Morphological study of the eye and adnexa in capuchin monkeys (Sapajus sp.)

Abstract

The objective of this study was to describe the anatomic and histologic features of the Sapajus sp. eye, comparing similarities and differences of humans and other species of non-human primates for biomedical research purposes. Computed tomography (CT) of adnexa, eye and orbit live animal, as well as formolized pieces of the same structures of Sapajus sp. for anatomical and histological study were also performed. The anatomical description of the eye and adnexa was performed using the techniques of topographic dissection and exenteration. Histological fragments were fixated in buffered formalin 10%, processed by the routine paraffin inclusion technique, stained with hematoxylin-eosin and special stains. CT scan evaluation showed no differences between the live animal and the formolized head on identification of visual apparatus structures. Anatomic and histologic evaluation revealed rounded orbit, absence of the supraorbital foramen and frontal notch, little exposure of the sclera, with slight pigmentation of the exposed area and marked pigmentation at the sclerocorneal junction. Masson's Trichrome revealed the Meibomian glands, the corneal epithelium and Bowman's membrane; in the choroid, melanocytes and Bruch's membrane were observed; and in the retina, cones and rods as well as, optic nerve, the lamina cribrosa of the nerve fibers bundles. Toluidine blue highlighted the membranes: Bowman, Descemet and the endothelium; in the choroid: melanocytes; and in the retina: nuclear layers and retinal pigment epithelium. In view of the observed results Sapajus sp. is an important experimental model for research in the ophthalmology field, which has been shown due to the high similarity of its anatomical and histological structures with the human species.

Fig 1. Images of computed tomography of the eye, adnexa and orbit of capuchin monkey in transverse and sagittal planes.

(A) Structure with soft tissues attenuation in lacrimal gland topography. (B) Disposition of the extrinsic rectus muscles in the orbit and thickness of the optic nerves, LON: 3.1 mm and RON: 3.0 mm. (C) Sagittal plane cut in which measures of the eye are identified in the facial-caudal (17.3 mm) and dorsoventral (19.9 mm). (D) Cutting in transverse plane with lens measurement, in transverse and dorsoventral axis. (E) Image of computed tomography in three-dimensional reconstruction for bone (with suppression of soft parts) showing the closed orbit.

Fig 2. Capuchin monkey.

(A) Identification of eyelids (upper eyelid: 1- supratarsal and 2- tarsal parts, 3- upper palpebral groove, 4- lateral commissure of eyelids, 5- medial commissure of eyelids and 6- lower eyelid), arrows indicate each region and external structures of the eye (7- pupil, 8- iris, 9- limbus cornea and 10- sclera). (B) External structures of the eyelids (1- duct of lacrimal glands, 2- lacrimal point, 3- superior lacrimal papilla, 4- semilunar fold of conjunctiva, 5- lacrimal caruncle, 6- inferior lacrimal papilla and 7- anterior limb of eyelid). Posterior aspect of the eyelid (1- conjunctival tunica of the eyelid and 2- tarsal or Meibomian glands). The arrows indicate each region. Evaluation after fixation of formalin structures. (C) Lacrimal gland: 1- orbital and 2- eyelid part. (D) Eye of Sapajus sp. with extrinsic muscles and 1- elevator of upper eyelid inserted. Front view location of the eye and organized muscles in the eye. Note the muscles responsible for the movement of the eye are four rectus muscles: 2- dorsal, 3- ventral, 4- lateral and 5- medial and two oblique muscles: 6- dorsal and 7- ventral. (E) Internal structures of the eye fixed in formalin, sagittal cut. 1- Anterior chamber: note the detail showing the anterior face of the 2- iris. 3- Posterior chamber: observe the 4- lens adhered to the zonular fibers. 5- Vitreous chamber. 6- Optic nerve: observe the 7- central artery of the retina in the center.

Fig 3. Capuchin monkey macerated head (Sapajus sp.).

(A) Bones that compose the orbit: frontal (yellow); zygomatic (red); maxillary (pink); lacrimal (orange); ethmoid (blue); sphenoid (green); palatine (gray). Walls of the orbit: 1- dorsal: frontal bone and minor sphenoid wing (yellow); 2- ventral: Maxillary, zygomatic and orbital processes of the palatine bone (pink); 3- lateral: Greater wing of sphenoid bone and zygomatic bone (red) and 4- medial: lacrimal, ethmoid and minor sphenoid wing bones (orange). Orbit limits: supraorbital border, zygomatic bone, frontal bone, maxillary bone, infraorbital border, anterior lacrimal crest. Sutures: 5-frontomaxillary, 6- frontozygomatic and 7- zygomaticomaxillary. Foraminas: 8- zygomaticofacial infraorbital and 9- maxillary infraorbital. The supraorbital foramina was not observed. Note the 10- optical channel. (B) Orbit width—distance from maxillofrontale point (mf) to ektokonchion point (ek). (C) Linear magnitude of the face. Orbit measurement—Rostral interorbital width or Bi Maxillofrontale (red line).

Fig 4. Photomicrography of the eye and adnexa of the capuchin monkey.

(A) Eyelids: Observe all the structures that comprise it: 1- epidermis, 2- dermis, 3- skeletal striated muscle fibers of the palpebral part of the orbicularis oculi and pilous follicles (note the 4- Zeis glands at the base of the follicle), 5- Moll glands, 6- tarsal glands, 7- excretory duct of the gland Tarsal and 8- lymphoid follicle. HE. Obj. 5x. (B) Lacrimal gland: glandular tubuloalveolar parenchyma forming 1- lobules and lobes composed of 2- ducts and numerous 3- serous acini, responsible for the 4- secretory portion. Note the 5- amphiphilic granules. HE. Obj. 20x. (C) Eye: 1- anterior chamber (space between the posterior surface of the 2- cornea and the anterior face of the 3- iris); 4- posterior chamber (located between the posterior face of the iris and 5- lens) e a 6- vitreous chamber (space after the lens). Observe the 7- iridocorneal angle (located between the cornea and the iris), 8- limbus (9- Schlemm's canal, 10- trabecular meshwork adjacent to the canal), 11- ciliary body, 12- ciliary processes, 13- scleral and 14- bulbar conjunctiva. HE. Obj. 2,5x. (D) Cornea: layers– 1- anterior epithelium, 2- Bowman's membrane, 3- stroma, 4- Descemet's membrane and 5- endothelium. HE. Obj. 20x. (E) Lens: layers– 1- capsule of the lens, 2- subcapsular epithelium and 3- lamellar fibers. HE. Obj. 63x. (F) Retina: 1- inner limiting membrane, 2- optic never fibers layer, 3- ganglion cell layer, 4- inner plexiform layer, 5- Inner nuclear layer, 6- outer plexiform layer, 7- external nuclear layer, 8- outer limiting membrane, 9- rods (basophylic and elongated), and 10- cones (basophilic and oval). Note the 11- pigment epithelium of the retina adhered to Bruch's membrane of the 12- choroid. HE. Obj. 40x.