though numerous, have been less fruitful. An account of the older work was given by Baglioni (1913), and the more recent work is reviewed by Dykgraaf (1933). The only technique until recently available has been the elimination of the sensory system by nerve section and cauterization, and the comparison of the behaviour of intact and operated fishes in response to various stimuli. With so diffuse a structure as the lateral-line system, receiving its nerve supply from the fifth, seventh, ninth and tenth cranial nerves, this method is particularly inadequate, and involves a violent mutilation of the animal. When one considers the crudity of many of these operations, it is not the uncertainty of the results which is remarkable, but rather that some of the conclusions reached should remain valid to-day in the light of far more penetrating experimental analysis. This method of organ elimination could yield at best only an indication of the kind of stimulus that is effective in evoking the excitation of lateral-line receptors. In current textbooks the conclusion of Parker (1904) that the effective stimulus for the lateral line is low-frequency vibration, and that of Hofer (1907) that it is movement of water (i. e. local currents) have received most notice. The observations of Dykgraaf (1933), who employed the more refined methods of von Frisch’s futterdressur technique, support Hofer’s conclusion, and to some extent also Parker’s. Dykgraaf considers the lateral-line system to be an organ of Ferntastsinn , and if this is taken to mean a mechanoreceptor of such sensitivity that it can function both as a touch organ and as a receptor for disturbances coming from a distance, it is undoubtedly a true description, for it is fully confirmed by the direct electrophysiological studies of Hoagland (1933 a, b, c and d ) and of Schriever (1935). The latter, apparently unacquainted with Hoagland’s work, did little more than to confirm several of his observations.


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