Mammals

 

The way in which mammals blink takes several forms:

  1. 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:

Ring-tailed lemur (Lemur catta).

Globe retraction during an upper and lower eyelid blink in a ring-tailed lemur. Played at 10% speed.

Figure 72.png

Stills from video, showing globe retraction during a blink. No nictitating membrane is seen.

Figure 73.png

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).

Figure 74.png

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.

Binturong (Arctictis binturong).

Figure 75.png

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

The eyelids come together as the left eye then the right retract as the claws approach (20% speed).

Grey-headed flying fox (Pteropus poliocephalus).

Double wink showing retraction of the right globe. Played at10% speed.

Figure 76.png

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.

Figure 77.png

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 other times synchronously in a drowsy female (20% of recording speed) 

Giraffe (Giraffa).

Figure 79.png

Upper and lower lid blink.

Asian elephant (Elephas maximus). 

                                                                                                                          POSTERIOR              ANTERIOR

Figure 79a.png

Upper and lower lid. 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. 

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

Figure 81.png

Upper and lower lid blink.

Sumatran tiger (Panthera tigris sondaica).

Figure 82.png

Upper and lower lid blink.

Lion (Panthera leo).

Figure 83.png

Upper and lower lid wink.

Domestic cat (Felis catus) with right facial paralysis.

This female had sustained a temporary 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.

Figure 84.jpg

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.

Figure 86.png

At 0ms, the right palpebral fissure is wider than the left due to weakness of the orbicularis oculi muscle (as 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.

Figure 85.png

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.

Mechanism of blink in the cat

Stibbe (1928) pointed out the differences between the nictitating membrane of birds and mammals. In both it consists of a crescentic fold in the conjunctiva in the inner angle of the orbit projecting towards the cornea. But whereas birds have a pair of muscles behind the eye which are attached to the tendon of the membrane and which pull it across the cornea, no such apparatus is found in mammals. In mammals, the movement of the membrane occurs with retraction of the globe. In birds, there is no globe retraction.

So, by what mechanism does the nictitating membrane move over the cornea? The innervation of the nictitating membrane in the cat has been studied closely as it has been widely used as a way of assessing the action of drugs on sympathetic nerves. Paton and Thompson (1970) and Thompson (1961) demonstrated that the membrane is held in a retracted position by two muscles: 1) the inferior smooth muscle which arises from fascia around the inferior rectus muscle and inserts into cartilage in the membrane (see Figure) and 2) the medial smooth muscle which arises from fascia around the medial rectus muscle and inserts into cartilage in the membrane (Figure). Both muscles are innervated by sympathetic nerves. The relationship of these two muscles to each other is shown in the Figures below from Thompson (1961).

Figure 87.png

Diagram of the right eye seen from the lateral side. The inferior smooth muscle is supplied by sympathetic nerves – the nerve to the inferior smooth muscle (nIM) - arising from the zygomatic nerve (Z). The origin of the inferior smooth muscle is the belly of inferior rectus (IR) and it inserts into the infraorbital nerve (IO); lacrimal nerve (L); lateral rectus (LR); optic nerve (II).

Figure 88.png

Diagram of the right eye seen from above. The medial smooth muscle is supplied by sympathetic nerves – the nerve to the medial smooth muscle (nMM) – arising from the infratrochlear nerve (I). The origin of the medial smooth muscle is the belly of medial rectus (MR) and it inserts into the cartilage (C) of the nictitating membrane. Also shown: ethmoidal nerve (Et); infratrocheal nerve (I); medial rectus (MR); lateral rectus (LR); nasociliary nerve (NC).

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).

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 (see Figure below).

Figure 89.png

To illustrate how the membrane might move with globe retraction, a deflated balloon is held by two nails in a state of tension wrapped around a plastic ball sitting over a hole. As the ball sinks into the hole, the edge of the balloon moves over the ball.

Footnote

Lesions involving the sympathetic chain 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)

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.

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.

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.

  

 

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).

Figure 91.png

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).

Figure 92.png

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.

Figure 93.png

Predominantly upper lid blink with minimal upward movement of the lower lid in a juvenile François' langur.

Cow (Bos taurus).

Figure 94.png

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.

Figure 95.png

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).

Figure 96.png

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.

Figure 97.jpg

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 and in elephants this is not the case. Here, the nictitating membrane is not obscured by the eyelids during a blink. Examples are provided in a meerkat (Suricata suricatta), a yellow mongoose (Cynictis penicillata) and an elephant. Presumably, eyelid blinks also occur in the mongoose family, but these were not observed. As described above, they were seen in elephants.

Nictitating membrane blink on head turn in a meerkat, played at 1/4 speed.

Figure 99.png

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.

Figure 100.png

Globe retraction during a blink in the meerkat.

Nictitating membrane blink with eyes wide open in a yellow mongoose, played back at 20% speed.

Figure 101.png

Stills from video above.

Two episodes of globe retraction with the head still followed by a nictitating membrane blink in the left eye on head turn in a common dwarf mongoose (Helogale parvula), played at 20% speed.

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.

The nictitating membrane is visible in elephants when they blink:

Nictitating membrane blinks with movement of the upper and lower lids which could be due to retraction of the globe, in an Asian elephant. Played back at 30% speed.

Figure 102.png

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.

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.

Figure 103.png

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 (Figure). 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).

Figure 105.png

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.

Figure 105a.png

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.

Figure 106.png

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.

Figure 107.png

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 muscle responsible for closing the eye in a blink is the palpebral part of orbicularis oculi, see link below for the anatomy, a muscle supplied by the facial nerve (VIIth cranial nerve). 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.

Figure 109.png

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. 

Elevation of the upper lid is performed by levator palpebrae superioris which is supplied by the oculomotor nerve (IIIrd cranial nerve). This muscle is closely linked to the superior rectus muscle. As a result, upward gaze is associated with elevation of the upper lid. In addition to the voluntary striated muscle, the eyelids 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.

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.

References

Arao, T. and Perkins, E. 1968. "The nictitating membrane of primates." Tha Anatomical Record 162(1):53-70.

Evans, H.E. and de Lahunta, A. 2013. Miller's Anatomy pf the Dog 4th Edition. Missouri: Elsevier Saunders.

Kempster, R.C, Bancroft, B.J. and Hirst, L.W. 2002. "Intraorbital Anatomy of the Koala." The Anatomical Record 267: 277-287.

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.

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