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

Keiko Meshida*, Stephen Lin, Daryl P. Domning, Paul Wang, Edwin Gilland

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

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 rectus muscles during other gaze changes.

Original languageEnglish
Pages (from-to)917-941
Number of pages25
JournalJournal of Anatomy
Volume238
Issue number4
DOIs
StatePublished - Apr 2021
Externally publishedYes

Keywords

  • accessory insertions
  • inferior oblique
  • ocular counter-rolling
  • superior oblique

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