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Extraocular Muscle Forces in Normal Human Subjects

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Extraocular Muscle Forces in Normal Human Subjects Extraocular muscle forces in normal human subjects Carter C. Collins, Melvin R. Carlson, Alan B. Scott, and Arthur Jampolsky Actively developed horizontal muscle forces and tissue stiffnesses were measured in 29 normal orthophoric volunteer subjects (18 to 33 years old) by means of noninvasive length-tension forceps. Mean active fixation force developed at 50 deg extreme gaze was 26% greater for the medial rectus (74.8 gm) than for the lateral rectus (59.1 gm). The variation of maximum active force among individuals was 2:1 (48 to 103 gm). These muscles developed up to 25% of their maximum active force out of their field of action. Active (counter) hysteresis force differences of over 10 gm were measured between nasal and temporal gaze directions. This study suggests that a muscle which develops a maximum active force of less than 45 gm ivould be suspect as paretic. Variations from the normal pattern of reciprocal innervation, reflected in the graded, active force of individual muscle contraction, may help in understanding some types of oculomotor pathology. The mean tissue stiffness -restraining movement of the globe in the nasal direction (1.05 gm/deg) is 11 % greater than in the temporal direction (0.94 gm/deg). This is consistent with a stronger medial rectus balanced by a greater load. Variation of stiffness of 2:1 was observed among individuals; 0.8 to 1.7 gm/deg pulling nasally and 0.77 to 1.2 gm/deg temporally. Passive hysteresis and viscous force differences of over 10 gm were observed between the passive forced pull and normal spring-return of the eye. Large stiffnesses may be normal if balanced by large active forces. Abrupt changes of the length-tension curve indicate the magnitude and location of restrictions. Key words: length-tension, active force, stiffness, hysteresis, reciprocal innervation, restrictions AAccurate information is needed on the ac- We also need to know the normal load (stiff- tive and passive forces that are present at a ness) that must be overcome to move the eye given positioning of the eyes. Strabismus from a certain eye position. This information diagnosis and surgical planning benefit from can be useful when making a differential knowing the magnitude of the actively devel- diagnosis of the strabismus disorder and oped forces of each muscle as well as the bal- can aid in decisions regarding surgical man- ance of agonist and antagonist active forces. agement. Most reported load (stiffness) values or ac- tive muscle forces are in one direction only1"3 or are unaccompanied by data on the relaxing From The Smith-Kettlewell Institute of Visual Sciences, antagonist muscle force acting against the San Francisco, Calif. 3 6 Supported by National Institutes of Health Research agonist force. " In addition, much of this grants 5R01-EY 01719, 5P30 EY 01186, and 5S01 data is from strabismic eyes, possibly non- RR 05566, and The Smith-Kettlewell Eye Research representative of normal subjects.5' 6 There is Foundation. an obvious need for such information from a Submitted for publication Dec. 21, 1979. comprehensive sample of normal individuals. Reprint requests: Dr. Carter C. Collins, Smith-Ket- tlewell Institute of Visual Sciences, 2232 Webster St., Using normal subjects, we have measured San Francisco, Calif. 94115. the magnitude of active (isometric) force de- 652 0146-0404/81/050652+13$01.30/0 © 1981 Assoc. for Res. in Vis. and Ophthal., Inc. Volume 20 Number 5 Extraocular muscle forces in human subjects 653 Fig. 1. Length-tension forceps as used with a subject. Electronic strain gauges in the forceps shanks measure force. Note the forceps grasping the nasal limbus. A small loudspeaker (ultra- sonic pulse source) mounted on the frame of a pair of glasses can be seen. Time of flight of sound from loudspeaker to a microphone mounted above the tip of the forceps is proportional to the distance of the forceps from the source (fixed on the head). veloped separately by the medial rectus 110 gm) and forceps-positioned eye displacement muscle and by the lateral rectus muscle dur- (up to 20 mm). ing fixation in horizontal gaze. We have also The forceps employed were the large Pierse measured the magnitude of the load (stiff- straight fixation forceps (Storz Model E1942-13). ness) that these muscles must overcome to The broad tip of the forceps permit a firm grip of the limbal conjunctiva. The shanks of the forceps move the eye in each direction. tip were milled to a width of 0.7 mm for a distance These data provide a quantitative baseline of 15 mm up the shank. Semiconductor strain of the active and passive forces acting on a gauges were mounted on these narrow beams to normal eye. In a patient with strabismus, dif- measure any force applied at right angles to the ferences from these values aid in making a long axis of the forceps. The force required to ro- differential diagnosis resulting in more accu- tate the globe or the force applied by muscles to rate quantitative planning of strabismus the globe as the forceps held the globe in a fixed surgery. position could then be measured.7 Force readings were linear within ±2% over a ±150 gm range. Methods and protocol Hysteresis was less than ±0.50 gm after ±100 gm We have measured 29 normal volunteer sub- of load had been applied.7 A small microphone jects ranging in age from 18 to 33 years. They with an opening near the tip of the forceps de- showed no pathological conditions. All were tected inaudible sound pulses from an ultrasonic within 2 A of being orthophoric. source attached to the head of the subject. This A newly developed clinical technique previ- ultrasonic device served as a sonar system and ously described7 was employed for assessing and provided a constant indication of the distance be- recording the individual medial and lateral rectus tween the ultrasonic source and the forceps tip. active muscle force as a function of eye position Because the ultrasonic source was fixed on the over a 100 deg range of horizontal gaze. The load head, a measure of eye position was obtained from (stiffness) of the orbital tissues was also deter- a knowledge of the forceps tip location. Position mined over a 60 to 100 deg range of eye position. accuracy was within ±3% over the range of ±50 The technique utilized a specially instrumented deg of eye position. forceps to obtain a measurement of force (up to This noninvasive forceps and ultrasonic sound Invest. Ophthalmol. Vis. Set. 654 Collins et al. May 1981 L-T FORCEPS PROTOCOL Temporal Passive Load ^ 500 0 50° Eye Position Nasal Temporal LMR Active Forces Track Hold •<V:-. %f\ Nasal Passive Load Pull LLR Active Forces Track Hold Fig. 2. Length-tension forceps protocol for left eye measurements. A, Subject maintains 30 deg right fixation with right eye. The left eye is slowly (10 deg/sec) rotated temporalward and returned several times. The resulting load (stiftness) record represents the resistance to tem- poral rotation of the eye. B, Forceps hold the left eye steadily at a 50 deg temporalward rotation as subject tracks a slowly (10 deg/sec), smoothly moving target from 50 deg left to 50 deg right and return with the right eye. A plot of actively developed force, FM, of the isolated left medial rectus muscle as a function of gaze effort can be determined. C, A mirror image of A results in the load (stiffness) for nasal rotation. D, Mirror image of B results in the active force, FL, of the isolated left lateral rectus muscle as a function of gaze effort can be deter- mined. source are shown in Fig. 1. The source of ul- a function of eye position. This instantaneous dis- trasound can be seen mounted on the frame of a play of data enabled us to determine whether the pair of glasses. The ultrasonic source may also be data were in the expected range, were reasonably mounted on a headband, with a flexible piece of linear, and were free of artifacts. If not, the mea- heavy copper wire to permit adjustment for surements were immediately repeated for confir- proper location (approximately 2 inches temporal mation. These data were simultaneously recorded to the outer can thus of the subject's eye). The ul- on a multitrack FM tape recorder for later play- trasonic source provides a sound field immediately back on an X-Y chart recorder to provide a perma- in front of the eye. This permits the position of the nent record. eye (forceps tip) to be monitored continuously From the family of innervated length-tension with force measurements over a 100 deg range of curves of oculorotary muscle it can be shown that eye position. active and elastic forces operate independently of The forceps are held perpendicular to the globe each other and can be separately measured. In this at all times in order to obtain proper readings of study we measured the stiffness associated with force and position. An error in the recorded force innervated muscles, not passive muscles, perse. If can result from misalignment. If the forceps are the muscle innervation remains constant, then the held within ±15 deg of the perpendicular to the force changes due to varying the length of the surface of the globe, the geometrical cosine error muscle are elastic in nature as seen from the con- is within 3% for force and position readings. A stant slope of the length-tension curve.0' fi Con- separate observer checked that the forceps were versely, force changes made with a constant mus- held within this angle at all times.
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