Efferent Visual System (Ocular Motor Pathways)

Our understanding of the anatomical pathways of the ocular motor system is incomplete. Nevertheless, detailed anatomical, physiologic, and pathologic knowledge of the ocular motor system has increased dramatically over the past several years because of results derived from primate model experiments, human electrophysiology testing, functional magnetic resonance imaging (fMRI) studies, and the clinical-pathologic-radiologic correlations of disorders in patients with documented eye movement abnormalities.

The ultimate purpose of the ocular motor system is to establish clear, stable, and binocular vision. To perform these tasks, 2 basic human eye movements exist:

1.gaze shift

2.gaze stabilization

These movements can be further divided into 6 functional systems or classes (see Anatomy and Clinical Testing of the Functional Classes of Eye Movements in Chapter 7):

1.vestibular

2.visual fixation

3.optokinetic

4.smooth pursuit

5.saccades

6.vergence

Each system appears to be under the control of—and modulated by—different regions of the brain (cortex) and brainstem, with considerable anatomical and functional overlap. This section provides an overview of the ocular motor system, with a detailed discussion of particularly clinically relevant structures. Interested readers can find a comprehensive description of the ocular motor system in the outstanding textbook by Leigh and Zee (Leigh RJ, Zee DS. The Neurology of Eye Movements. 4th ed. New York: Oxford University Press; 2006.) To facilitate learning, the discussion follows a top-to- bottom approach:

cortical control of eye movements, including basal ganglia (BG), thalamus, and superior colliculus (SC)

brainstem or premotor coordination of conjugate eye movements, including the vestibular-ocular system and cerebellum

ocular motor cranial nerves ( CNs III, IV, and VI) extraocular muscles (EOMs)

Cortical Input

The efferent visual system spans a large segment of the central nervous system, with many areas of the brain generating eye movements (Fig 1-23).

Figure 1-23 Overview of the cortical centers involved in the control of human eye movements. MST = medial superior temporal visual area, MT = medial temporal visual area. (Used with permission from Leigh RJ, Zee DS. The Neurology of Eye

Movements. 4th ed. New York: Oxford University Press; 2006.)

The following list of major anatomical structures and their functions helps set a foundation for discussion of the pathways for coordinating conjugate eye movements (Fig 1-24):

rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF): excitatory burst neurons that generate vertical and torsional saccades

interstitial nucleus of Cajal (INC): inhibitory burst neurons for vertical saccades and neural integrator for vertical and torsional gaze

region of riMLF and INC: inhibitory burst neurons for vertical and torsional saccades posterior commissure (PC): projecting axons from INC to contralateral CNs III, IV, and VI, and the INC

medial longitudinal fasciculus (MLF): major pathway for relaying signals within the brainstem nucleus raphe interpositus (RIP): omnipause cells

nucleus reticularis tegmenti pontis (NRTP): long-lead burst cells dorsolateral pontine nuclei (DLPN): neurons for smooth pursuit

nucleus prepositus hypoglossi (NPH): neural integrator for horizontal gaze

pontine paramedian reticular formation (PPRF): excitatory burst neurons that generate horizontal saccades and inhibitory burst neurons for horizontal saccades

medullary reticular formation (MedRF): inhibitory burst cells for horizontal gaze

cell groups of paramedian tracts (PMTs): neurons that project from the CN VI nucleus to the cerebellum

CNs III, IV, and VI: neurons that project directly to EOMs

vestibular nuclei (CN VIII): neurons that project to saccade generators and ocular motor cranial nerves

y-group cells: cells that project to CNs III and IV nuclei for vertical smooth pursuit and vertical vestibular eye movements

Figure 1-24 Schematic representation of sagittal section of brainstem showing the location of the important structures involved in eye movements. The shaded areas indicate, respectively, the mesencephalic reticular formation (MRF), paramedian pontine reticular formation (PPRF), and medullary reticular formation (MedRF). The dorsolateral pontine nuclei (DLPN) and y-group cells are not visible because this illustration is a mid-sagittal section and both cell groups are laterally located; they are best visualized on an axial view (through the rostral pons for DLPN and through the rostral medulla for y-group cells just above the inferior cerebellar peduncle). Key: III = oculomotor nucleus; IV = trochlear nucleus; VI = abducens nucleus; cg = central gray; INC = interstitial nucleus of Cajal; mamb = mamillary body; MLF = medial longitudinal fasciculus; N III = rootlets of the oculomotor nerve; N VI = rootlets of the abducens nerve; VII = facial nerve nucleus; nD = nucleus of Darkschewitsch; NPH = nucleus prepositus hypoglossi; NRTP = nucleus reticularis tegmenti pontis; PC = posterior commissure; riMLF = rostral interstitial nucleus of the medial longitudinal fasciculus; RIP = nucleus

raphe interpositus; sc = superior colliculus. (Modified from Büttner-Ennever JA, Horn AKE. Pathways from cell groups of the paramedian tracts to the floccular region. Ann NY Acad Sci. 1996;781:532–540.)

Saccadic system

The cortical, or supranuclear, input for generating saccadic eye movements is divided into 2 parallel and interconnected descending pathways: visually reflexive (parietal lobe) movements and memoryguided and volitional (frontal lobe) movements. In general, these cortical fibers project to the following structures in an organized framework (Fig 1-25):

subcortical structures: SC, BG, and thalamus

brainstem neural network or premotor neurons: several types of pontine neurons, including omnipause cells of the RIP and long-lead burst cells of the NRTP

brainstem saccade generators: PPRF and riMLF

motoneurons of the ocular motor cranial nerves: CNs III, IV, and VI

Figure 1-25 Schematic illustration of the saccadic system showing the relevant cortical centers for generating saccades. Note that this illustration is not meant to show all the hypothetical supranuclear pathways for the saccadic system. Key: BSG = brainstem saccadic generator; CN = caudate nucleus of the basal ganglia; CS = cerebellar structures; DLPC = dorsolateral prefrontal cortex; FEF = frontal eye field; PON = precerebellar pontine nuclei; PPC = posterior parietal cortex; PVC = primary visual cortex; SC = superior colliculus; SEF = supplementary eye field; SNr = substantia nigra pars

reticulata. (Used with permission from Kline LB. Neuro-Ophthalmology Review Manual. 6th ed. Thorofare, NJ: Slack; 2008:49.)

(Note that few cortical fibers project directly to the PPRF and riMLF.)

Visually guided movements require afferent system information either from the primary visual system and cortex or from the accessory afferent system. The visually guided (to seen or to remembered targets) and volitional saccadic supranuclear input comes largely from the frontal eye fields (FEFs, or Brodmann area 8). Cortical cells discharge prior to all voluntary and visually guided contralateral saccades. Supplementary eye fields (SEFs)—located on the dorsomedial surface of the superior frontal gyrus—receive input from the FEFs and are responsible for programming saccades, particularly as part of learned behavior. The FEF projects to the ipsilateral SC and many other areas, including the contralateral FEF, SEF, BG, NRTP, and RIP. Cortical projections to the SC also arise from the posterior parietal cortex (PPC) for visually guided reflexive saccades.

The SC is divided into a superficial (dorsal) and deep (ventral) part. The sensory signal (input from the visual cortex and retina) is processed mainly by the superficial SC. The motor signal originates within the deeper layers (the stratum griseum profundum and stratum album profundum) that receive position information from the more superficial layers. The SC projects contralaterally to multiple locations throughout the brainstem, most particularly to the RIP, NRTP, and DLPN.

Both the parietal and frontal lobe supranuclear pathways travel mainly to the SC; few fibers connect directly to brainstem premotor neurons. The supranuclear pathways also go through the BG (caudate nucleus, putamen nucleus, and substantia nigra pars reticulate). The BG appears to have several roles in the saccadic system, including inhibiting unnecessary reflexive saccades during fixation and helping in the control of voluntary saccades.

The thalamus (internal medullary lamina and pulvinar) is involved in the programming of saccades. It receives information from the cortex and brainstem and projects only to the cortex and BG. Therefore, the thalamus appears to relay messages from the brainstem to the cortical eye fields.

For information on clinical disorders of saccadic dysfunction, see Clinical Disorders of the Ocular Motor Systems in Chapter 7.

Smooth pursuit system

Saccadic and smooth pursuit eye movements were once thought to be derived from distinct supranuclear pathways; however, it now appears that considerable overlap exists between these systems. In addition, there are 2 major visual pathways, one for the movement of images (magnocellular: M cells) and the other for discrimination of images (parvocellular: P cells).

The smooth pursuit system for visual targets originates in V5—the human homologue of the medial temporal (MT) visual area in the rhesus monkey—where it receives input from the primary visual system, both from the cortex (striate and extrastriate areas) and likely from magnocellular input directly from the LGN (Fig 1-26). The medial superior temporal (MST) area is also involved in generating pursuit signals in response to moving stimuli. The area appears to be supplied with information about head movement as well as eye movement commands (efference copy) and thus generates pursuit movements to follow a target while the head is moving. Target recognition and selection probably receive additional input through the reciprocal connections to the posterior parietal cortex. Information from the MT and MST projects via the posterior portion of the internal capsule to the DLPN and lateral pontine nuclei, including the NRTP. From these pontine nuclei, projections are sent to the cerebellum (paraflocculus and dorsal vermis), with outflow signals to the vestibular nuclei and the y-group—a collection of cells at the inferior cerebellar peduncle. The smooth pursuit system is a double decussating pathway (the decussation occurs in both the pons and cerebellum); therefore, it can be simplistically considered an ipsilateral system.