Medical Hypotheses 83 (2014) 607–613

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Accommodation: The role of the external muscles of the eye A consideration of refractive errors in relation to extraocular malfunction B.K. Hargrave ⇑ University of Western Australia, Australia Sydney Technical College, Australia University of London, United Kingdom

a r t i c l e

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Article history: Received 20 May 2014 Accepted 7 August 2014

a b s t r a c t Speculation as to optical malfunction has led to dissatisfaction with the theory that the lens is the sole agent in accommodation and to the suggestion that other parts of the eye are also conjointly involved. Around half-a-century ago, Robert Brooks Simpkins suggested that the mechanical features of the human eye were precisely such as to allow for a lengthening of the globe when the eye accommodated. Simpkins was not an optical man but his theory is both imaginative and comprehensive and deserves consideration. It is submitted here that accommodation is in fact a twofold process, and that although involving the lens, is achieved primarily by means of a give – and – take interplay between adducting and abducting external muscles, whereby an elongation of the eyeball is brought about by a stretching of the delicate elastic fibres immediately behind the cornea. The three muscles responsible for convergence (superior, internal and inferior recti) all pull from in front backwards, while of the three abductors (external rectus and the two obliques) the obliques pull from behind forwards, allowing for an easy elongation as the eye turns inwards and a return to its original length as the abducting muscles regain their former tension, returning the eye to distance vision. In refractive errors, the altered length of the eyeball disturbs the harmonious give – and – take relationship between adductors and abductors. Such stresses are likely to be perpetuated and the error exacerbated. Speculation is not directed towards a search for a possible cause of the muscular imbalance, since none is suspected. Muscles not used rapidly lose tone, as evidenced after removal of a limb from plaster. Early attention to the need for restorative exercise is essential and results usually impressive. If flexibility of the external muscles of the eyes is essential for continuing good sight, presbyopia can be avoided and with it the supposed necessity of glasses in middle life. Early attention to the need for muscle flexibility and for frequent change of focus, it is believed, leads to ocular wellbeing and obviates the reliance on glasses. It is a consideration yet to be widely entertained. The alarming increase in myopia has led to considerable investigation in recent years as to increase in the length of the eyeball. Thus far however there is little agreement regarding causes. Ó 2014 Elsevier Ltd. All rights reserved.

Disposition of the muscles Is the sclera extensible and are the muscles appropriately placed so to extend it? The sclera, the eye’s tough outer tunic, possesses elastic fibres around the optic nerve, around the equator of the globe and in ⇑ Address: 37 Nicholas Drive, Kingston, Tasmania 7050, Australia. Tel.: +61 3 62298696. E-mail address: [email protected] http://dx.doi.org/10.1016/j.mehy.2014.08.006 0306-9877/Ó 2014 Elsevier Ltd. All rights reserved.

abundance immediately behind the cornea. It is thickest posteriorly (1 mm) and gradually becomes thinner anteriorly, here being only 0.3 mm thick. It is into this thinner region that four of the eye’s six external muscles (the rectus muscles) are inserted, all within a few millimetres of the cornea. The fibres of these muscles enter the sclera in parallel and then fan out to become lost in the meridional fibres of the sclera. Whereas the rectus muscles are inserted into the thinnest region of the sclera, the other two muscles (the obliques) are inserted laterally into the thicker, posterior region of the globe. As with

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The action of the muscles

Fig. 1. Angular disposition of the muscles. Right eye viewed from above, visual axis directed straight ahead for distance vision.

the recti, the fibres enter the sclera in parallel and then lose themselves amongst the oblique and equatorial fibres of this region of the sclera. The two vertical recti (superior and inferior) are at an angle of about 25° to the visual axis and the two obliques at an angle of 45°. It is of importance to note here that the traction of all four recti is from in front backwards, towards the rear of the socket, while that of the obliques is from behind forwards, towards the nasal wall of the socket, and hence opposed to that of the recti, as indicated by the arrows Fig. 1. The points of insertion in the sclera of the two obliques are not far apart and together these two muscles form a nearly continuous band round the eyeball (Fig. 2). Thus they contribute to its support, somewhat in the manner of a sling.

The manner in which the external muscles of the two eyes cooperate to turn the eyes in all directions is somewhat complicated and need not concern us here. Suffice it to differentiate between conjugate movements, in which the axes of the two eyes are parallel, and disjugate movements, in which the axes incline either towards or away from each other. Here we are concerned with one action only – the disjugate movement of convergence, wherein the gaze is transferred from a far to a near object, and where the eyes must at the same time accommodate – that is, increase their focal power. It is to be noted that the eyeball is not a perfect sphere (the a-p, transverse and vertical diameters being, respectively 24, 23.5 and 23 mm). The point about which the muscles rotate the eyeball is not in fact the true centre of the globe; this point is slightly closer to the retina than to the front of the eyeball, and may be thought of as the centre of a hypothetical sphere (see Fig. 3, below). Thus the anterior region of the sclera, ciliary body, iris and cornea are all situated relatively anterior to this sphere. In conjugate movements, in which the eye is rotated freely in all directions as in a balland-socket joint, these relatively anterior structures do not participate. By contrast, these forward structures are intimately involved in convergence [Ref. [4] gives a full account].

Convergence Fig. 3 shows again the right eye in its socket, directed straight ahead. It will be appreciated at once that contraction of the medial rectus will turn the eye inwards. Not so obviously, this muscle is assisted in this action by the superior rectus (above the eyeball) and the inferior rectus (beneath). Note that all three adducting muscles (convergers) pull from in front backwards. The abducting muscles (or divergers), are the external rectus and the two obliques. Again it is easy to see that contraction of the external rectus will turn the eye outwards. It is assisted in this action – not so readily apparent – by the superior oblique (above the globe) and the inferior oblique (beneath). Note that these two muscles pull from behind forwards. When the eye is directed

Fig. 2. Dissection to show the ocular muscles of the right eye from the lateral aspect [From E. Wolff – ‘The Anatomy of the Eye and Orbit’, 1968].

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Fig. 3. Right eye from above.

straight ahead, as in distance vision, the opposed tractions of the convergers and divergers are balanced.

What happens when the eyes converge? Fig. 4(1), again shows the right eye directed straight ahead for distance vision. Suppose now that this eye, together with the left, prepares to turn inwards to fixate a near object. What sequence of events should we expect? 1. Recall, first and foremost, that the muscles responsible for convergence all pull from in front backwards (indicated by the arrows). If they are to operate without restraint, then, clearly any opposing tension must first be reduced. 2. Now recall that the traction of the two obliques is from behind forwards (arrow), and thus opposed to that of the three converging recti. Therefore if there is not to be a tug-of-war, obviously these muscles must now relax. 3. As the two obliques relax, then, together with the external rectus, the eye will slide slightly backwards and laterally in the orbit (Fig. 4(2)) The harmonious balance between the two opposing muscle groups has thus been disturbed and must now be restored if the eye is to continue to be adequately supported in its socket. 4. Room to manoeuvre and the freedom to do so is now available to the three converging muscles (superior, internal and inferior recti). As these muscles contract, taking up the slack brought about by the relaxation of the obliques, they turn the eye inwards as they do so (Fig. 4(3)). 5. It is here that we must bring to mind a fact of the first order of importance. The recti are inserted into the sclera within a few millimetres of the cornea, and It is here that the sclera is thinnest and where it is also richly endowed with elastic fibres. Consequently, as the converging recti contract to turn the eye inwards, they pull on these fibres, slightly stretching the eyeball as they do so (Fig. 4(4)). It was proposed at the outset that there were two factors involved in accommodation. In addition to the increase in curvature of the lens, and its slight movement forwards in the eye, it

was suggested that these actions were accompanied by a lengthening of the eyeball itself, as we have attempted to show. This is a matter of profound significance, as it is hoped to make clear presently. When the eye readjusts for distance vision, the converging recti relax their tension, thereby reducing their pull on the elastic fibres at the front of the eye. The two obliques, together with the external rectus, now regain their tension, rotating the eye outwards. At the same time the obliques pull it forwards once more towards the nasal wall of the socket. The eye is in focus again for distance vision and the opposed traction between convergers and divergers is again balanced, as in Fig. 4(1). The movements indicated are of course only of the order of millimetres.

Refractive errors The three refractive errors of presbyopia, myopia and hyperopia are examined briefly in terms of extraocular malfunction.

Presbyopia It is believed that presbyopia is that condition which most clearly gives support to the theory of accommodation outlined in this paper. The reduced ability of the lens to respond adequately to the demands of accommodation in middle life is well known. All too familiar is the rapidly established dependency upon glasses that almost inevitably ensues. It would seem that a reliance upon the lens is established early in life when learning to read. There is little or no attempt to encourage the child to change focus at frequent intervals, and the external muscles therefore are less likely to be called into play. Long periods watching television or spent at the computer encourage a habit of staring fixedly. As with other muscles elsewhere in the body, muscles not used tend to waste. The need exists to encourage the external muscles to resume and maintain flexibility by means of appropriate exercises and a changed mental attitude.

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Fig. 4. Changes when the eyes converge.

Myopia It has been seen how, during adjustment for near vision, the delicate elastic fibres behind the cornea are stretched, thus slightly lengthening the eyeball. One might therefore describe the eye as having been rendered temporarily myopic (Fig. 5). When the normal eye readjusts for distance vision in the manner described, the ‘myopia’ is overcome; the recti relax their tension and the two obliques regain theirs, rotating the eye outwards and pulling it forward once more towards the nasal wall of the orbit. If, however, the obliques habitually fail fully to regain their former tension in re-establishing distance vision, the chronic

slackness eventually results in a permanently elongated eyeball; in other words, a myopic eye. One might therefore reasonably describe the myopic eye as one permanently accommodated. There is assuredly more than one cause of myopia. A spasm of accommodation (i.e. spasm of the ciliary muscle) referred to in textbooks, and described as usually temporary, can give rise to a condition known as pseudomyopia. Speculation suggests that such a spasm deregulates the flow of aqueous fluid, some of which may pass into the posterior chamber or the eye, causing a build-up of pressure and an enlargement of the globe (See the section on The Ciliary Body).

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stresses experienced by the posterior sclera as a result of accommodation, convergence, vitreous pressure and extraocular muscles. His conclusion is that convergence, and more generally, the tension in the extraocular muscles, are mechanically much more important than accommodation because of the sizeable increase in vitreous pressure. The oblique muscles, he maintains, because of their attachment sites at the back of the globe near the optic nerve entrance port, have the capability of producing local stress concentrations which may be very important in understanding pathological myopia. However, by contrast, the views submitted in this paper emphasise the weakness of the obliques in myopia; an over-strong reaction would result in hyperopia, wherein their excessive opposition to the converging recti results in a foreshortened eyeball (see the following section Hyperopia). In a paper by Bayramlar et al. [3], it is suggested that the increase in vitreous length results from the effect of accommodative convergence rather than accommodation itself. Much use of convergence may be one of the contributing factors in adult onset and adult progression of myopia, it is suggested. Fig. 5. Accommodated eye is rendered temporarily myopic as eyeball lengthens.

Whatever the cause, a myopic eye is one that has become longer. In contrast to the normal eye, here the obliques fail to restore the eye to distance vision because the longer unwieldy eye renders them unequal to the task. Every attempt to accommodate is likely to make the eye longer, thus exacerbating the condition and increasing the demands on the obliques. Worse, for a myope wearing his distance correction and attempting to read, an additional accommodative effort will be required and the condition further aggravated. The obliques contribute to the support for the eyeball through their sling-like embrace, which is weakened in myopia. As a consequence, in cases of high myopia a bulging of the sclera may occur in the region between their insertions, leading to a possible detachment of the retina. Meng et al. [1] comment on the alarming rise in the incidence of myopia in recent decades which has generated an extensive amount of research, much of it concerned with the reasons for the increase in axial length of the eyeball. References to two other interesting papers follow. In the extensive research into the causes of myopia attention of course has been directed towards the reason for the axial increase in length. An abstract of a paper by Greene [2] examines the

Hyperopia How may the external muscles respond to the foreshortened hyperopic eye? Whatever the cause of the hyperopia, the tensions of the two muscle groups (adducting and abducting) will be adversely affected. The constant need to bring even parallel rays to focus will require the former to be over-contracted as they endeavor to lengthen the globe against the opposed tension of the obliques; in turn, increased tension is required as these muscles attempt to restore distance vision. Unlike the situation in myopia, wherein one group of muscles lacks normal tension, here there is a continuing tug-of-war in operation Fig. 6. The manner in which other important ocular structures (anterior sclera, cornea and iris) are called into play in the act of accommodation is dealt with in some detail elsewhere. So, too, is the refractive error of astigmatism [see Ref. [4]] Suffice it here to briefly outline the role of the external muscles. However it is important to outline here the contributory role of the ciliary body and lens. The ciliary muscle, as we know, is currently regarded as the sole agent of accommodation: however in the present context its role is seen rather as a complementary one. Fig. 7 shows the ciliary body to be more or less triangular in shape in antero-posterior section, with the iris taking origin from

Fig. 6. Hyperopia.

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Fig. 7. A-p section of the eyeball through the anterior region. [From E. Wolff – ‘The Anatomy of the Eye and Orbit’, 1968] (Wolff’s diagram does not include the dotted line).

Fig. 8. Section of the corneo-scleral junction. [From E. Wolff – The Anatomy of the Eye and Orbit, 1968].

the middle of the anterior side of the triangle. The outer side of the triangle is formed by the ciliary muscle, which is adjacent to the sclera. From the inner side, the ciliary processes take origin, and to these are attached the fibres of the zonule of Zinn which encloses the crystalline lens. The ciliary muscle, which constitutes the bulk of the ciliary body, consists of two bundles of fibres, the outermost running meridionally (antero-posteriorly) and the inner ones circularly. The meridional (or longitudinal) fibres (Brücke’s muscle) take origin from the scleral spur and the ligamentum pectinatum (Fig. 8) and can be traced posteriorly into the suprachoroid as far back as the equator of the globe or beyond. The circular fibres (Müller’s muscle) form the anterior and inner portion of the ciliary body and lie within Brücke’s muscle. They are concentric with the margin of the cornea (among the meridional fibres, there are in addition radial, or junctional fibres, believed to connect with the circular fibres).

How do the two sets of fibres cooperate in accommodation? It has been seen that, as the two obliques relax their tension, the converging recti stretch the anterior region of the globe. Coordinately the meridional fibres of the ciliary muscle relax, it being essential that the scleral and closely underlying uveal tunics move together. At the same time, the circular fibres contract. Their function is to reduce the tension of the zonule, thus allowing the lens to increase its curvature, and also to pull it very slightly forward and further away from the retina. In returning the eyes to distance vision, the converging recti reduce their pull on the front of the eyeball and the obliques resume their former tension, pulling the eye forward once more towards the front of the orbit. The visual axes are now parallel again. Correspondingly, the circular ciliary fibres now relax, tightening the zonule and flattening the lens; the meridional fibres contract as

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both scleral and uveal tunics become shorter, and are pulled forward again towards the scleral spur (the radial fibres assist in flattening the lens). The harmonious functioning of both sets of ciliary fibre is affected in both myopia and hyperopia. A second important function of the ciliary muscle is the regulation of the amount of aqueous fluid, controlled by the longitudinal fibres of this muscle. Malfunction may impede the drainage of aqueous through the Canal of Schlemm, ultimately leading to an increase of the fluid in the posterior chamber of the eye, thereby extending it.

Summary An attempt has been made in the foregoing to outline a theory of accommodation proposed some years ago by Robert Simpkins, wherein the lens is held to play a coordinating role rather than that of the sole operator. The eye’s external muscles in particular, are believed to be the primary agents. The crux of the argument is basically that the eyeball is extensible to the extent that it can be stretched anteriorly by reason of: (1) the thinness of the sclera in this region and the presence of elastic fibres immediately behind the cornea; (2) the orientation and interplay of the external muscles, which is such as to provide an agency for this operation; and (3) the position of the centre of rotation of the eyeball as being closer to the retina than to the front of the eye, thus enhancing the ability of the external muscles to perform conjugate movements (which do not entail an alteration of the length of the globe) and also to perform the disjugate movement of convergence (which lengthens the globe and thereby provides the necessary condition for accommodation). Thus the act of accommodation is viewed here in a different light, with ciliary body and lens participating in, rather than entirely controlling, the function. The structure of the anterior sclera and ciliary body, together with their close proximity to each other, is seen to make for coordinated rather than independent activity on the part of these units. The effect of refractive errors on the behavior of the external muscles has also been considered. The harmonious interplay between the opposing groups will undoubtedly be disturbed, and itself aggravate the condition.

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No attempt has been made here to discuss the treatment of refractive errors. Nor has the effect of glasses on the eyes been discussed. As might be imagined, however, glasses can do nothing whatever to restore harmonious activity to the external muscles; on the contrary, while correcting out-of-focus effects, they ensure the permanence of the muscular imbalance responsible, or – as is more likely – exacerbate the condition. As elsewhere in the body, muscles under-used tend to waste. If accommodation is brought about in the manner described here, it is essential that efforts should be made to encourage frequent changes of focus. Stasis is the deadly enemy of good sight and unrelieved fixity, as in sitting at a computer or watching television for long periods are very probable contributory causes of myopia, particularly among young children. It’s time for a reappraisal! Conflict of interest The author declared that there is no conflict of interest. Acknowledgements (1) Wolff’s Anatomy of the Eye and Orbit 8th Edition by Byron et al. CopyrightÓ 1997 Anatomy J. Bron, Ramesh C. Tripathi and Branda J. Tripathi. Published by Hodder and Stoughton Limited. Diagrams 2, 7, 8, 10 &11 reproduced by permission of Hodder Education. (2) Simpkins, R. Brooks: New Light on the Eyes. Lond., Vincent Stuart, 1958. (3) Simpkins, R. Brooks: ‘Oculopathy’, Bradford, Health Science Press, 1963. References [1] Meng Weihua, Butterworth Jacqueline, Malecaze Francois, Calvas Patrick. Axial length of myopia: a review of current research. Ophthalmologica 2001;225:127–34. [2] Greene PR. Myopia and extraocular muscles. Doc Ophthalmol Proc Ser 1981;28:163–9. [3] Bayramlar Hüseyin, Cekic Osman, Hepsßen Ibrahim F. Does convergence, not accommodation, cause axial-length elongation at near?. Ophthalmic Res 1991;31:304–8. [4] Hargrave, BK, Accommodation: The role of the external muscles of the eye. ISBN 0-646-46793-X (Earlier Edition: June 2004). Also: Barbara K Hargrave: DVD: Let Your Eyes do the Work, – Not the Glasses!. ISBN 978-0-9874009-6-3..

Accommodation: The role of the external muscles of the eye: A consideration of refractive errors in relation to extraocular malfunction.

Speculation as to optical malfunction has led to dissatisfaction with the theory that the lens is the sole agent in accommodation and to the suggestio...
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