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

Abstract

Each rectus extraocular muscle in cetaceans divides into two portions: a massive palpebral belly that inserts into the deep surface of the eyelids and a smaller scleral belly that inserts onto the eyeball. While the cetacean palpebral insertions have long been recognized, their homologies and functions remain unclear. To compare cetacean rectus EOM insertions with the global and orbital rectus EOM insertions of other mammals we dissected orbital contents of 20 odontocete species, 2 mysticete species and 18 non-cetacean species, both aquatic and terrestrial. Four cetacean species were also examined with magnetic resonance imaging (MRI). All four rectus muscles in cetaceans had well-developed palpebral bellies and insertions. Adjacent palpebral bellies showed varying degrees of fusion, from near independence to near complete fusion. Fusion was most complete towards palpebral insertions and less towards origins. A medial moiety of the superior rectus palpebral belly is likely the levator palpebrae superioris. Smaller but still robust scleral insertions were present on all recti, with the medial rectus (MR) being significantly more muscular than the others. All non-cetacean species examined had recti with distinct global and orbital insertions, the latter generally onto Tenon's capsule. Orbital insertions in pygmy hippopotamus and Florida manatee extended into the deep surfaces of the eyelids, hence qualifying as palpebral insertions. Our results suggest that rectus EOMs of mammals generally have both global and orbital insertions, and that palpebral bellies of cetaceans and other species are modified homologs of the orbital insertions. The presence of palpebral insertions in pygmy hippopotamus and absence in other cetartiodactyls suggests an intermediate condition between terrestrial cetartiodactyls and cetaceans. Palpebral insertions in Florida manatee and reports of their presence in some pinnipeds suggest parallel evolution in multiple aquatic lineages. Various functions of cetacean palpebral recti have been proposed, including eyelid dilators, protection during diving and thermogenesis for warming eye and brain. For further insight into their possible functions, we observed eye movements of captive bottlenose dolphins (Tursiops truncatus) at the U.S. National Aquarium. Our observations showed that in addition to rotation of the eyeball the entire surrounding palpebral region also moves during gaze changes. For example during upward gaze the globe not only rotates in supraduction but translates dorsally as well. It appears the rectus palpebral bellies are responsible for flexing the palpebral structures and thus also translating the globe, while the scleral insertions act directly for ocular rotation. Along with frequent non-conjugate eye movements, the oculomotor mechanics and repertoire of cetaceans are thus quite distinctive. Summarily, axial displacement within the orbit is a major 'eye movement' in cetaceans, with protrusion and retraction mediated by well-developed circular muscles and retractor bulbi respectively. Torsional eye movements driven by elaborate oblique EOMs are likewise significant. The roles of rectus EOMs for ocular rotation via their scleral insertions, especially the highly muscular MR, are for typical supra/infraductions and nasal/temporal ductions. The palpebral bellies accentuate these ductions by translating the globe and surrounding structures in the same direction.

Keywords: eye muscles; orbital insertions; rectus extraocular.

FIGURE 1

Massive palpebral belly and weakly developed scleral belly of rectus EOMs in cetaceans. (a, b) SR, LR and MR in minke whale (Balaenoptera acutorostrata, USNM 593554 R) and (c) MR in pygmy sperm whale (Kogia breviceps, USNM 594027 R) demonstrate the scleral parts inserting onto the anterior hemisphere close to the equator (widest point) of the globe. (d) Scleral MR is slightly thicker than that of the other rectus EOMs in minke whale (Balaenoptera acutorostrata, USNM 504674 L), although it is not nearly as muscular as that in Odontoceti. (e, f) MRI clearly show massive palpebral belly and weaker scleral belly of rectus EOMs in sperm whale (Physeter macrocephalus, 594183 R) and in Risso's dolphin (Grampus griseus, 594001 L) respectively. Yellow dotted circles show the joint insertion of palpebral belly of rectus EOMs (SR and IR), ECM and ICM in (e). Scleral part of SR is not visible in (f); probably it is pushed against the palpebral part of SR (superior to SO in this image). Abbreviations: A, apical, toward orbital apex; CN II, optic nerve; ECM, external circular muscle (orbitalis); ICM, internal circular muscle; IO, inferior oblique; IR, inferior rectus; LR, lateral rectus; MR, medial rectus; MRI, magnetic resonance imaging; N, nasal; p, palpebral belly; ORM, ophthalmic rete mirabile; RB, retractor bulbi; s, scleral belly; SO, superior oblique; SR, superior rectus; T, temporal; V, ventral. Scale bars: 10 mm

FIGURE 2

Different fusion types of palpebral belies in cetaceans. Type 1: each palpebral belly of rectus EOMs is fused with adjacent counterparts as shown in (a) minke whale (Balaenoptera acutorostrata, USNM 504674 R). Type 2: palpebral rectus EOMs are fused except MR as in (b) Gervais' beaked whale (Mesoplodon europaeus, USNM 550070 R). In Type 3, MR is covered by third layer of ECM in (c) Atlantic spotted dolphin (Stenella frontalis USNM, 594532 L), (d) Stenella frontalis (USNM 594532 R) and (e) Fraser's dolphin (Lagenodelphis hosei, USNM 594200 L). MR is partially covered by palpebral belly of IR and third layer of ECM in (f–g) harbour porpoise (Phocoena phocoena, USNM 593413 L, USNM 593411 R), (h) Atlantic white‐sided dolphin (Lagenorhynchus acutus, USNM 571446 R) and (i) bottlenose dolphin (Tursiops truncatus, USNM, 594531 R). The thick CT ‘pocket’ encloses MR in (j) Atlantic spotted dolphin (Stenella frontalis, USNM 594532 R). (k, l) Fused palpebral bellies of rectus EOMs are demonstrated in the cross‐sectional MRI of melon‐headed whale (Grampus griseus, USNM 594001 L). The red line in (k) is the plane of section of (l). While MR has palpebral (red dots) and scleral (yellow) parts as in other recti, palpebral belly of MR is completely separated from the fused SR, LR and IR palpebral bellies (red dots). Abbreviations: A, apical, toward orbital apex; CN II, optic nerve; CT, connective tissue; ECM, external circular muscle (orbitalis); IO, inferior oblique; IR, inferior rectus; LR, lateral rectus; MR, medial rectus; N, nasal; RB, retractor bulbi; SO, superior oblique; SR, superior rectus; T, temporal; V, ventral. Scale bars: 10 mm

FIGURE 3

Muscular scleral belly of MR in small‐to‐middle‐sized toothed whales. They remain muscular throughout their course and cylindrical in shape. (a) Harbour porpoise (Phocoena phocoena, USNM 593413 L). (b) Risso's dolphin (Grampus griseus, USNM 5940010 R). (c) Atlantic spotted dolphin (Stenella frontalis, USNM 594532, L). Abbreviations: A, apical, toward orbital apex; D, dorsal; MR, medial rectus; N, nasal; p, palpebral belly; RB, retractor bulbi; s, scleral belly; T, temporal; V, ventral. Scale bars: 10 mm

FIGURE 4

Palpebral grooves found in the external surface of the eyelid in cetaceans. Mysticetes such as (a) minke whale (Balaenoptera acutorostrata, USNM 593554 R) and (b) fin whale (Balaenoptera physalus, USNM 594182 L) have prominent main grooves (yellow arrows) on dorsal and ventral eyelids, each with multiple accessory grooves (light blue arrows). In contrast, odontocetes such as (c) bottlenose dolphin (Tursiops truncatus USNM 593582 R) exhibits less developed main groove on each side.  Abbreviations: N, nasal; T, temporal; V, ventral. Scale bars: 10 mm

FIGURE 5

Two insertions of rectus EOMs in terrestrial mammals. Inner portion inserts onto the sclera while the outer part is continuous with the connective tissue layer corresponding to Tenon's capsule (T) in human orbit. Inner and outer portions of EOMs in the figures correspond to the global (g) and orbital layer (o) in human EOMs respectively. Tenon's capsule was sacrificed in deep dissections and was not preserved except in (a), (f), (g), (i), (j) and (k). The continuity of the outer portion (o) with the Tenon's capsule are well exhibited in (a), (f) and (g). (a) Bobcat MR (Lynx rufus, MCWC#2017‐00498 L), (b) raccoon LR (Procyon lotor, KM005 R), (c) grey squirrel LR (Sciurus carolinensis, KM010 L), (d) woodchuck LR (Marmota monax, KM003 R), (e) white‐tailed deer IR (Odocoileus virginianus, KM001 R), (f) red fox LR (Vulpes vulpes, NZP W020‐0053 R), (g) clouded leopard IR (Neofelis nebulosa, NZP N19‐0240 L), (h) slender‐tailed meerkat SR (Suricata suricata, NZP114197 R), (i) scimitar‐horned oryx SR (Oryx dammah, NZP113469 L), (j) white‐faced saki MR and IR (Pithecia pithecia, NZP115799 R), (k) red fox MR (Vulpes vulpes, NZP W020‐0053 R, close‐up) and (l) Florida panther SR (Puma concolor, USNM 602250 L).  Abbreviations: A, apical, toward orbital apex; CN II, optic nerve; CN III, oculomotor nerve; CN V, trigeminal nerve (maxillary division); D, dorsal; g, global layer; IO, inferior oblique; IR, inferior rectus; LPS, levator palpebrae superioris; LR, lateral rectus; MR, medial rectus; N, nasal; o, orbital layer; RB, retractor bulbi; SO, superior oblique; SR, superior rectus; T, temporal; Tc, Tenon’s capsule. Scale bars (a–j, l): 10 mm, (k): 5 mm

FIGURE 6

Two bellies of rectus EOMs in aquatic mammals. (a, b) Massive palpebral belly and fibrous scleral belly of SR in Florida manatee (Trichechus manatus latirostris, MEC 16111 R). (b) scleral IR is wider than that of other recti in the same specimen. Palpebral IR was severed in order to show the scleral IR. (c) SR in pygmy hippopotamus (Hexaprotodon liberiensis, USNM 256491 R) has its own palpebral belly (palpebral SR was severed to show the scleral SR) while (d) palpebral belly of LR and IR merge and form one belly towards the eyelid insertion. (e, f), Two insertions of MR and SR, respectively, in the Asian small‐clawed otter (Amblonyx cinereus, NZP 114768 R). Outer portions insert onto the connective tissue layer (Tenon's capsule, not shown) as in the terrestrial mammals examined.   Abbreviations: A, apical, toward orbital apex; g, global layer; IR, inferior rectus; LPS, levator palpebrae superioris; LR, lateral rectus; MR, medial rectus; N, nasal; o, orbital layer; p, palpebral belly; s, scleral belly; SO, superior oblique; SR, superior rectus; t, trochlea; V, ventral. Scale bars (a–d): 10 mm, (e, f): 5 mm