Overview of anatomy and physiology of the ocular motor system

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Publisher Summary

This chapter reviews that the shared goal of all components of the ocular motor system is to maintain clear, single vision by placing and maintaining an object of visual interest on the fovea, the retinal region, with the highest density of photoreceptors and the best visual acuity. Several functional classes of eye movements coexist to meet this shared goal. These include saccades, smooth pursuit, vergence, optokinetic responses, and vestibular reflexes. It discusses that separate premotor or supranuclear command networks exist for initiation and modulation of each functional class of eye movements. These premotor networks converge upon a “final common pathway” that includes the ocularmotoneuron, the neuromuscular junction, and the final effector organ of eye movements— that is, the extraocular muscle. The chapter also reviews that the complexity and the variety of demands that the ocular motor system must meet in order to maintain stable vision require complex anatomy and physiology at every level from extraocular muscle to cortical ocular motor regions.

Introduction

The shared goal of all components of the ocular motor system is to maintain clear, single vision by placing and maintaining an object of visual interest on the fovea, the retinal region with the highest density of photoreceptors and the best visual acuity. Several functional classes of eye movements coexist to meet this shared goal. These include saccades, smooth pursuit, vergence, optokinetic responses, and vestibular reflexes. Anatomically and physiologically, separate premotor or supranuclear command networks exist for initiation and modulation of each functional class of eye movements. These premotor networks converge upon a “final common pathway” that includes the ocular motoneuron, neuromuscular junction, and the final effector organ of eye movements – the extraocular muscle. It has long been held true that all motoneurons and extraocular muscle fibers participate in all types of eye movements (Scott and Collins, 1973), though some may be more important for certain types of eye movements (Büttner-Ennever et al., 2001, Büttner-Ennever, 2005).

Modern biologic, anatomic, and physiologic techniques such as gene expression profiling, single cell recordings to determine cell electrophysiologic properties, lesional inactivation with observation of behavioral changes, and tracer methodologies to determine neural networks have greatly advanced understanding of the ocular motor system – to the point of challenging some classically held truisms such as the concept of a definitive “final common pathway” and absolute conjugacy of the ocular motor system (Mays et al., 1986, Zhou and King, 1998, Miller et al., 2002, Miller, 2003, Sylvestre et al., 2003). The complexity and variety of demands that the ocular motor system must meet in order to maintain stable vision require complex anatomy and physiology at every level – from extraocular muscle to cortical ocular motor regions.

Section snippets

Saccades

Saccades are rapid, conjugate eye movements with which we explore a visual scene or shift gaze to point the fovea at pertinent details in the visual world (Robinson, 1964). Because of the small foveal size, a high degree of accuracy is required. Saccades may be voluntary or reflexive and generated to actual targets or to memory for target location. They are fast eye movements, with most ranging between 300 and 500 °/s; and they are brief, most lasting less than 100 ms so as not to disrupt vision.

Overview and muscle actions

Six extraocular muscles control the movements of each eye: medial rectus, lateral rectus, superior rectus, inferior rectus, superior oblique, and inferior oblique. The medial rectus, superior rectus, inferior rectus, and inferior oblique are innervated by the oculomotor nerve (cranial nerve III). The lateral rectus is innervated by the abducens nerve (cranial nerve VI). The superior oblique is innervated by the trochlear nerve (cranial nerve IV).

Coordinated extraocular muscle action facilitates

Neuromuscular junction

In the classic skeletal muscle neuromuscular junction (NMJ) or motor end-plate, a nerve axon terminates on the mid-belly of a muscle fiber in a large synaptic expansion. The pre-synaptic terminal consists of enlargements of the terminal nerve fibers called synaptic boutons. These are separated from the post-synaptic muscle end-plate by the synaptic cleft, through which acetylcholine (ACh) passes after active vesicle release from the pre-synaptic terminal. The post-synaptic end-plate contains

Ocular motoneurons (cranial nerves and nuclei)

The ocular motoneurons for horizontal eye movements are located in the abducens and oculomotor nuclei. These motoneurons supply the lateral rectus and the medial rectus, respectively. For vertical eye movements, the motoneurons are in the trochlear and oculomotor nuclei. The trochlear motoneurons supply the superior oblique and the oculomotor motoneurons supply the superior and inferior rectus muscles and the inferior oblique.

Internuclear

The medial longitudinal fasciculus (MLF) carries signals from the abducens nucleus to the contralateral medial rectus portion of the oculomotor nucleus (Fig. 12). These signals allow conjugate horizontal eye movements with co-contraction of the ipsilateral lateral rectus and contralateral medial rectus muscles. The MLF also carries signals for vertical gaze from the medullary vestibular nuclei to the midbrain vertical gaze control centers. These signals are most important for vertical smooth

Burst and pause neurons

A combination of factors including the initial force to overcome the elastic inertia of the extraocular orbital tissues, high saccadic velocity, long saccadic duration, and the requirement for a high degree of accuracy to place the small fovea on target make saccades a very demanding task for the brain. Many of these demands are met directly by brainstem burst neurons that carry the immediate premotor or supranuclear saccadic command and that project monosynaptically to ocular motoneurons (Horn

References (216)

  • A.T. Bahill et al.

    Glissadic overshoots are due to pulse width errors

    Arch. Neurol.

    (1978)
  • R.W. Baloh et al.

    Quantitative measurement of saccade amplitude, duration, and velocity

    Neurology

    (1975)
  • S. Barash et al.

    Saccadic dysmetria and adaptation after lesions of the cerebellar cortex

    J. Neurosci.

    (1999)
  • R.R. Batton et al.

    Fastigial efferent projections in the monkey: an autoradiographic study

    J. Comp. Neurol.

    (1977)
  • S. Bense et al.

    Direction-dependent visual cortex activation during horizontal optokinetic stimulation (fmri study)

    Hum. Brain Mapp.

    (2006)
  • S. Bense et al.

    Brainstem and cerebellar FMRI-activation during horizontal and vertical optokinetic stimulation

    Exp. Brain Res.

    (2006)
  • A. Bergeron et al.

    Superior colliculus encodes distance to target, not saccade amplitude, in multi-step gaze shifts

    Nature Neurosci.

    (2003)
  • R. Bhidayasiri et al.

    A hypothetical scheme for the brainstem control of vertical gaze

    Neurology

    (2000)
  • D.C. Bienfang

    Crossing axons in the third nerve nucleus

    Invest. Ophthalmol.

    (1975)
  • G. Blohm et al.

    Direct evidence for a position input to the smooth pursuit system

    J. Neurophysiol.

    (2005)
  • A.Y. Bondi et al.

    Morphologic and electrophysiologic identification of multiply innervated fibers in rat extraocular muscles

    Invest. Ophthalmol. Vis. Sci.

    (1983)
  • P. Brodal

    The projection from the nucleus reticularis tegmenti pontis to the cerebellum in the rhesus monkey

    Exp. Brain Res.

    (1980)
  • J.A. Büttner-Ennever

    The extraocular motor nuclei: organization and functional neuroanatomy

    Prog. Brain Res.

    (2005)
  • J.A. Büttner-Ennever et al.

    Medial rectus subgroups of the oculomotor nucleus and their abducens internuclear input in the monkey

    J. Comp. Neurol.

    (1981)
  • J.A. Büttner-Ennever et al.

    Pathways from cell groups of the paramedian tracts to the floccular region

    Ann. N.Y. Acad. Sci.

    (1996)
  • J.A. Büttner-Ennever et al.

    Vertical glaze paralysis and the rostral interstitial nucleus of the medial longitudinal fasciculus

    Brain

    (1982)
  • J.A. Büttner-Ennever et al.

    Raphe nucleus of the pons containing omnipause neurons of the oculomotor system in the monkey, and its homologue in man

    J. Comp. Neurol.

    (1988)
  • J.A. Büttner-Ennever et al.

    Cell groups of the medial longitudinal fasciculus and paramedian tracts

    Rev. Neurol. (Paris)

    (1989)
  • J.A. Büttner-Ennever et al.

    Motoneurons of twitch and nontwitch extraocular muscle fibers in the abducens, trochlear, and oculomotor nuclei of monkeys

    J. Comp. Neurol.

    (2001)
  • J.A. Büttner-Ennever et al.

    Modern concepts of brainstem anatomy: from extraocular motoneurons to proprioceptive pathways

    Ann. N.Y. Acad. Sci.

    (2002)
  • J.A. Büttner-Ennever et al.

    Motor and sensory innervation of extraocular eye muscles

    Ann. N.Y. Acad. Sci.

    (2003)
  • J.A. Büttner-Ennever et al.

    Sensory control of extraocular muscles

    Prog. Brain Res.

    (2005)
  • U. Büttner et al.

    Saccadic dysmetria and “intact” smooth pursuit eye movements after bilateral deep cerebellar nuclei lesions

    J. Neurol. Neurosurg. Psychiatry

    (1994)
  • S.C. Cannon et al.

    Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey

    J. Neurophysiol.

    (1987)
  • M.R. Carry et al.

    Mitochondrial morphometrics of histochemically identified human extraocular muscle fibers

    Anat. Rec.

    (1986)
  • L. Chelazzi et al.

    Spontaneous saccades and gaze-holding ability in the pigmented rat. II. Effects of localized cerebellar lesions

    Eur. J. Neurosci.

    (1990)
  • B. Chen et al.

    The feedback circuit connecting the superior colliculus and central mesencephalic reticular formation: a direct morphological demonstration

    Exp. Brain Res.

    (2000)
  • G. Cheng et al.

    Transcriptional profile of rat extraocular muscle by serial analysis of gene expression

    Invest. Ophthalmol. Vis. Sci.

    (2002)
  • B. Cohen et al.

    Projections from the superior colliculus to a region of the central mesencephalic reticular formation (cmrf) associated with horizontal saccadic eye movements

    Exp. Brain Res.

    (1984)
  • M. Corbetta

    Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems?

    Proc. Natl. Acad. Sci. U.S.A.

    (1998)
  • J.D. Crawford et al.

    Generation of torsional and vertical eye position signals by the interstitial nucleus of Cajal

    Science

    (1991)
  • J.A. Cromer et al.

    Neurons associated with saccade metrics in the monkey central mesencephalic reticular formation

    J. Physiol.

    (2006)
  • K.E. Cullen et al.

    Analysis of primate IBN spike trains using system identification techniques. I. Relationship to eye movement dynamics during head-fixed saccades

    J. Neurophysiol.

    (1997)
  • K.E. Cullen et al.

    Analysis of primate IBN spike trains using system identification techniques. II. Relationship to gaze, eye, and head movement dynamics during head-free gaze shifts

    J. Neurophysiol.

    (1997)
  • J.L. Demer

    The orbital pulley system: a revolution in concepts of orbital anatomy

    Ann. N.Y. Acad. Sci.

    (2002)
  • J.L. Demer et al.

    Evidence for fibromuscular pulleys of the recti extraocular muscles

    Invest. Ophthalmol. Vis. Sci.

    (1995)
  • J.L. Demer et al.

    Evidence for active control of rectus extraocular muscle pulleys

    Invest. Ophthalmol. Vis. Sci.

    (2000)
  • J.L. Demer et al.

    Evidence for a pulley of the inferior oblique muscle

    Invest. Ophthalmol. Vis. Sci.

    (2003)
  • M. Dieterich et al.

    FMRI signal increases and decreases in cortical areas during small-field optokinetic stimulation and central fixation

    Exp. Brain Res.

    (2003)
  • I.M. Donaldson

    The functions of the proprioceptors of the eye muscles

    Phil. Trans. R. Soc. Lond. B Biol. Sci.

    (2000)
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