New models of the oculomotor mechanics based on data obtained with chronic muscle force transducers

Several phenomenological models of the oculomotor mechanics that produce saccadic eye movements have been developed. These models have been based on measurements of macroscopic muscle and orbital tissue properties and measurements of eye kinematics during saccades. We recorded the forces generated by the medial and lateral recti during saccades in an alert, behaving monkey using chronically implanted force transducers. With this new data, we tested the ability of the classic saccade models to generate realistic muscle force profiles. Errors in the predictions of the classic saccade models led to a reexamination of the current models of extraocular muscle. Both a phenomenological, Hill-type muscle model and an approximation to Huxley's molecular level muscle model based on the crossbridge mechanism of contraction (distribution moment model) were derived and studied for monkey extraocular muscle. Simulations of the distribution moment model led to insights suggesting (i) specific modifications in the lumped force/velocity relationship in the Hill-type model that resulted in this type of phenomenological model being able to generate realistic dynamics in extraocular muscle during saccades; (ii) the distribution of activity in the different fiber types in extraocular muscle may be central to the characteristics exhibited by the muscle during saccades; (iii) the transient properties of lengthening muscle such as yielding are not significant during saccades; and (iv) the series elastic component in active muscle may be predominantly generated by the elastic properties of the cross-bridges.

[1]  L. Stark,et al.  Control of human eye movements: I. modelling of extraocular muscle , 1974 .

[2]  R. Close,et al.  Dynamic properties of inferior rectus muscle of the rat , 1974, The Journal of physiology.

[3]  C. Collins,et al.  Muscle tension during unrestrained human eye movements. , 1975, The Journal of physiology.

[4]  D. Robinson Oculomotor unit behavior in the monkey. , 1970, Journal of neurophysiology.

[5]  E S Luschei,et al.  Development of isometric tension in simian extraocular muscle , 1971, The Journal of physiology.

[6]  S. A. Wainwright,et al.  Mechanical Design in Organisms , 2020 .

[7]  Joel Miller,et al.  Extraocular muscle forces in alert monkey , 1992, Vision Research.

[8]  D. Robinson The mechanics of human saccadic eye movement , 1964, The Journal of physiology.

[9]  J. D. Porter,et al.  Structural organization of the extraocular muscles. , 1988, Reviews of oculomotor research.

[10]  C C Collins,et al.  Extraocular muscle forces in normal human subjects. , 1981, Investigative ophthalmology & visual science.

[11]  A. Huxley Muscle structure and theories of contraction. , 1957, Progress in biophysics and biophysical chemistry.

[12]  D. Robinson,et al.  A METHOD OF MEASURING EYE MOVEMENT USING A SCLERAL SEARCH COIL IN A MAGNETIC FIELD. , 1963, IEEE transactions on bio-medical engineering.

[13]  William H. Press,et al.  Numerical recipes in C , 2002 .

[14]  P. H. Schiller The discharge characteristics of single units in the oculomotor and abducens nuclei of the unanesthetized monkey , 2006, Experimental Brain Research.

[15]  D. Robinson,et al.  Mechanical components of human eye movements. , 1969, Journal of applied physiology.

[16]  A. Fuchs Saccadic and smooth pursuit eye movements in the monkey , 1967, The Journal of physiology.

[17]  A. Fuchs,et al.  Firing patterns of abducens neurons of alert monkeys in relationship to horizontal eye movement. , 1970, Journal of neurophysiology.

[18]  G. Zahalak A distribution-moment approximation for kinetic theories of muscular contraction , 1981 .

[19]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[20]  L. Stark,et al.  The main sequence, a tool for studying human eye movements , 1975 .

[21]  N. Curtin,et al.  Energetic aspects of muscle contraction. , 1985, Monographs of the Physiological Society.

[22]  A. Fuchs,et al.  A method for measuring horizontal and vertical eye movement chronically in the monkey. , 1966, Journal of applied physiology.

[23]  L Stark,et al.  Parametric sensitivity analysis of a homeomorphic model for saccadic and vergence eye movements. , 1976, Computer programs in biomedicine.

[24]  Joel Miller,et al.  Extraocular muscle sideslip and orbital geometry in monkeys , 1987, Vision Research.

[25]  C. Bell,et al.  Tension and rate of tension development during isometric responses of extraocular muscle. , 1971, Journal of neurophysiology.