The Organization of the Octavolateralis Area in Actinopterygian Fishes: A New Interpretation

The octavolateralis area of actinopterygian fishes can be subdivided into a dorsal lateralis area composed of first-order lateral line nuclei, and a ventral octavus area composed of nuclei receiving first-order input from the eighth nerve. Three patterns of organization of the lateralis area are recognized in the present study. The organization of this area in polypteriforms and chondrosteans is similar to that in chondrichthyans. On the basis of recent studies in chondrichthyans (McCready and Boord, '76; Boord and Campbell, '77; Bodznick and Northcutt, '80), it is hypothesized that this pattern reflects the subdivision of the lateral line system into mechanoreceptive and electroreceptive portions. As petromyzontid agnathans also share this pattern of organization, it is hypothesized that they are electroreceptive. The lateralis area of holosteans and nonelectroreceptive teleosts exhibits a second organizational pattern that is hypothesized to reflect the loss of the electroreceptive portion of the lateral line system; it is suggested that electroreception was lost sometime between the chondrostean and teleostean radiations. Each group of electroreceptive teleosts is believed to have evolved electroreception independently (Bullock, '74), a situation that is reflected centrally by a third organizational pattern within the lateralis area, which is distinctly different from that of early radiations of electroreceptive fishes. The octavus area of actinopterygians exhibits two patterns of organizationthat of polypteriforms, chondrosteans, and holosteans, and that of teleosts. The functional significance of these patterns has yet to be elucidated. Since the classic anatomical studies of Pearson ('36a,b), Larsell('67), and others on the octavolateralis (acousticolateralis) area of fishes, there has been a substantial increase in information concerning the sensory systems that have primary projections to this area, and traditional notions of the functional nature of these sensory systems -the otic endorgans and the lateral line system are being reexamined. For example, whereas the labyrinth of most fishes was once thought to contain only vestibular endorgans, it is now known to serve an auditory function in chondrichthyans and actinopterygians (e.g., see reviews by Popper and Fay, '77; Fay and Popper, '80). Furthermore, the importance of the mechanoreceptors of the lateral line (lateralis) system as auditory endorgans (as they are often classified) can be questioned on the basis of recent studies that, taken together, suggest that they may be responsive to a class of stimuli biologically distinct from sound (Dijkgraaf, '63, '67; Schwartz, '67; Cahn, '72; Pitcher et al., '76; Partridge and Pitcher, '80; Sand, '81). In addition, the lateralis system of certain fishes can be considered to include the electroreceptors, a class of endorgans discovered only within the past 20 years (Lissman and Machin, '58; Bullock et al., '61), and thus not considered in much of the literature dealing with the anatomy and evolution of the octavolateralis area. Thus, as many as four classes of sensory endorgans can be grouped within the octavolateralis system: the auditory and vestibular endorgans of the labyrinth, innervated by the octavus (eighth) nerve, and the mechanoreceptive lateralis endorgans and electroreceptors, innervated by various components of the anterior and posterior lateralis nerves in different taxa. C.A. McCormicks present address is Department of Anatomy, Georgetown University Schools of Medicine and Dentistry, 3900 Reservoir Rd, NW, Washington, DC 20007. 0362-2525/82/1712-0159$06.50