Chapter 12 - Nuclear, internuclear, and supranuclear ocular motor disorders

https://doi.org/10.1016/B978-0-444-52903-9.00018-2Get rights and content

Abstract

In the brainstem, lateral and vertical eye movements are controlled by separate structures, the former mainly in the pons and the latter in the midbrain. The abducens nucleus (VI) in the pons controls all ipsilateral eye movements, i.e., ipsilateral saccades as well as the horizontal vestibulo-ocular reflex (VOR). This nucleus contains the abduction motoneurons, but also the internuclear neurons involved in adduction, passing through the contralateral medial longitudinal fasciculus (MLF) before relaying in the third-nerve nucleus in the midbrain. Lesions affecting the abducens nucleus result in complete ipsilateral eye movement paralysis, and lesions damaging the MLF result in internuclear ophthalmoplegia, whereas an association of these two lesions leads to the “one-and-a-half” syndrome. Ipsilateral saccades are controlled by the ipsilateral paramedian pontine reticular formation located close to the sixth nucleus, whereas the ipsilateral VOR is controlled by the contralateral medial vestibular nucleus. Vertical eye movements are controlled by the third- and fourth-nerve nuclei in the midbrain. A lesion unilaterally affecting the third-nerve nucleus results in an ipsilateral third-nerve paralysis and a contralateral upgaze paralysis because of the decussation of the superior rectus motoneurons, at the level of the third-nerve nuclei. Vertical saccades are controlled by the rostral interstitial nucleus of the MLF (riMLF) located close to the third-nerve nucleus. Downward and upward saccade paralysis results from bilateral riMLF damage whereas upgaze paralysis usually results from a unilateral lesion affecting the region of the posterior commissure, suggesting that the suprareticular control of these two types of vertical saccade is distinct.

Introduction

Eye movement commands originate in diverse cerebral hemispheric areas for saccades, smooth pursuit, and convergence, or in the labyrinths for the vestibular ocular reflex. They are carried out in the brainstem by the immediate premotor (supranuclear and internuclear) structures and the ocular motor nuclei (see Chapter 2). Conjugate lateral eye movements are mainly organized in the pons, and vertical eye movements and convergence in the midbrain. In this chapter we will see the main types of eye movement paralysis resulting from brainstem lesions. Such types of abnormality are easily detected at the bedside by studying four main types of eye movement: (1) saccades, i.e., rapid eye movements made towards a visual target (such as the examiner's finger); (2) smooth pursuit, elicited by a small visual target moving slowly in front of the subject's eyes; (3) the vestibulo-ocular reflex (VOR), tested using oculocephalic movement, by passive movement of the subject's head; and (4) convergence, elicited by a small object moving slowly towards the subject's nose. Since the pathways of lateral and vertical eye movements are separate in the brainstem, these two types of eye movement will be reviewed successively. More details about the anatomy of these pathways may be found in Chapter 2.

Section snippets

Final common pathway: structures

The final common pathway of conjugate lateral eye movements begins in the abducens nucleus, located in the paramedian dorsal part of the lower pontine tegmentum (see Chapter 2). The abducens nucleus contains (Fig. 12.1, Fig. 12.2; see Fig. 2.4): (1) the motoneurons of the abducens nerve, which originate in the nucleus, first form the abducens nerve fascicles, coursing anteriorly through the lower part of the paramedian pontine reticular formation (PPRF) in the lower medial pontine tegmentum and

Final common pathway: structures

The final common pathway of vertical eye movements is formed by the oculomotor and trochlear nuclei and nerves. The motor neurons of the trochlear nerve decussate in the brainstem, as do those innervating the superior rectus muscle in the oculomotor nucleus, which originate in one oculomotor nucleus, cross the midline, and then pass through the contralateral oculomotor nucleus and nerve (Warwick, 1953). More details about the anatomical pathways serving vertical gaze may be found in Chapter 2.

References (85)

  • J. Bogousslavsky et al.

    Internuclear ophthalmoplegia, prenuclear paresis of contralateral superior rectus, and bilateral ptosis

    J Neurol

    (1983)
  • J.A. Büttner-Ennever et al.

    The reticular formation

  • J.A. Büttner-Ennever et al.

    Vertical gaze 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.

    Ptosis and supranuclear downgaze paralysis

    Neurology

    (1989)
  • S.C. Canon et al.

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

    J Neurophysiol

    (1987)
  • C.M. Chen et al.

    Wall-eyed bilateral internuclear ophthalmoplegia from lesions at different levels of the brainstem

    J Neuroophthalmol

    (2007)
  • H.J. Cho et al.

    The clinical syndrome and etiological mechanism of infarction involving the nucleus prepositus hypoglossi

    Cerebrovasc Dis

    (2008)
  • M.C. Chubb et al.

    Contribution of y-group of vestibular nuclei and dentate nucleus of cerebellum to generation of vertical smooth eye movements

    J Neurophysiol

    (1982)
  • D. Deleu et al.

    Dissociated ipsilateral horizontal gaze palsy in one-and-a-half syndrome: a clinico-pathologic study

    Neurology

    (1989)
  • D. Deleu et al.

    Impairment of smooth pursuit in pontine lesions: functional topography based on MRI and neuropathologic findings

    Acta Neurol Belg

    (1997)
  • C.M. Fisher

    Some neuro-ophthalmological observations

    J Neurol Neurosurg Psychiatry

    (1967)
  • E.M. Frohman et al.

    Quantitative oculographic characterization of INO in MS

    J Neurol Neurosurg Psychiatry

    (2002)
  • T.C. Frohman et al.

    The medial longitudinal fasciculus in ocular motor physiology

    Neurology

    (2008)
  • K. Fukushima et al.

    Neuronal activity related to vertical eye movement in the region of interstitial nucleus of Cajal in alert cats

    Exp Brain Res

    (1990)
  • B. Gaymard et al.

    Smooth pursuit eye movement disorders after pontine nuclei lesions in man

    J Neurol Neurosurg Psychiatry

    (1993)
  • G.M. Halmagyi et al.

    Jerk-waveform see-saw nystagmus due to unilateral mesencephalic lesion

    Brain

    (1994)
  • M.R. Hanson et al.

    Selective saccadic palsy caused by pontine lesions: clinical, physiological and pathological correlations

    Ann Neurol

    (1986)
  • C. Helmchem et al.

    Deficits in vertical and torsional eye movements after uni- or bilateral muscimol activation of the interstitial nucleus of Cajal of the rhesus monkey

    Exp Brain Res

    (1996)
  • C. Helmchem et al.

    Deficits in vertical and torsional eye movements after uni- and bilateral muscimol inactivation of the interstitial nucleus of Cajal of the alert monkey

    Exp Brain Res

    (1998)
  • C. Helmchem et al.

    Localizing value of torsional nystagmus in small midbrain lesions

    Neurology

    (2002)
  • A.K.E. Horn et al.

    Premotor neurons for vertical eye movements in the rostral mesencephalon of monkey and human: histologic identification byparvalbumin immunostaining

    J Comp Neurol

    (1998)
  • A.K.E. Horn et al.

    Saccadic premotor neurons in the brainstem: functional neuroanatomy and clinical implications

    Neuroophthalmology

    (1996)
  • R.S. Jampel et al.

    Monocular elevation paresis caused by a central nervous system lesion

    Arch Ophthalmol

    (1968)
  • J.L. Johnston et al.

    Sparing of the vestibulo-ocular reflex with lesions of the paramedian pontine reticular formation

    Neurology

    (1989)
  • E. Jouvent et al.

    Convergence nystagmus and vertical gaze palsy of vascular origin

    Rev Neurol

    (2005)
  • J.L. Juncos et al.

    Mesencephalic cholinergic nuclei in progressive supranuclear palsy

    Neurology

    (1991)
  • C.R.S. Kaneko

    Eye movement deficits after ibotenic acid lesions of the nucleus prepositus hypoglossi in monkeys

    I. Saccades and fixation. J Neurophysiol

    (1989)
  • J.R. Keane

    Internuclear ophthalmoplegia: unusual causes in 114 of 410 patients

    Arch Neurol

    (2005)
  • S. Kobayashi et al.

    Oculomotor nerve nuclear complex syndrome

    A case with clinicopathlogical correlation. Neuroophthalmology

    (1986)
  • G. Kommerell et al.

    Unilateral lesion of the paramedian pontine reticular formation

    Neuroophthalmology

    (1987)
  • R.J. Leigh et al.

    Eye movements in parkinsonism: it's saccadic speed that counts

    Neurology

    (2000)
  • Cited by (32)

    • Eye motor manifestations in children with neurometabolic disorders

      2022, Journal of the Formosan Medical Association
      Citation Excerpt :

      Typical presentation in patients with bilateral vestibular failure is oscillopsia only during head and body movements.11 From an anatomic perspective, the eye movement control can be approached as infranuclear, nuclear, internuclear, and supranuclear.12,13 The supranuclear ocular motor dysfunction, accounting for about 10% of eye movement problems, deserves special attention that a substantial number of neurometabolic diseases have supranuclear ocular motor problems.14

    • Nonvestibular Dizziness

      2021, Otolaryngologic Clinics of North America
      Citation Excerpt :

      The MLF links the horizontal gaze centers in the pons (sixth cranial nerve nucleus and the paramedian pontine reticular formation) and the third cranial nerve nucleus in the midbrain (including the medial rectus subnucleus).16 In the normal state, horizontal gaze in one direction is triggered by the ipsilateral pons, and signals are transmitted through decussating fibers to the contralateral MLF, and in turn, the contralateral 3rd cranial nerve nucleus in the midbrain, allowing for the contraction of the ipsilateral lateral rectus muscle and contralateral medial rectus muscle, thus facilitating conjugate horizontal gaze.17 A lesion of the MLF can cause disruption of this pathway, resulting in an INO—defined as an abnormality of adduction (slowed adduction, limited range of adduction, or complete failure of adduction) during horizontal gaze (Video 2).

    • Saccadic delay in multiple sclerosis: A quantitative description

      2020, Vision Research
      Citation Excerpt :

      They can result in visual complaints and are associated with greater general disability in MS. Hitherto, many studies described the extensive range of abnormalities based on clinical examinations. ( Coric, Nij Bijvank, van Rijn, Petzold, & Balk, 2018; Downey et al., 2002; Frohman, Frohman, Zee, McColl, & Galetta, 2005; Nerrant & Tilikete, 2017; Pierrot-Deseilligny, 2011; Prasad & Galetta, 2010). However, the clinical diagnosis can be challenging, especially when subtle abnormalities are involved (Frohman, Frohman, & O'Suilleabhain, 2003).

    • Convergence-Retraction Nystagmus in a Dog With Presumptive Ischemic Encephalopathy Following Acute Cervicothoracic Myelopathy

      2020, Topics in Companion Animal Medicine
      Citation Excerpt :

      Venus infarction of the brain is rare, and usually it is accompanied by hemorrhage;53 thus we hypothesized that our case represented an arterial infarction. Accepting the hypothesis of relation between the brain infarct and a presumptive spinal cord infarct, an embolus might have traveled from the cervicothoracic spinal cord arteries, through the ventral spinal artery which becomes basilar artery, following the basilar bifurcation and either the caudal perforating artery or the paramedian branches of the proximal portion of the caudal cerebral artery, and reaching dorsal midbrain.6,54 In humans, the pathway of the embolus after the basilar artery follows the posterior thalamo-subthalamic paramedian artery causing infarction in the rostral interstitial nucleus of medial longitudinal fasciculus and thus dorsal midbrain syndrome.55,56

    • Eye Movement Disorders: Conjugate Gaze Abnormalities

      2018, Liu, Volpe, and Galetta's Neuro-Ophthalmology: Diagnosis and Management
    View all citing articles on Scopus
    View full text