Frogs (Order Anurans)
Frogs are an Order within the Class of Amphibia but, despite the name, only a minority of frogs are truly amphibious after they cease to be tadpoles. The majority are wholly terrestrial, and a few are wholly aquatic. Wholly aquatic anurans such as aglossal toads, never develop eyelids (Walls 1963).
The terrestrial white-lipped tree frog (Litoria infrafrenata) has upper and lower eyelids. The way in which it blinks is shown below.
Blinking in terrestrial white-lipped frog, played at 30% speed.
At 160ms after the onset of the blink, the eyeballs are retracting into the head. This is most obvious in the left eye which is seen in profile. There is narrowing of the palpebral fissure (the gap between the eyelids), which is due to the retraction of the globes. An opaque membrane has appeared above the lower eyelid, travelling vertically in an upward direction. This is often called a nictitating membrane, but, as with the Lemon shark, it is an extension of the lower eyelid which is folded underneath the eyelid when the eye is fully open.
During sleep, the membrane rises incompletely.
Nictitating membrane half way up the cornea in a sleeping splendid tree frog (Litoria splendida)
The eyeballs retract and the lower lid elevated, one fold transparent the other not in a blink in a Green and golden Bell frog (Litoria aurea), played at 20% speed
Globe retraction and elevation of the nictitating membranes in a red-eyed tree frog (Litoria chloris), played at 20% speed.
Drawing of a section of the lower eyelid based on Rana pipiens. The nictitating membrane (nm) is shown to be attached to and folded under the lower eyelid (ll), (Walls 1963).
In the Figure below, the muscles which move the nictitating membrane in various vertebrates are shown. Diagram 'a' shows the posterior aspect of a frog’s eye with the tendon of the nictitating membrane (n) circling the globe and overlying the retractor bulbi muscle (R.b).
The musculature of the nictitating membrane in various vertebrates (Walls 1963).
According to Walls: ‘The thickened rim of the lower eyelid continues round the posterior part of the globe as a cord (tendon to nictitans) and passes through retractor bulbi. When this muscle contracts, the eyeball is pulled into the head and the transparent fold of the lower eyelid is pulled up over the cornea to meet the upper eyelid which is motionless. A broad hammock-like muscle, the levator bulbi, raises the globe to its normal elevated position and the lower lid slips back into its folded position. The eye can close without complete retraction. The tendon of the nictitating membrane (n) is pulled by the globe when the retractor bulbi muscle (Rb) contracts.’
A coronal view of the tendon of the nictitating membrane is shown below.
Coronal view of the tendon of the nictitating membrane (n) of the frog (Ecker 1889).
According to Ecker (1889): The pigmented free border of the nictitating membrane passes, at the inner and outer angles of the eye, into a tendon which passes for some distance to fibrous tissue then descends to the under surface of the eyeball and joins that the opposite side, so that the free border of the eyelid, together with this tendon form a complete ring. The tendinous part of the ring, which is thin and threadlike, is found on the under surface of the eyeball and lies under the m. retractor bulbi and is bound to this muscle. The m. retractor pulls the eyeball into the cavity backwards and downwards, while the levator raises it. There is less agreement about their movements of the eyelids, or rather of the lower eyelid, for the upper has no independent movements. Duges says that the two muscles which he considers to be levatores palpebrae inferiores, and which according to him are connected with the m. retractor bulbi, draw up the lid as it is being drawn backwards and downwards by the latter muscle. The depression of the lid on the relaxation of the retractor and projection of the eyeball is due simply to elasticity. Manz on the contrary has shown that the sinking of the eyeball by the contraction of the retractor must necessarily cause a rising of the nictitating membrane as its tendons are attached to that muscle and so must follow its movements. Depression of the lower lid occurs simultaneously with the raising of the eyeball by means of m. levator bulbi, through the contraction of the m. depressor palpebrae inferioris, which proceeds from that muscle; this is easily understood, as they are but parts of the same muscle.
In summary, blinking in frogs is initiated by retraction of the globe by the retractor bulbi muscle. This causes elevation of the nictitating membrane by pulling on its tendon, which circles the globe. The nictitating membrane is an extension of the lower eyelid. There is no muscle pulling on the nictitating membrane tendon other than the retractor bulbi muscle to which it is attached, so movement of the nictitating membrane/lower eyelid and retraction of the globe cannot occur independently of each other. The upper eyelid has no muscles or tendons attached to it. Any movement of the upper eyelid which occurs is therefore passive, caused by the eyeball, on which it rests, retracting into the skull and then protruding at the end of the blink. Depression of the lower lid at the end of the blink is done by contraction of depressor palpebrae inferioris, a branch of the levator bulbi muscle which raises the globe. In frogs, all blinks involve the same structures.
Innervation of the muscles involved in blinking
Retractor bulbi: Abducens nerve (VIth cranial nerve)
Levator bulbi: Trigeminal nerve (Vth cranial nerve)
Depressor bulbi inferioris: Trigeminal nerve
NB Amphibia have only ten pairs of cranial nerves; mammals have twelve pairs.
Comments on the evolution of blinking in frogs
The ancestors of frogs probably spent much of their time in shallow water. Their eyes and orbits evolved to sit like turrets on the skull, allowing aerial vision for the detection of prey and predators, while the rest of the animal was submerged. The nictitating membrane might protect the cornea from floating debris when the eye is open. In addition, it moistens and cleans the surface of the cornea by spreading the oily secretions from the Harderian gland which lies amongst the muscles behind the eyeball. Retraction of the globe into the skull protects the eye from mechanical injury from pressure or from a blow; an important function as the frog lacks a neck and can jump but cannot turn its head away to avoid injury. Uniquely, blinking in frogs also aids in swallowing as the retracted eyes project into the throat.
Ecker, A (Translated by Haslam, G). 1889. The anatomy of the frog. Oxford: OUP.
Walls, GL. 1963. The vertebrate eye and its adaptive radiation. New York and London: Hafner.