Innervation of the medial rectus muscle in the ratfish,Hydrolagus colliei

Abstract

Oculomotor organization in elasmobranch fish (sharks, skates, and rays) differs from that in other vertebrates in that the medial rectus muscle is innervated by contralateral rather than ipsilateral motoneurons. Distinguishing whether this innervation pattern is unique to the elasmobranchs, or is the ancestral pattern for cartilaginous fishes, requires examination of a representative of the sister group to the elasmobranchs, the holocephalans (ratfish). In the present study, the innervation pattern of the medial rectus was examined in a ratfish, Hydrolagus colliei, by using biotinylated dextran amines (BDA, 3,000 MW). Labeled cells were revealed in the contralateral oculomotor nucleus. Therefore, an innervation pattern in which the medial rectus muscle is innervated by contralateral motoneurons is the primitive condition for cartilaginous fishes.

Evolution and Development of Extra-Ocular Nerves and Muscles in Vertebrates

“…Likewise, we can assume that a counteraction occurs between SR/IR whereas the counteraction should be between the NR/LR. The detail of this connection remains to be determined in chondrichthyans and lungfish [11][12][13].…”

“…Among teleosts, frogs, birds, and mammals each have a specific pattern of innervation by vestibular inputs [1,4,17,42,45]. By contrast, studies in chondrichthyans (cartilaginous fishes) revealed a different pattern with a combination of ipsilateral and contralateral nerve fibers [11,12]. Many details of vestibular relationships are incomplete in lampreys (which lack a horizontal canal) but can be compared to the pattern of connections in gnathostomes [42,43,[46][47][48].…”

“…In contrast to gnathostomes, chondrichthyans and lungfish (Fig. 1) show a dorsal branch around the optic nerve to innervate the superior rectus and the nasal rectus (NR) whereas only two ventral branches form the inferior rectus and inferior oblique innervation [11][12][13]16,54]. Among tetrapods, Latimeria and teleosts exhibit one branch that passes dorsal to the optic nerve to reach the superior rectus [9,16,19,31], which is innervated from the contralateral cranial nerve CNIII [19,36,52,55,56].…”

“…The ages of different lines are indicated as approximations in millions of years. Assembled from [4,8,9,[11][12][13]20,22,23,27,31,32,71,75,76].…”

“…Chondrichthyans are well described and have the simplest connections between the vestibular output and the ocular motor neurons [11,12]. A few things are different about the vestibular organization and the utricle that indicates a separation between chondrichthyans and lungfish [13] and the remaining gnathostomes [44,45]; it evolved an anterior and a posterior branch within elasmobranchs [11,145].…”