The oblique extraocular muscles in cetaceans: Overall architecture and accessory insertions

Abstract

The oblique extraocular muscles (EOMs) were dissected in 19 cetacean species and 10 non‐cetacean mammalian species. Both superior oblique (SO) and inferior oblique (IO) muscles in cetaceans are well developed in comparison to out‐groups and have unique anatomical features likely related to cetacean orbital configurations, swimming mechanics, and visual behaviors. Cetacean oblique muscles originate at skeletal locations typical for mammals: SO, from a common tendinous cone surrounding the optic nerve and from the medially adjacent bone surface at the orbital apex; IO, from the maxilla adjacent to lacrimal and frontal bones. However, because of the unusual orbital geometry in cetaceans, the paths and relations of SO and IO running toward their insertions onto the temporal ocular sclera are more elaborate than in humans and most other mammals. The proximal part of the SO extends from its origin at the apex along the dorsomedial aspect of the orbital contents to a strong fascial connection proximal to the preorbital process of the frontal bone, likely the cetacean homolog of the typical mammalian trochlea. However, the SO does not turn at this connection but continues onward, still a fleshy cylinder, until turning sharply as it passes through the external circular muscle (ECM) and parts of the palpebral belly of the superior rectus muscle. Upon departing this “functional trochlea” the SO forms a primary scleral insertion and multiple accessory insertions (AIs) onto adjacent EOM tendons and fascial structures. The primary SO scleral insertions are broad and muscular in most cetacean species examined, while in the mysticete minke whale (Balaenoptera acutorostrata) and fin whale (Balaenoptera physalus) the muscular SO bellies transition into broad fibrous tendons of insertion. The IO in cetaceans originates from an elongated fleshy attachment oriented laterally on the maxilla and continues laterally as a tubular belly before turning caudally at a sharp bend where it is constrained by the ECM and parts of the inferior rectus which form a functional trochlea as with the SO. The IO continues to a fleshy primary insertion on the temporal sclera but, as with SO, also has multiple AIs onto adjacent rectus tendons and connective tissue. The multiple IO insertions were particularly well developed in pygmy sperm whale (Kogia breviceps), minke whale and fin whale. AIs of both SO and IO muscles onto multiple structures as seen in cetaceans have been described in humans and domesticated mammals. The AIs of oblique EOMs seen in all these groups, as well as the unique “functional trochleae” of cetacean SO and IO seem likely to function in constraining the lines of action at the primary scleral insertions of the oblique muscles. The gimble‐like sling formed by SO and IO in cetaceans suggest that the “primary” actions of the cetacean oblique EOMs are not only to produce ocular counter‐rotations during up‐down pitch movements of the head during swimming but also to rotate the plane containing the functional origins of the rectu...

The unique rectus extraocular muscles of cetaceans: Homologies and possible functions

“…This indicates that the combination of function of the massive palpebral bellies of the rectus muscles, the ECM (orbitalis), and the palpebral grooves on the eyelid are all involved in moving the entire orbital region in cetaceans. Also, the dorso‐ventrally located palpebral grooves provide additional flexibility for upward‐downward movement of the eyeball facilitated by SO and IO, which supports our hypothesis that oblique muscles are mainly responsible for moving the eyeball (incyclotorsion and excyclotorsion, or inward rotation and outward rotation) together with the fused palpebral rectus EOMs (Meshida et al, 2021).…”

“…Scleral bellies and insertions of rectus EOMs in most cetaceans are small in comparison to the palpebral ones, with thin fibrous tendons inserting into the anterior hemisphere of the globe close to the equator (widest point) of the eyeball. The insertion of the scleral belly of superior rectus (SR) is anterior (on conjunctival side) to the scleral insertion of superior oblique (SO), while that of the scleral belly of inferior rectus (IR) is posterior (on apical side) to the scleral insertion of IO (Meshida et al, 2021, figs 4 and 7). There is a tendency for the scleral bellies of rectus EOMs to be more fibrous in baleen whales than in smaller toothed whales.…”

“…The rectus extraocular muscles (EOMs) of mammals, and vertebrates generally, insert onto the sclera of the eye to effect ocular rotations. In addition to these scleral insertions, the four rectus EOMs in cetaceans have large, fleshy palpebral insertions that spread into the deep surface of the upper and lower eyelids (Figure 1 and see Meshida et al, 2020, 2021). The unusual cetacean palpebral rectus divisions have been known at least since the time of John Hunter's Observations on the structure and oeconomy of whales (Hunter, 1787).…”

“…He termed these palpebral insertions as ‘ dilatores of the eyelids’ and gave functional names also to the scleral portions of the rectus muscles, calling them collectively the ‘interior straight muscles’ and separately, the ‘elevator, depressor, adductor and abductor’ muscles of the eye (Hunter, 1787). He also gave clear accounts of the oblique EOMs (Meshida et al, 2021) and the retractor bulbi muscles (Meshida et al, 2020), though without naming the latter as such. Richard Owen confirmed and clarified Hunter's results in editorial notes added to a republication of Hunter's papers (Hunter, 1840).…”

“…Of particular importance is the presence of both global and orbital insertions of EOMs demonstrated in humans and a variety of laboratory animals. An overview of current understanding of human EOMs and their pulley system is summarized elsewhere (Demer, 2017; Meshida et al, 2021). The globe is surrounded by a dense, elastic fibrovascular connective tissue called Tenon's capsule (fascia bulbi) which also invests the anterior (distal) portions of the EOMs (Dutton, 2011; Fink, 1962).…”