What is caused by the ciliary muscle

The ciliary muscle affects zonular fibers in the eye fibers that suspend the lens in position during accommodation , enabling changes in lens shape for light focusing. When the ciliary muscle contracts, it releases the tension on the lens caused by the zonular fibers fibers that hold or flatten the lens. This release of tension of the zonular fibers causes the lens to become more spherical, adapting to short range focus. The other way around, relaxation of the ciliary muscle causes the zonular fibers to become taut, flattening the lens, increasing long range focus.

Contraction of the lens happens when there is parasympathetic activation of the M3 muscarinic receptors on the ciliary muscles. This leads to contraction of the ciliary muscles, a consequent reduction in the size of the ciliary body, and a lessening of the tension on the lens, hence allowing the lens to spring back into a more spherical shape to accommodate for close vision.

Unlike the muscles of the iris which receives both types of autonomic innervation--the iris sphincter is exclusively innervated by parasympathetics and the iris dilator exclusively by sympathetics , the ciliary muscle receives only parasympathetic innervation.

The ciliary fibers have circular Ivanoff , [1] longitudinal meridional and radial orientations. According to Hermann von Helmholtz 's theory, the circular ciliary muscle fibers affect zonular fibers in the eye fibers that suspend the lens in position during accommodation , enabling changes in lens shape for light focusing. When the ciliary muscle contracts, it pulls itself forward and moves the frontal region toward the axis of the eye.

This releases the tension on the lens caused by the zonular fibers fibers that hold or flatten the lens. The other way around, relaxation of the ciliary muscle causes the zonular fibers to become taut, flattening the lens, increasing the focal distance , [3] increasing long range focus.

Although Helmholtz's theory has been widely accepted since , its mechanism still remains controversial. Alternative theories of accommodation have been proposed by others, including L. A cohort aged 35 years and older was required for the study, to investigate ciliary muscle characteristics from incipient presbyopia onwards. The data acquired from this sample were compared with a young cohort described previously, 17 aged 19—34 years mean Twenty-nine older volunteers aged 35—70 years, with no history of ocular abnormality or intraocular surgery were recruited for the study, using email announcements at Aston University.

The mean age of older participants was The younger and older cohorts together comprised 79 subjects aged 19—70 years mean The complete sample, therefore, represented youthful ciliary muscle, through to incipient and established presbyopia.

The study was approved by the Ethics Committee of Aston University and was performed in accordance with the tenets of the Declaration of Helsinki. Written, informed consent was obtained from all participants after explanation of the nature and possible consequences of the study.

Data were collected from the older cohort using the methods detailed previously. All further measurements were taken from the right eye only. Objective accommodative responses to 4. The targets subtended a constant angular subtense of 4. Average target luminance and Michelson contrast values were The scanning spot moves rapidly across the eye, acquiring A-scans in 0.

Forty degrees represented the minimum level of horizontal eye movement needed to view the distant targets, beyond the AS-OCT device, and meant that the optical axis of the instrument was through the sclera, rather than the cornea, reducing optical distortion.

Near targets, subtending 4. For each of the two sides of the eye imaged, all targets were positioned along the same axis, with subjects asked to ensure that the near stimuli appeared directly over the distant Maltese cross to reduce the possibility of varying acquisition planes.

Targets of the varying stimulus vergence levels were presented in random order, and multiple images were acquired of nasal and temporal ciliary muscle in each accommodative state, ensuring good visibility of the muscle in at least three images wherever possible.

Image analysis was performed by one examiner ALS using the inbuilt software Visante version 2. The examiner was masked to the accommodative state of subjects by use of a code to save image sets after scan acquisition. A refractive index of 1. Ciliary muscle maximum thickness Fig. The distance from the scleral spur to the inner apex of the muscle Fig. Figure 1. View Original Download Slide. Measurement of temporal ciliary muscle maximum thickness.

Figure 2. Measurement of distance from inner apex IA to scleral spur SS on the temporal side. After analysis of the three nasal and temporal images in which the ciliary muscle was most clearly defined, using an applied refractive index of 1.

The objective measures of accommodative response to the near stimuli were used to determine the magnitude of ciliary muscle biometric changes for each subject, per dioptre of accommodation. Emmetropic and myopic eyes were considered separately in light of previous findings of altered ciliary muscle morphology in axial myopes. Table 1 summarizes the effect of age on nasal and temporal ciliary muscle biometric characteristics.

Table 1. View Table. Changes in thickness measures with age also displayed some refractive-group dependent asymmetry. However, in emmetropic eyes, CM2 reduced with age on the temporal side, by 2. Ciliary muscle maximum width and distance from inner apex to scleral spur measures were obtained from only 37 of the 79 participants due to technical problems encountered with the AS-OCT device hard-drive failure and unrecoverable image files.

Despite the reduced data sets, the power of all statistical tests performed to ascertain the effect of age on these parameters was 0. Ciliary muscle maximum width increased significantly with age, by 2. Figure 3 illustrates graphically the effect of age on maximum ciliary muscle width. Figure 3. Nasal and temporal ciliary muscle maximum width versus age.

The reduction was similar on both sides: nasally, the decrease was 4. Figure 4 illustrates the relationship between age and ciliary muscle inner apex to scleral spur values. Figure 4. Nasal and temporal inner apex to scleral spur values versus age. CM25 shown by Sheppard and Davies 17 to increase significantly with accommodation in youthful eyes thickens in response to an accommodative stimulus throughout life. Figure 5 illustrates graphically the change in nasal and temporal CM25 with accommodative effort versus age.

Figure 5. Nasal A and temporal B CM25 versus age for minimum accommodation open circles and dashed regression line and in response to an 8. In conjunction with the thickening of CM25, Sheppard and Davies 17 highlighted a shortening of ciliary muscle anterior length and overall length measures during accommodation.

Both overall length and anterior length continue to reduce with accommodative effort throughout life. Figures 6 and 7 illustrate the change in nasal and temporal ciliary muscle anterior length in response to an 8.

Figures 8 and 9 show the effect of age on nasal and temporal ciliary muscle overall length changes in response to an 8. Figure 6. Nasal A and temporal B anterior ciliary muscle length in emmetropes versus age for minimum accommodation open circles and dashed regression line and in response to an 8. Figure 7. Nasal A and temporal B ciliary muscle anterior length in myopes versus age for minimum accommodation open circles and dashed regression line and in response to an 8.

Figure 8. Nasal A and temporal B ciliary muscle total length in emmetropes versus age for minimum accommodation open circles and dashed regression line and in response to an 8. Figure 9. Nasal A and temporal B ciliary muscle total length in myopes versus age for minimum accommodation open circles and dashed regression line and in response to an 8.

There are limited published data documenting the effect of age on human ciliary muscle morphology and contractility. The present investigation represents the largest in vivo study to date to investigate relaxed and contracted ciliary muscle characteristics across a broad range of subject ages. More posteriorly, CM25 is unchanged in both refractive groups with age, while CM50 and CM75 become progressively thinner temporally. Regarding ciliary muscle lengths, the overall length is unchanged with age for both refractive groups, while anterior length measures decrease on both sides in emmetropic, but not myopic, eyes.

Overall, the observed changes reflect a general antero-inwards shift of ciliary muscle mass throughout life. The anterior thickening of the ciliary muscle is in agreement with a recent in vivo MRI study 11 and earlier in vitro data.

The quantity of circular 31 and radial 6 fibers, compared to the longitudinal portion, may increase with age, resulting in a bulging of the anterior portion of the ciliary muscle.

Thinning of the posterior region of the human ciliary muscle has not previously been documented, although the present study has identified a significant reduction in temporal CM50 and CM75 in both refractive groups. Sheppard and Davies 17 highlighted increased thickness of CM50 and CM75 parameters on the temporal side, compared to the nasal aspect, in youthful eyes.

There was a significant activity of the muscle, clearly able to contract under binocular stimulation of accommodation. This supports a purely lenticular-based theory of presbyopia and it might stimulate the search for new solutions to presbyopia by making use of the remaining contraction force still presented in the aging eye.

Accommodation is a remarkable feature of the visual system allowing to focus object placed at different distances. The crystalline lens changes its shape in a controlled way due to forces applied by the ciliary muscle. The range of distances where the eye can focus properly is reduced with aging, reaching presbyopia the inability to accommodate at the end of the 4th decade of live. Both the crystalline lens and the ciliary muscle may have reduced accommodation functionality with age.

While it is accepted that the hardening of the lens plays a major role 1 , the functionality of the ciliary muscle seems to be at least partially preserved at presbyopic ages.

This is supported by studies where 3D ultrasound bio microscopy UBM 2 and magnetic resonance imaging MRI 3 , 4 were used to monitor the activity of the ciliary muscle during the accommodative process. While both techniques provide useful information to understand the mechanism driving accommodation, they must also face some disadvantages, as UBM is a contact technique the subject must have an ultrasound prove coupled to the eye and MRI is limited by image resolution and by a long acquisition time about several minutes.

In addition to the direct observation of the ciliary muscle, other evidences of the accommodative functionality of the muscle exist 5 , 6. If a near visual stimulus is presented to the eye, the ciliary muscle would contract releasing tensional forces of the zonular fibers that hold the crystalline lens.

Therefore, the lens in the near accommodative state would be less attached to the ocular walls than in the far unaccommodating form. By using this approach, it has been shown that some subjects from a group of presbyopes still had an increase in lens wobbling when accommodation was forced and that could be related to a potentially preserved functionality of the ciliary muscle 6.

Several studies directly visualizing the ciliary muscle 2 , 3 , 4 , or using indirect techniques 5 , 6 , have reported some functionality of the ciliary muscle at early presbyopic ages typically 40 to 60 years old. However, it is unknown whether the muscle still operates in older ages in senescence. The reason is that UBM and MRI methods, where contact with the eye and long gaze stability are required, do not seem to be the more optimal techniques to accurately assess the functionality of the ciliary muscle at advanced ages.

On the other hand, indirect methods to assess the functionality of the ciliary muscle have used commercially available Dual Purkinje Image eye trackers 7. It should be noticed, however, that these instruments were primary designed for measuring the direction of gaze. Even with this drawback, researchers estimated how the lens wobbles using data from the overshooting artifact that was typically observed after every saccadic movement of the eye 5 , 6. The artifact consists of an oscillation of the fourth Purkinje image rear lens reflection; PIV with respect to the first Purkinje image corneal reflection; PI.

It occurs typically after every saccadic movement but it cannot be interpreted as a post-saccadic oscillation of gaze but instead as an oscillation of the lens with respect to the cornea lens wobbling. While this approach permits an indirect quantification of the wobbling phenomenon, it still presents some problems regarding the physical quantification of lens wobbling, like the visualization of the movement eye trackers only measure and save gaze data and the extraction of data 8 , the tracking of Purkinje images and the customization of the illumination scheme that generates more clear Purkinje images see for instance the semi-circular array of infrared LEDs in Tabernero et al.

Recently, an instrument that overcomes those disadvantages has been presented 8. Based also on the tracking of Purkinje images, this instrument was specifically designed to measure crystalline lens and intraocular lens IOL wobbling. The measurement can be quickly performed a few seconds and requires no physical contact with the eye.

By using this new instrument, the objective of this article is to show a clear and robust evidence of a significant functionality of the ciliary muscle at advanced ages well beyond the typical onset of presbyopia.

A movement of the IOL in the capsular bag after a saccade i. IOL wobbling is the consequence of the braking deceleration of the eye during the last part of the saccade.

It can be experimentally visualized through an image reflected on the IOL PIV is reflected from the rear IOL surface compared to an image reflected from the cornea PI , recorded both at high speed frames per second for this particular application.

Assuming that the inertial oscillations of an IOL are essentially generated by a displacement of the lens with respect to the equilibrium position, we used an exact ray-tracing technique to calculate the positions of cornea and lens Purkinje images.

The results of the simulation are summarized in Fig. In this case, as in the experimental set-up, Purkinje images were generated by a semicircular array of LEDs. This figure described a well-aligned eye left panels where both semicircular reflections were well aligned and it compares to the situation where a 0. We also performed a simulation where the IOL is tilted around the vertical axis.

A semicircular array of point sources emits light towards an eye model implanted with an intraocular lens IOL. The IOL is placed initially co-aligned with the cornea left panels and also decentered horizontally by 0. Similar amounts of Purkinje images shifts where found in the real experiment when the saccadic movement was forced.

Figure 2 showed a real sequence of Purkinje images taken in one of the subjects participating in the study. The graphs below each image represented the horizontal position of PIV lens reflection with respect to the corneal reflection PI as a function of time.

The oscillating behavior of the lens IOL in this case was very clear and evident from the images. A movie clip version of this figure that includes the full temporal resolution range has been included as Supplementary video S1. It was possible that decentration or tilt of the IOL dominated alone the wobbling effect, although the combined effect of IOL tilting and decentration could certainly be possible as well. The sequence corresponds to subject 1.

Each frame was taken with an exposure time of 3. The graph below each image represents the horizontal distance from the PIV to the PI corneal reflex as a function of time. The green dot in each graph corresponded to the current frame on top. A very clear post-saccadic oscillatory behavior of the IOL can be inferred from this sequence. The previous section demonstrated that an IOL under inertial braking forces in the eye shows some clear and recordable movement.

Anatomically, the capsule of the lens, where the IOL is implanted, is joined to the ciliary muscle by the zonular ligaments.

A contraction of the ciliary muscle liberates tension on those ligaments and potentially increases IOL wobbling. For this reason, the relative magnitude of wobbling measured under different conditions on the same subjects can be used to directly test the hypothesis that the ciliary muscle works i.

We recorded IOL wobbling under binocular conditions fixating to a close visual stimulus 4D forcing accommodation as much as possible and also after paralyzing the ciliary muscle.

Figure 3 shows all data collected from the three advanced age subjects in the study, under natural conditions graphs on the left and after paralyzing the contraction of the muscle right. Data presented in these figures corresponded to three overlapped sequences of saccades.

Each saccade sequence was first normalized to zero when it reached the stationary point and after that, all three sets of data were manually overlapped starting all at the beginning point of the saccade. The solid line represents the fitting of the lens wobbling sequence to a harmonic function with an exponentially decaying amplitude. Movie clips of the three subjects under both conditions have been included as Supplementary movie clips Supplementary video S1 , Supplementary video S2 and Supplementary video S3 corresponding to subjects S 1 and S 2 and S 3.

In both situations, subjects fixated to the same stimulus placed at a distance of 4 D to the eye. Solid lines corresponded to an oscillatory model with exponential decaying amplitude fitted to the experimental data red open dots. Figure 3 qualitatively shows that paralyzing muscle contraction had an attenuating affect on IOL wobbling, although there was a significant variety in the magnitude of the effect between subjects and conditions.

Figure 4 shows the parameters that quantitatively characterized the wobbling of these three subjects, for both natural and pharmacologically paralyzed accommodation. Left and central panels show the maximum amplitude of IOL wobbling and the oscillation frequency while the panel to the right showed the refraction measured under both conditions.

The wobbling amplitude was defined as the maximum value of the first oscillating peak. Under natural conditions, that peak was larger than with the accommodation paralyzed. The oscillation frequency was obtained directly from the fitting of the data to the exponentially decaying harmonic functions.

Objective data on refraction for the far and near targets in each subject during the experiment was obtained with the binocular Hartmann-Shack wavefront sensor. Results were similar in both conditions revealing, as expected, no defocus changes between conditions. Maximum amplitude of IOL wobbling left panel , frequency of IOL wobbling middle panel and refractive state right panel for the three subject participating in the study.

Data is presented for the two conditions of the experiment natural and under pharmacologically induced cyclopegia. The color code represents each subject as in the previous figure black is s 1; green is s 2; red is s 3. IOL wobbling amplitude was clearly attenuated after paralyzing muscle contraction, which was presumably the main reason that validates the initial hypothesis that old subjects still maintain a significant functionality of the muscle contraction.

However, an alternative explanation to the attenuated IOL wobbling after instilling tropicamide in the eye could be related to differences in the saccades under natural and pharmacological conditions. This situation was further explored with measurements of the speed and amplitude of the ocular movements Fig.

Mean saccade velocity Fig. Also, the amplitude of the saccades Fig. These data were used as a calibration factor to estimate differences to the measurements when drops were instilled.