98 - Comparative Anatomy of the Circular Muscle Layers in Mammalian Orbit and Their Possible Functions

Poster Board Number: 98
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Abstract Body : Introduction and objective: This study further examines circular orbital muscles recently found both external and internal to the extraocular muscles (EOMs) in cetaceans (Meshida et al., 2020; doi: 10.1002/ar.24278). An External Circular Muscle (ECM) formed a cone-shaped, multi-layered smooth muscle sheet outside the rectus EOMs in all cetaceans examined except a juvenile sperm whale (USNM 594183 right), whose ECM comprised mixed layers of smooth and striated muscle. Cetaceans also had an Internal Circular Muscle (ICM) between the rectus EOMs and the retractor bulbi (RB). The ECM corresponds to the musculus orbitalis of Muller, while an ICM has not been described in non-cetacean species. This study examines 1) presence of striations in ECM/orbitalis of other mammals, 2) presence/absence of ICM in non-cetaceans, 3) functions of ECM and ICM.
Materials and methods: Twenty-five orbital specimens from 16 Families (2 Balaenopteridae, 3 Delphinidae, 1 Physeteridae, 1 Hippopotamidae, 2 Bovidae, 1 Cervidae, 1 Elephantidae, 1 Trichechidae, 1 Suidae, 2 Canidae, 5 Felidae, 1 Herpestidae, 1 Mephitidae, 1 Mustelidae, 1 Leporidae, 1 Macropodidae) were collected from Smithsonian National Museum of Natural History, Smithsonian National Zoological Park, Mercer County Wildlife Center NJ, and the Florida Fish and Wildlife Commission. Samples of the tissue layers external to the EOMs were taken from each specimen, sectioned, stained for histological analysis (H&E and Masson’s Trichrome) and photographed to evaluate presence and make-up of the ECM/orbitalis. Samples of tissue layers between the EOMs and the deeper RB muscle were likewise examined for evidence of an ICM.
Results: All species examined had an ECM/orbitalis muscle, ranging from minor sheets (e.g., rabbit, otter) to broad cones of muscle surrounding the EOMs (cetaceans, bovids). Except for sperm whale, ECM samples lacked striations and had elongated, centrally located nuclei, hence, were likely smooth muscle. The 3rd layer of ECM from the left orbit of a juvenile sperm whale had striations, consistent with samples from the right orbit of the same specimen in our previous study. The ICM in fin whale (USNM 594182) had striated fibers while similar muscles were absent in non-cetacean species except American bison (NZP 115107) and Scimitar horned oryx (NZP 113469). In these, muscle slips from the oblique EOMs spread between the rectus EOMs and the RB, like the cetacean ICM.
Conclusion: Skeletal fibers in sperm whale ECM may increase force or speed of ocular protrusion, extending the visual field where it is blocked by the rostrum and trunk. Except some primates, the bony orbit is generally open ventro-temporally, with orbital fascia contacting the temporalis muscle. The ECM/orbitalis is usually robust in this area, suggesting it helps protect orbital contents during mastication. As an ICM was found only in bison, oryx and cetaceans, it may be unique to cetartiodactyls. The ICM being continuous with the obliques in bison and oryx supports our hypothesis that the ICM of cetaceans arose from oblique EOMs.
Significance/implications: Rather than a minor smooth muscle as in humans, mammalian orbital muscles can be well-developed circular layers of smooth and skeletal muscle with diverse functions. To determine if striated contributions to ECM are unique to sperm whales, more cetacean taxa and life stages will be examined, while further sampling of Cetartiodactyla will pinpoint the origin of the ICM and illuminate its potential functions.