Architecture and Function of Orbitalis and Oblique Eye Muscles in Mammals

Introduction and objectives: The basic plan of ocular anatomy, innervation and function is highly conserved among vertebrates. However, our study on mammalian orbits has revealed considerable variation such as a well-developed multi-layered orbitalis muscle (external circular muscle, ECM) investing the extraocular muscles (EOMs) externally, an internal circular muscle (ICM) coursing between the internal surface of the rectus EOMs and retractor bulbi (RB) found in cetaceans and elaborate oblique EOM scleral insertions in certain groups of carnivores. This study will present these new anatomical findings and discuss their possible functions.
Materials and methods: Thirty-six orbital specimens from 18 Families (2 Balaenopteridae, 3 Delphinidae, 1 Physeteridae, 1 Hippopotamidae, 2 Bovidae, 1 Cervidae, 1 Elephantidae, 1 Trichechidae, 1 Suidae, 2 Canidae, 7 Felidae, 1 Herpestidae, 1 Mephitidae, 7 Mustelidae, 1 Procyonidae,1 Leporidae, 1 Macropodidae, 1 Didelphidae) were collected from Smithsonian National Museum of Natural History, Smithsonian National Zoological Park, Mercer County Wildlife Center, Florida Fish and Wildlife Commission, Virgina Department of Wildlife Resources, and Wildlife Futures Program University of Pennsylvania School of Veterinary Medicine. Samples from 25 specimens were taken from the tissue layer external to the EOMs corresponding to the ECM/orbitalis, sectioned and stained for histological analysis (H&E and Masson’s Trichrome).
Results: All specimens examined had an ECM/orbitalis muscle ranging from minor sheets of muscle to multi-layered cone-shaped muscles surrounding the external surface of the EOMs. Lack of striation in histology suggested that the ECM/orbitalis were smooth muscle except the 3 rd layer of ECM in a juvenile sperm whale (USNM 594183 L) which showed clear striation. Circular muscle streaks resembling the cetacean ICM were identified in terrestrial cetartiodactyls (American bison, NZP 115107; Scimitar-horned oryx NZP 113469), originating from the superior (SO) and inferior (IO) oblique muscles. Among specimens examined, 11 out of 19 carnivores (7 Felidae and 2 Canidae, 2 Mustelidae) had split tendons of SO and/or IO. SO tendons bifurcated after the trochlea and wrapped the global layer of superior rectus (SR). An anterior tendon ran anterior to the scleral insertion of SR and a posterior one coursed posterior to it. IO initially traveled between the orbital and global layers of inferior rectus, bifurcated and inserted anterior and posterior to the scleral insertion of lateral rectus.
Conclusion: Recruitment of striated muscle in the sperm whale ECM 3rd layer may increase the force of protrusion of the orbit, compensating the visual fields blocked by the huge rostrum and trunk. The presence of ICM in the bison and oryx suggests that ICM is unique in cetartiodactyls. The split tendons of oblique EOMs found in all Felidae, Canidae and some Mustelidae indicates that bifid tendons evolved multiple times and support both vertical and counter-rolling eye movements.
Significance/implications: Orbitalis muscle (ECM) and ICM will be examined in other mammals to further investigate their functional and phylogenetic implications. Oblique muscle insertions will also be examined in a variety of mammals to determine if the split tendons are confined to certain groups of carnivores and to further reveal their possible functions.
Disclaimer The contents of this presentation are the sole responsibility of the author(s) and do not necessarily reflect the views, opinions or policies of Uniformed Services University of the Health Sciences (USUHS), The Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., the Department of Defense (DoD) or the Departments of the Army, Navy, or Air Force. Mention of trade names, commercial products, or organizations does not imply endorsement by the U.S. Government.