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Protective Ocular Mechanisms in Woodpeckers T Wygnanski-Jaffe Et Al 84

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Protective Ocular Mechanisms in Woodpeckers T Wygnanski-Jaffe Et Al 84 Eye (2007) 21, 83–89 & 2007 Nature Publishing Group All rights reserved 0950-222X/07 $30.00 www.nature.com/eye 1 2 3 Protective ocular T Wygnanski-Jaffe , CJ Murphy , C Smith , LABORATORY STUDY M Kubai2, P Christopherson4, CR Ethier5 and mechanisms in AV Levin1 woodpeckers Abstract shearing forces as the vitreous moves within the globe and the globe moves within the orbit.6 Aims Woodpeckers possess mechanisms Impact amplifies the acceleration–deceleration- protecting the eye from shaking/impact. induced forces.7 Mechanisms available to woodpeckers but not Animal models for SBS have been created by humans may help explain some eye injuries in laboratory shaking of rats, mice, pigs, and cats. Shaken Baby syndrome (SBS). Most researchers examined the brains without Methods Gross dissection and histologic 1 looking at the eyes or orbits.8,9 In murine Department of examination of eyes and orbits of seven Ophthalmology and Vision models, when eye examination was conducted, woodpeckers. Sciences, M158, The retinal haemorrhage may or may not be seen.10 Results All birds showed restricted axial Hospital for Sick Children, The woodpecker presents a naturally occurring globe movement due to the tight fit within the 555 University Avenue, model resistant to mechanical forces similar to Toronto, Ontario, Canada orbit and fascial connections between the those encountered in SBS, and we therefore M5G 1X8 orbital rim and sclera. The sclera was reasoned that insight into the pathophysiology reinforced with cartilage and bone, the optic 2Department of Surgical of SBS could be gained from understanding nerve lacked redundancy, and the vitreous Sciences, School of mechanisms in the woodpecker eye that protect lacked attachments to the posterior pole retina. Veterinary Medicine, it from injury during rapid acceleration– Conclusions Woodpecker eyes differ from University of Wisconsin, deceleration while pecking. Madison, WI, USA human infants by an inability of the globe to move axially in the orbit, the sclera to deform, 3Department of Pathology and the vitreous to shear the retina. These Materials and methods and Laboratory Medicine, findings support current hypotheses that The Hospital for Sick Children, abusive acceleration–deceleration-induced 12 prepared adult woodpecker skulls University of Toronto, ocular injury in human infants may be related representing five species collected from a Toronto, Canada to translation of vitreous within the globe and variety of sources were examined to assess the 4Department of the globe within the orbit. The woodpecker orientation and structure of the orbit within the Pathobiology, College of presents a natural model resistant to skull. All skulls were photographed from at Veterinary, Medicine, mechanical forces that have some similarity least three orientations with a metric ruler Auburn University, to SBS. (Figure 1). Auburn, AL, USA Eye (2007) 21, 83–89. doi:10.1038/sj.eye.6702163; Seven dead woodpeckers were collected from 5 published online 18 November 2005 parts of Wisconsin by the School of Veterinary Departments of Mechanical and Industrial Medicine, University of Wisconsin, Madison Engineering and Keywords: woodpeckers; shaken baby campus. All seven birds had been collected after Ophthalmology, University syndrome; protective mechanisms death from a variety of causes: two tower of Toronto, Toronto, Canada strikes, one hawk kill, four unknown. The woodpeckers represented three species: two Correspondence: AV Levin, flickers (Colaptes auratus), two red-headed Tel: þ 1 416 813 1076; Introduction Fax: þ 1 416 813 6261. woodpeckers (Melanerpes erythrocephalus), and E-mail: alex.levin@ Retinal haemorrhages are one of the principle three yellow bellied sapsuckers (Sphyrapicus sickkids.ca manifestations of Shaken Baby syndrome (SBS), varius). occurring in 50–100% of cases.1–5 Other ocular All birds were immersion fixed in 10% Received: 31 May 2005 findings include schisis of the macula induced neutral buffered formalin for periods ranging Accepted in revised form: by vitreous traction, optic atrophy, and less from 3 days to 6 months. Using loupes, we 17 September 2005 Published online: commonly, retinal detachment. Retinal performed macroscopic dissection of the fascial 18 November 2005 haemorrhages in SBS are thought to be in part attachments between the anterior portions of the result of acceleration–deceleration-induced the globe and surrounding structures using a Proprietary interest: none Protective ocular mechanisms in woodpeckers T Wygnanski-Jaffe et al 84 Figure 1 Woodpecker skull intraocular bony ossicle (specimen is labelled with writing on the ossicle) is anterior to orbital rim. Orbit is oriented such that visual axis is approximately 751 from saggital plane. scalpel blade, scissors, and ronjeurs. In one bird, the globe was approached by first invading the intracranial Figure 2 Tight fascial connections between the eye, orbit and space and dissecting forward so that the orbit was surrounding tissues, encasing the woodpecker eye and anchor- ing the globe to surrounding structures. Asterix indicates level opened from behind and above. After we inspected the of the scleral ossicle. Arrow indicates cornea. relationship of the globe and optic nerve to the bony orbit, the eyes were enucleated. The extraocular muscles were identified and used for orientation of the globe. Five medially from the quadrate process. The globe is of the dissected eyes were then decalcified for 30–60 min oriented in the skull such that the visual axis makes an using Decal I (Surgipath Medical Industries Inc., angle of approximately 751 relative to the sagittal plane, Richmond, IL, USA) and inspected under a dissecting placing the posterior pole of the retina tangential to the microscope after dividing the globe into two calottes at anterior–posterior plane of the strike. 1501, below the optic nerve. These five eyes were then In fixed specimens the palpebral fissure is narrow and routinely processed for paraffin embedding and allows exposure of less than 50% of the corneal surface. It subsequently sectioned at 8 mm for histologic is exposed to a greater degree in life. On dissection of the examination. Sections were stained with haematoxylin periocular tissues we found that a shallow cone of and eosin, Masson trichrome or alcian blue, and periodic extensive very adhesive fascial interconnections involved acid Schiff. All steps of the gross and microscopic the periorbita, the orbital rim and the sclera. These were dissections were photographed. Five dissections were the subocular ligament, the subocular performed at the University of Wisconsin School of laryngomandibular ligament, and the postorbital Veterinary Medicine by the authors (TWJ, CJM, AVL) ligaments. Although the prolonged formalin fixation with two additional birds being dissected at The Hospital made fine gross dissection of the tissues difficult, we for Sick Children by one or two authors (TWJ, AVL). found that virtually the majority of the bulbar surface of Slight variations on the above technique were used for the lids, beginning at the conjunctival fornices and the latter birds, since they were used for the purpose of extending peripherally, is intimately related and attached identifying the angle of the visual axes, optic nerve to the underlying sclera from the orbital rim forward lengths, and axial globe lengths. (Figure 2). Only the regions extending 1–2 mm peripherally from the upper and lower lid margins are free of these fascial attachments. This causes the anterior Results portion of the globe to be bound firmly to the overlying We found no significant ocular or orbital variations lids and orbital rim. among the seven different species of woodpeckers. Laterally, the medial aspect of the globe at the plane of Examination of gross specimens as well as the prepared the ora serrata is actually well within the orbital limits. skulls revealed that, the woodpecker orbits take up most The orbital rim lies just posterior to the posterior margin of the skull and have a far greater volume than the brain of the scleral ossicles (Figure 1). The scleral ossicles are cavity, which is posterior and medial to the orbits. The small bones in the anterior sclera that unite to form a ring two globes are separated at the midline by a thin (approx. that extend from just posterior to the limbus to the 0.1 mm) bony interorbital septum. The globe is supported equatorial region of the globe. The scleral ossicles are a inferio-laterally by the bony quadrate process (Figure 1). constant anatomic feature in the eyes of all birds. They The quadrate bone suspends the lower jaw in non- determine the shape of the eye, serve as firm anchors for mammalian vertebrates and represents the evolutionary the origin of the striated ciliary muscles and provide forerunner of an inner ear bone (the incus) in mammals. protection to the lateral aspect of the globe that lies The orbital floor consists of a firm membrane that runs largely outside of any bony orbital protection. The Eye Protective ocular mechanisms in woodpeckers T Wygnanski-Jaffe et al 85 nictitating membrane covers the eye inferiorly and configuration lying completely tangential to the sclera. medially during rest and passes laterally across the These muscles effect rotational movements of the eye, globe. although the degree of ocular movement would be Macroscopic dissection of the orbit after the lids, limited by the firm fascial attachments of the sclera to the periorbita, and superior orbital rims were removed, periorbita. revealed that the globe
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