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Marine Biological Laboratory, Woods Hole, Massachusetts 02543
In vertebrates, primary vestibular afferents from the semicircular canals are linked to extraocular motoneurons by second-order vestibular neurons, which reflect a functional compartmentalization and topographic organization of hindbrain segments during development (1–4). Since the overall patterning of hindbrain segments is specified by the expression of particular genes (5), segmental segregation of second-order vestibular neurons suggests evolutionary relationships between specific oculomotor behaviors and the expression of particular genetic regulatory elements (e.g., a particular Hox gene (6)). Accordingly, neurons arising from the same hindbrain segment should always be correlated with a given oculomotor behavior regardless of species (3). However, the neurons subservient to horizontal eye movements in cartilaginous fishes (sharks, skates, and rays) are asserted, by some, to be organized quite differently from those of other vertebrates (7–9).
Anatomical studies of extraocular motoneurons in the adults of elasmobranch species have uniformly demonstrated that medial rectus (MR) muscle innervation is contralateral, as compared with ipsilateral in all other vertebrates (7,10,11), including an eye muscle similarly located in the lamprey orbit (9). On the other hand, innervation of the lateral rectus (LR) muscle is ipsilateral in elasmobranches, just as it is in all other vertebrates (Fig. 1). The contralateral innervation of the MR, taken with the ipsilateral innervation of the LR, has suggested that vertical axis second-order vestibuloocular reflex (VOR) pathways in elasmobranchs must be realized in another way than shown for most vertebrates in Figure 1 (7). In addition, labeling of the oculomotor nucleus withhorseradish peroxidase conjugates failed to demonstrate the existence of other afferent projections from the hindbrain (8), such as the excitatory abducens internuclear neurons (Abd Int) and prepositus neurons, both of which are essential for achieving symmetric conjugate horizontal motion of both eyes during saccades, fixation, and visual tracking (12–15).
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First, however, the precise anatomical configuration of the central horizontal oculomotor system in elasmobranchs must be analyzed in rigorous structure/function experimental paradigms. This study was meant to locate the neurons projecting to the oculomotor nucleus of the lesser spotted dogfish, Scyliorhinus canicula, by applying biocytin to either the oculomotor nuclei or the medial longitudinal fasciculus (MLF). Animals were anesthetized with 0.05% ethyl-aminobenzoate until respiration ceased. After cartilage removal, the rostral cerebellum was aspirated to visualize the hindbrain at the level of the anterior medullary velum. Either the right MLF or caudal oculomotor nucleus was cut (n = 6 and 4, respectively), and biocytin crystals were applied for 20 min. Cartilage was replaced, the skin was tightly sutured, and the animals were resuscitated. They were again anesthetized after 48–72 h and perfused with 4% formaldehyde and 0.5% glutaraldehyde. The midbrain and hindbrain were dissected out, gelatin embedded, and sectioned at 75 µm. The sections were processed with the use of the avidin-biotin peroxidase complex including NiCo intensification (18).
In all cases, many heavily labeled vestibular neurons were found in the contralateral descending/posterior octaval subnucleus (Fig. 2A) and ipsilateral anterior octaval subnucleus (not illustrated). However, in all experiments, neurons were distributed throughout the contralateral hindbrain from the dorsal to ventral surface (Fig. 2B, D). In particular, a distinct subgroup of neurons largely ventrolateral to the abducens nucleus (Fig. 2E) was reminiscent of the contralateral abducens internuclear neurons described in all other vertebrates (Fig. 1). Neurons were also distributed dorsally up to, and surrounding, the MLF; these neurons could be envisioned as analogous to the prepositus nucleus described in mammals. Clearly, neurons ipsilateral to either the oculomotor or MLF biocytin label were either sparse or absent (Fig. 2C, F). Significant terminal arborization appeared throughout the ipsilateral Abd nucleus (Fig. 2F) that conceivably derived from axon collaterals of ascending vestibular neurons. If so, then individual vestibular neurons might contact a pair of synergistic horizontal extraocular motoneurons (see Fig. 1). Neurons were also found in the pretectum, midbrain, and cerebellar nuclei that are, in all probability, correlated primarily with vertical eye movements and gaze (not illustrated). Overall, the distribution pattern of neurons throughout the brainstem of the elasmobranchs was surprisingly more extensive than expected and only different in anatomical detail from that observed in other vertebrates (6,19–21).
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This work was supported by the Grass Foundation (W. Graf, M. McFarlane, and E. Gilland) and NIH Research Grants (R. Baker).
Literature Cited
This article has been cited by other articles:
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  O. A. Masseck and K.-P. Hoffmann Responses to Moving Visual Stimuli in Pretectal Neurons of the Small-Spotted Dogfish (Scyliorhinus canicula) J Neurophysiol, January 1, 2008; 99(1): 200 - 207. [Abstract] [Full Text] [PDF]
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