Mammals
The way in which mammals blink takes several forms:
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Globe retraction with closure of the upper and lower eyelids.
Here the most visible feature of the blink is closure of the eye as the upper and lower lids come together. With the benefit of video, it may be possible to see that the eyeball has also retracted. The nictitating membrane may also have been deployed but it is hidden by the eyelids.
Species showing this type of blink include:
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Ring-tailed lemur (Lemur catta).
Globe retraction during an upper and lower eyelid blink in a ring-tailed lemur. Played at 10% speed.
Stills from video, showing globe retraction during a blink. No nictitating membrane is seen.
Both upper and lower eyelids contribute to the blink.
Coquerel's sifaka (Propithecus coquereli)
Here the upper lid predominates in this partial blink.
Comment: The prominent eyes of arboreal creatures like lemurs, make them susceptible to injury from branches and twigs. Retraction of the globes is the way they have dealt with this.
Koala (Phascolarctos cinereus).
Upper and lower eyelid closure with globe retraction.
The orbital anatomy of the koala was studied by Kempster (2002). As with placental mammals, the retractor bulbi muscle consists of 4 fascicles and is supplied by the abducens nerve. The levator palpebrae superioris muscle shares its tendon of origin with the superior rectus muscle and is supplied by the oculomotor nerve. The nictitating membrane covers one third of the cornea when fully extended.
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Binturong (Arctictis binturong).
Upper and lower eyelid closure with globe retraction. The palpebral fissure is almost circular with the eyes open.
Short-beaked echidna (Tachyglossus aculeatus)
Lower eyelid elevation with globe retraction played at 10% speed
Two-toed sloth (Genus Choloepus)
The eyelids come together as the left eye then the right retract as the claws approach (20% speed).
Brazilian tapir (Tapirus terrestis)
The eyelids come together as the right eye retracts (10% speed).
Grey-headed flying fox (Pteropus poliocephalus).
Double wink showing retraction of the right globe. Played at 10% speed.
Upper and lower lid wink with globe retraction. Again, the open palpebral fissure is almost circular.
Asian small-clawed otter (Aonyx cinereal).
Globe retraction during a blink. Played at 5% speed.
Partial wink in which the left palpebral fissure narrows as the eyeball retracts into the orbit.
Pygmy hippotamus (Hexaprotodon liberiensis)
Upper and lower lid blinks with globe retraction.
Australian sea lion (Neophoca cinerea)
Repeated episodes of elevation and lowering of lower lid in a drowsy male (20% of recording speed)
Lowering of the upper lid and elevation of lower lid, sometimes independently at other times synchronously in a drowsy female (20% of recording speed)
Giraffe (Giraffa).
Upper and lower lid blink.
Asian elephant (Elephas maximus).
POSTERIOR ANTERIOR
Upper and lower lid blink. At 240ms, the eyelids have come together. In the next three frames, the white nictitating membrane is seen to withdraw toward the anterior canthus.
Upper and lower lid contraction with exposure of the nictitating membrane followed by globe retraction and medial movement of the eye in an Asian elephant. Played at 20% speed.
At 160ms, the eyeball has retracted and the white nictitating membrane is visible. At 240ms, the membrane has reached its maximal excursion. The eyelids remain open.
Upper lid and nictitating membrane blink with globe retraction in the right eye: a) Pre-blink. The edge of the nictitating membrane (white in the photo, blue in the diagram) can be seen on the medial side of the iris. b) The eyelids come together, the upper (orange) moving more than the lower. Both are sinking into the orbit as the globe retracts. c) The upper lid rises revealing the nictitating membrane. d) The nictitating membrane withdraws towards the medial canthus.
Mechanism of blinking in the elephant
Modified drawing (Harrison, 1847) of the view from behind the closed eyelids showing the palpebral fissure (thick black), nictitating membrane (blue) containing cartilage which extends through a pedicle to the harderian gland (green) and to which are attached nictitator muscles (brown), a: superior nictitator; b: inferior nictitator. The muscle fibres forming a background to these structures are of orbicularis palpebrarum. According to Harrison, the superior nictitator extends upwards and outwards from the membrane pedicle to insert into the fibrous tissue of the superior margin of the orbit. The inferior nictitator extends outwards and downwards inserting into the inferior margin of the orbit. Together they pull the membrane across the eye during a blink. When they relax, the membrane springs back to its resting position by elastic recoil. Harrison found no lachrymal puncta, ducts or sac in the elephant.
White rhino (Ceratotherium simum)
Upper and lower lid blink with globe retraction. Played at 20% speed.
Guinea pig (Cavia porcellus).
Guinea pigs blink infrequently as their tear fluid is slow to evaporate.
Upper and lower lid blink in response to blowing into the eye.
Fishing cat (Prionailurus viverrinus)
Upper and lower lid blink.
Sumatran tiger (Panthera tigris sondaica).
Upper and lower lid blink.
Lion (Panthera leo).
Upper and lower lid wink.
Domestic cat (Felis catus) with right facial paralysis.
This female had sustained a right facial nerve injury as a result of being bitten behind the ear by a dominant male cat. The facial nerve supplies orbicularis oculi, the sphincter muscle of the eye. As a result, she was unable to blink with her eyelids on the right side. During light blinks, like those in the video, the nictitating membrane does not appear. On stronger blinks, the nictitating membrane is seen to move across as the globe retracts. Any such movement on the left side is of course obscured by the closed eyelids. In the Figure, the left eye has closed during a blink while the right eye remains open. No nictitating membrane is visible indicating that not every blink is accompanied globe retraction and deployment of the nictitating membrane (see below).
Two blinks in a domestic cat with right facial palsy.
Right facial paralysis causing the right eye to fail to close during a blink which closed the left eye. The blink in the left eye involves both upper and lower eyelids.
Blink on head turn in a domestic cat with right facial palsy. The right eye fails to close revealing movement of the nictitating membrane across the the cornea as the globe retracts.
Another blink is shown in the Figure.
At 0ms, the right palpebral fissure is wider than the left due to weakness of the orbicularis oculi muscle (as a result of the facial nerve palsy). At 180ms, the left eye is closing as the cat blinks. At 250ms, the right eyeball has retracted and in the next two stills, the nictitating membrane crosses the cornea and then returns. The blink has finished by 490ms. The head turned to the right during the course of the blink.
In the Figure below, the eyeball is seen to retract, causing movement of the nictitating membrane, during a blink.
At 90ms, the eyeball has retracted and the nictitating membrane is visible. At 130ms, the nictitating membrane has moved a little further across the eye. This is a partial blink.
In summary, in cat blinks, both upper eyelid, lower eyelid and nictitating membrane are involved together with globe retraction. Not all blinks involve globe retraction. Of note, is that members of the cat family often have no eyelashes.
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Mechanism of blink in the cat
​Stibbe (Stibbe, 1928) first pointed out that the way in which the nictitating membrane operates in mammals is different from other classes of vertebrate. In dissections of a number of mammals he found the membrane to be a stout, crescent shaped fold in the conjunctival membrane arising in the medial canthus, enclosing a T-shaped cartilage curved to the convexity of the cornea to provide a tight fit, and attached to the inner aspect of the eyeball and to the internal tarsal ligament. It did not appear to be as mobile or elastic as the bird membrane. In calves, sheep, rabbits and cats he was unable to find any functional muscle equivalent of pyramidalis or quadratus attached to the membrane. The harderian gland was embedded in the back of the membrane. Acheson (Acheson, 1938) later found two thin sheets of smooth muscle arising respectively from the fascial cover of the medial and inferior recti muscles and inserted into the respective sides of the cartilage. The muscles were innervated by sympathetic
nerves.
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The figure above is derived from Thompson’s (Thompson, 1961 ) anatomical study of the cat nictitating membrane:
A. Cat right eye with the nictitating membrane held in the inferior part of the medial canthus by the inferior and medial smooth muscles. a) Nictitating membrane cartilage; b) Harderian gland; c) Inferior smooth muscle attached to the cartilage and inferior rectus. d) medial smooth muscle attached to medial rectus. e) inferior rectus; f) medial rectus
B. As for A, with the edge of the nictitating membrane closer to the pupil as the smooth muscles have relaxed.
With the eye open, the nictitating membrane is held in a state of tension in the medial canthus by the inferior and medial smooth muscles. The cat is said to have a mechanism for actively protruding the nictitating membrane by contracting muscle fibres of levator palpebrae superioris and lateral rectus (VI cranial nerve) which insert into the membrane (Barnett & Crispin, 1998). The inferior and medical smooth muscles are supplied by sympathetic nerves. The medial rectus is supplied by the IIIrd cranial nerve and the lateral rectus by the VIth cranial nerve. The orbicularis muscle is supplied by the VIIth cranial nerve.
Not all mammals are wired this way. In some rabbits, for example, sympathetic nerves play no part in reflex retraction of the nictitating membrane (Cegavske 1976).
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What causes the membrane to move out or protrude across the cornea? This varies with the mammalian species. In most it moves across the cornea by elastic recoil as the globe retracts.
Footnote
Lesions involving the sympathetic nerve supply to the eye in a cat cause paralysis of the nictitating membrane, which then remains in view with the eye open.
Paralysis of the left nictitating membrane in a cat following a bite to the neck. The lower eyelid is slightly elevated and the pupil (though largely obscured by the nictitating membrane) appears to be smaller. These are features of Horner's syndrome. (Video by Samantha Morris)
Nictitating membranes lie obliquely across the eyes, which are being held open, in a drowsy cat.
In the cat, according to Paton and Thompson (1970), in addition to the effect of retraction of the globe, movement of the nictitating membrane across the cornea is assisted by contraction of leashes of striated muscle arising from external rectus and levator palpebrae superioris and inserting into the membrane.
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As with most mammals (Duke-Elder 1958), the upper and lower eyelids are closed by orbicularis oculi and the upper eyelid is opened by levator palpebrae superioris. In some species, for example, the elephant, the lower lid is drawn down by depressor palpebrae inferioris.
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Of interest is the fact that the globe only retracts during closure of the eyelids in a blink. There is no mechanical reason for this. Synchronous contraction of orbicularis oculi and of the retractor bulbi are coordinated in the brainstem.​
Domestic dog (Canis familiaris)
The figure above shows the effect of pressing the left eye into the orbit in a Labrador: a) The eyelids are pulled apart. b) Pressure is exerted on the eyeball. The nictitating membrane rises from below the eye. c) With further pressure the nictitating membrane has risen to almost cover the eye. The palpebral fissure has narrowed due to the globe lying deeper in the orbit.
Mechanism of nictitating membrane blink in the dog.
The case above shows that passive movement of the eyeball into the orbit by pressure causes the nictitating membrane to move over the eye (incidentally, vets will know that this also happens in newly euthanized dogs).
The figure above is a schematic representation of how the membrane (blue) is able to move over the eye when the globe is pulled into the orbit by the four bellies of the retractor bulbi muscle (Misk & Hifay, 1978): A, the globe is retracted and the membrane, arising from the inferior part of the medial canthus, is attached (g and h) to the wall of the orbit. B, the eye pushes the membrane aside as the retractor bulbi muscle relaxes and the eye protrudes.
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As with the domestic cat, muscles insert into the cartilage of the nictitating membrane, and these pull the membrane downwards and medially into the medial canthus. Interruption of the sympathetic nerve supply to these muscles in Horner syndrome, causes the nictitating membrane to move a little towards the pupil.
Domestic goat (Capra hircus)
Demonstration of the nictitating membrane in the left eye: a) The thumb of the vet is seen everting the upper eyelid exposing its pink conjunctival surface (yellow in the diagram). The pupil is horizontally elongated. The resting nictitating membrane (blue in the diagram), with a black pigmented fleck, can also be seen in the medial canthus. b) The membrane starts to move across the eye. c) the membrane moves further across the eye, and there is protrusion of a boomerang shaped cartilage.
2) Globe retraction with predominantly upper eyelid closure
Here there is globe retraction with upper lid closure. Again, it is not possible to see if the nictitating membrane has been deployed. In primates, the degree to which it is able to move across the cornea varies markedly from species to species (Arao 1968). In Gorilla gorilla, it covers about 10% of the cornea. Examples of this type of blink include:
Western lowland gorilla (Gorilla gorilla gorilla).
This gorilla has deep set eyes. When he blinks, the eyes are lightly closed at 40ms, the upper lids moving more than the lower lids. He screws his eyes up at 80ms by contracting the orbital part of orbicularis oculi (see below).
Common chimpanzee (Pan troglodytes).
There is obvious retraction of both eyeballs at 40ms on the video and this is apparent on the still at 120ms with lowering of the upper eyelids. Closure of the eyes is done by the upper eyelids.
François' langur (Trachypithecus francoisi).
Upper lid blink, played at 10% speed.
Predominantly upper lid blink with minimal upward movement of the lower lid in a juvenile François' langur.
Cow (Bos taurus).
At 40ms, the upper lid has lowered and the eyeball has retracted. By 120ms, the upper lid has covered the eye. The position of the lower lid is unchanged.
At 80ms, the left eye has closed, with mainly the upper eyelid involved. At 120ms, the right eyeball has retracted and the palpebral fissure has narrowed. At 280ms, the upper lid has covered the right eye.
Mechanism of blink in the cow.
The anatomy of the retractor bulbi muscle in a calf is shown in the figures below from Stibbe (1928).
Dissection of the orbit of a calf from above, showing a broad conical sheath of muscle running from the eyeball to the back of the orbit.
Dissection of a calf nictitating membrane to show the anvil shape of the cartilage abutting onto the leading edge of the membrane.
3) Globe retraction and nictitating membrane movement without eyelid blinking
While most mammals only retract their eyeballs and deploy their nictitating membranes during an eyelid blink, in the mongoose family, the okapi and the rock hyrax this is not the case. Here, the eyelids do not come together when the eye retracts and the nictitating membrane crosses. Examples are provided in a meerkat, a yellow mongoose, a dwarf mongoose, an okapi and a rock hyrax. Eyelid blinks are rarely seen in the mongoose family, but the eyelids do come together in sleep.
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Meerkat (Suricata suricatta)
Nictitating membrane blink on head turn in a meerkat, played at 1/4 speed.
Nictitating membrane blink on head turn in a meerkat with no associated closure of the eyelids.
Again, the deployment of the nictitating membrane is related to retraction of the globe (see below)
Nictitating membrane blink with globe retraction in a meerkat, played at 10% speed.
Globe retraction during a blink in the meerkat.
Nictitating membrane blink on head turn in the right eye: a) Pre-blink. The nictitating membrane (blue in the drawing) is visible below the iris. b) The nictitating membrane rises obliquely from the medial canthus and reaches the pupil. c) The nictitating membrane covers the eye. The palpebral fissure narrows due to globe retraction.
Yellow mongoose (Cynictis penicillata
Nictitating membrane blink with eyes wide open in a yellow mongoose, played back at 20% speed.
Stills from video above.
Common dwarf mongoose (Helogale parvula)
Two episodes of globe retraction with the head still followed by a nictitating membrane blink in the left eye on head turn, played at 20% speed.
Mechanism of blinking in the meerkat
Overlapping sagittal views of the meerkat nictitating membrane blink, pre-blink and during a blink: The membrane (blue) lying in the inferior fornix of the medial canthus, rises to cover the cornea when the globe retracts.
Not all mongoose-like mammals blink on head turn:
Multiple head turns are seen in this ring-tailed mongoose from Madagascar (Galidia elegans) but none is associated with a blink (played at 20% speed). There is dispute as to whether this should be grouped with mongooses, the name ring-tailed vontsira now being preferred.
Okapia johnstoni
Nictitating membrane blinks with globe retraction played back at 10% speed
Nictitating membrane blink with globe retraction in the left eye: a) The nictitating membrane is just visible below the left eye and in the medial canthus before the blink. b) The membrane starts to rise. c) The membrane expands further from below the eye and from the medial canthus. The globe has retracted. d) The membrane has covered the eye. Its surface reveals the cartilage within. The upper and lower eyelids have sunk a little into the orbit with the globe retraction.
Rock hyrax (Procavia capensis)
Nictitating membrane blink with globe retraction played back at 10% speed
4) Upper eyelid blink with no globe retraction and no nictitating membrane present
In humans, it is the upper eyelid which closes the eye during blinking.
Spontaneous blink in a female child. This is achieved by downward movement of the upper lids. The lower lids move horizontally towards the medial canthi. Played back at 30% speed.
Stills from video showing that it is the upper lid which covers the eye. The line is drawn through the inner canthus when the eye is open.
During the blink, both upper and lower eyelids shorten, drawing the mobile outer canthus towards the fixed inner canthus. Thus, with each blink, lacrimal fluid on the surface of the eye is swept towards the puncti which drain it into the tear ducts. Globe retraction has been replaced by prominent brows as the principle means of protecting the eyes from pressure and blows. It is equivalent to having permanently retracted eyes. In addition, the nictitating membrane has all but disappeared, the only trace of it being the plica semilunaris (Figure).
The lines denote the position of the outer and inner canthi with the eyes shut. At 170ms, the outer canthus has moved towards the inner canthus.
A vestige of the nictitating membrane, the plica semilunaris, marked by an arrow.
While the lower lid plays little part in shutting the eye during a blink, it is by no means immobile. For example, it lowers on downward gaze (Figure). On upward gaze, the upper lid elevates (Figure). These movements, of course, prevent the eyelids from occluding vision during vertical eye movements.
Both upper and lower lids descend on downward gaze. The dotted lines mark the upper and lower limits of the palpebral fissure in the primary position.
Both upper and lower lids ascend on upward gaze. The dotted lines mark the upper and lower limits of the palpebral fissure in the primary position.
Mechanism of human blink
The nictitating membrane is vestigial in humans and eye closure is done by orbicularis oculi which is supplied by the VIIth cranial nerve.
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The figure above​​ shows the muscle surrounding the closed palpebral fissure (yellow) of the right eye and fixed to the orbit at the medial canthus: a) Palpebral (aka pretarsal) part; b) Preseptal part; c) Orbital part.
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The eyes are held open by tonic contraction of levator palpebrae superioris (IIIrd cranial nerve) and Mueller’s muscle (sympathetic nerve supply). During a blink, the levator relaxes and the palpebral part of orbicularis oculi contracts causing the upper lid to descend onto the lower lid (Evinger & al., 1991). Both lids move towards the medial canthus, sweeping the tear film towards the puncti at the medial end of both lids. Contraction of the pre-septal and orbital parts are responsible for screwing the eyes up. On upward gaze (due to contraction of superior rectus, supplied by the IIIrd cranial nerve), the upper lid is elevated by levator palpebrae superioris, also supplied by the IIIrd cranial nerve. If the lid did not rise it would restrict vision on upward gaze.
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Of 22 primate species examined by Arao and Perkins (Arao & Perkins, 1968), 21 had nictitating membranes. It was vestigial in chimpanzees (Pan troglodytes), covered only one tenth of the eye in gorillas (Gorilla gorilla); one eighth of the eye in macaque monkeys, one third of the eye in marmosets and half of the eye in the mongoose lemur (Eulemur mongoz) and the lesser bushbaby (Galago senegalensis). Only in the potto (Perodicticus potto) and angwantibo (Arctocebus calabarensis) did the membrane cover the eye.
​​​As mentioned above, the muscle responsible for closing the eye in a blink is the palpebral part of orbicularis oculi. While this muscle is depicted as being similar in the upper and lower lids, its action with respect to the two lids is very different. Both lids shorten during a blink, but only the upper lid moves in such a way as to close the palpebral fissure. This suggests that the lower lid is tethered in some way. Observation of the lids when the eyes are being screwed up may help to explain this (Video). Contraction of the orbital part of orbicularis oculi below the eye, pushes the lower lid up. The lower lid is tethered to the orbital part of orbicularis oculi, not to the lower rim of the orbit.
'Screwing up' the eyes. The lower lid elevates causing the palpebral fissure to become crescent shaped. At the same time, the cheeks elevate. Both are due to contraction of the orbital part of the lower half of orbicularis oculi.
The dotted lines mark the upper and lower limits of the palpebral fissure before the action. There is minimal downward movement of the upper lids; most of the movement affecting the eye when it is screwed up is done by the lower lid.
The eyelids also have smooth muscle, Müller's muscles (the superior and inferior tarsal muscles), which are innervated by sympathetic nerves. Müller's muscles keep the eyes open with tonic (sustained) contraction. Lesions of the sympathetic nerves to the eye cause Horner’s syndrome with slight drooping of the upper lid and elevation of the lower lid.
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Summary of mammalian blink.
Four types of mammalian blink were observed: 1) Blinks involving upper and lower eyelids with globe retraction causing movement of the nictitating membrane. 2) Predominantly upper lid closure with globe retraction and movement of the nictitating membrane. 3) Globe retraction causing movement of the nictitating membrane 4) Upper eyelid closure with no globe retraction and no nictitating membrane.
In the first three types of blink, the eye is protected from blunt injury by globe retraction. In the fourth type, the eyes are protected by protuberant brows.
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References
Arao, T. and Perkins, E. 1968. "The nictitating membrane of primates." Tha Anatomical Record 162(1):53-70.
​Barnett, K., & Crispin, S. (1998). Feline ophthalmology. Saunders.
Evans, H.E. and de Lahunta, A. 2013. Miller's Anatomy pf the Dog 4th Edition. Missouri: Elsevier Saunders.
​Evinger, C., & al., e. (1991). Eyelid movements. Mechanisms and normal data. Invest Ophthalmol Vis Sci, 32(2):387-400. PMID: 1993591.
​Harrison. (1847). On the anatomy of the lachrymal apparatus in the elephant. Proceedings of the Royal Irish Academy, 4, 158-165.
Kempster, R.C, Bancroft, B.J. and Hirst, L.W. 2002. "Intraorbital Anatomy of the Koala." The Anatomical Record 267: 277-287.
​Misk, N., & Hifay, A. (1978). The anatomy of the tendons of insertion of the extrinsic muscles of the eyeball in dog and cat. Egypt J Vet Sci, 15: 555-59.
Paton, W.D.M. and Thompson, J.W. 1970. "The roles of striated and smooth muscle in the movement of the cat's nictitating membrane." J. Physiol. 206: 731-746.
Payne, A.P. 1994. "The harderian gland: a tercentennial review." J. Anat. 185:1-49.
Stibbe, E.P. 1928. "A comparative study of the nictitating membrane of birds and mammals." J. Anat. 62: 159-176.
Thompson, J.W. 1961. "The nerve supply to the nictitating membrane of the cat." J Anat. 1961 Jul; 95(Pt 3): 371–385.
