Ocular Motility Disorders: Brainstem
Ji-Yun Park
Department of Neurology, Ulsan University Hospital, Ulsan, Korea
Ocular motility disorders: brainstem
Ji-Yun Park
Department of Neurology Ulsan University Hospital, Ulsan
PPRF/NPH,mVN riMLF/INC Vestibular nuclei
Accessory optic n.
Vestibular n.
y-group marginal zone Perioculomotor
MRF
INC n. prepositus SC
Flocculus region Pontine
n.
Visual cortex
Vestibular n.
Flocculus region
Eye muscles Motoneurons Retina
① Saccades
② VOR
③ OKN
④ Smooth pursuit
⑤ Vergencce
⑥ Gaze holding
Types of Eye Movements
Common final pathway
Supranuclear eye movement abnormalities
Selective involvement of eye movement - saccade(mainly) or pursuit involvement - vestibular eye movement : typically spared Bell’s phenomenon : Palpebral-oculogyric reflex
- Defective voluntary supraduction and a normal Bell’s phenomenon indicates a supranuclear defect ( ex. Parinaud syndrome, Progressive Supranuclear palsy)
Horizontal gaze
PPRF lesion Loss of horizontal saccades directed towards the side of the lesion, in all fields of gaze
Contralateral gaze deviation, in acute phase
Ipsilateral smooth pursuitand vestibular eye movementsmay be preserved
Bilateral lesions cause total horizontal gaze palsyand slowing of vertical saccades
“ipsilesional, horizontal gaze palsy”
: Loss of all conjugate movements Vergence and vertical movements are spared.
Horizontal gaze-evoked nystagmus on looking contralaterally.
Contralateral gaze deviation, in acute phase.
In the intact hemifield of gaze, horizontal movements may be preserved, but ipsilaterally directed saccades are slow by contralateral inhibition of VI n.
Abducens Nu. Lesion
Conjugate Horizontal gaze palsy
• PPRF lesion
: Selective loss of horizontal saccades directed towards the side of the in all fields of gaze
• Abducens nuclear lesion
: Impairment of saccades, smooth pursuit, VOR : normal centripetal saccades from contralateral side : associated peripheral facial nerve palsy
Abducens nerve palsy by nucleus and fascicle
Location of the Lesion
Associated Symptoms/Signs
Most Common Causes
Nucleus (pons)
Ipsilateral horizontal conjugate gaze palsy Ipsilateral facial weakness (peripheral)
Infarction Hemorrhage Neoplasm (metastasis) Fascicle
(pons)
Ipsilateral abduction paresis of one eye With associated neurological Sx/signs Contralateral hemiparesis Ipsilateral facial weakness and contralateral hemiparesis
Infarction Hemorrhage Neoplasm Demyelination
Abducens Fascicular lesion
Raymond syndrome
Ipsilateral abduction paresis + Contralateral hemiparesis Millard-Gubler syndrome
Ipsilateral abduction paresis + Ipsilateral facial paresis + Contralateral hemiparesis
Internuclear Ophthalmoplegia (INO)
Abducting Nystagmus
Clinical Features of Internuclear Ophthalmoplegia (INO)
• Weakness of the ipsi. MR for conjugate eye movements—
especially saccades, leading to “adduction lag”
• Nystagmus or postsaccadic drift on abduction of the eye contralateral to the lesion—dissociated nystagmus : Herring’s law of equal innervation
• Adduction may be preserved during convergence
• Skew deviation—hypertropia on the side of the lesion : interruption of central projections from otolithic input
• Vertical/torsional nystagmus in internuclear Ophthalmoplegia
• Bilateral INO also causes vertical gaze-evoked nystagmus, impaired vertical pursuit, and decreased vertical vestibular responses
MLF lesion
Neural integrators: vertical GEN SCC: hemi-seesaw nystagmus Graviceptive pathway: contralesional OTR
Internuclear ophthalmoplegia
dissociated nystagmus
adduction lag Vertical nystagmus
Skew deviation
See-saw nystagmus
INO, Adduction during convergence
• Changes in vergence in patients with INO are variable.
• Posterior INO(preserved convergence)
– caudal lesion with preservation of MR subdivision of the oculomotor nuclear complex
• Anterior INO(absent convergence)
– rostral lesion with preservation of MR subdivision of the oculomotor nuclear complex
• More systematic studies are required to better understand the changes in vergence that occur with INO
• 33 patients with dissociated torsional–vertical nystagmus and INO.
– 11 (33%): ipsiversive torsional in both eyes with vertical components in the opposite directions
– 18(55%): ipsiversive torsional nystagmus with a larger upbeat component in the contralesional eye
– 4(12%): ipsiversive torsional nystagmus with a greater downbeat component in the ipsilesional eye
• The patterns of jerky seesaw nystagmus in INO suggest a disruption of neural pathways from the contralateral vertical semicircular canals with or
Hypothetical explanations of the various patterns of dissociated torsional-vertical nystagmus in INO
(A) An excitatory three neuron VOR arc from the PC is linked to the ipsilateral SO and contralateral IR muscles.
Damage to this pathway by a lesion in the (MLF) (angled arrow) would cause primarily an upward deviation of the right eye and extorsion of the left eye (dotted arrows). The resulting corrective quick phases of nystagmus would be mostly downbeating in the right eye and intorsional in the left eye (lined arrow).
(B) By selective damage to the pathway from the AC (angled arrow), the nystagmus would be mostly extorsional in the right eye and upbeating in the left eye.
(C) Combined damage to the pathways from the PC and AC (angled arrow) would give rise to conjugate ipsiversive torsional nystagmus with opposite vertical components due to partial cancellation of vertical actions by the recti
Bilateral INO (WEBINO) with vertical gaze-evoked nystagmus
One and a half Syn.
Ipsilateral horizontal gaze palsy and internuclear ophthalmoplegia Only surviving horizontal conjugated movement is abduction of the contralateral eye Paralytic pontine exotropiaon looking straight ahead(one eye is deviated laterally)
Vergence and vertical movements may be spared
“Eight-and-a-half” syndrome
One-and-a-half syndrome
1. Involvement of excitatory burst neurons in the PPRF
: SCA2 (Horn AKE et al, Neuro-ophthalmology 1996;16:229-240) Experimental slow saccades by injecting lidocaine into the PPRF (Barton et al., 2003)
2. Lesions of the omnipuase neurons
: using experimental excitotoxins are also reported to cause slow horizontal and vertical saccades. (Kaneko CRS, J Neurophysiol 1996;75:2229-2242) 3. Both burst (PPRF) and omnipause cell populations may be affected : slow saccade after cardiac surgery (Hanson, et al. Ann Neurol 1986;20;209-217)
4. It is also possible that disturbance of other inputs to the posterior burst neurons (i.e., LLBN) could lead to slow saccades. For example, acute inactivation of the superior colliculus causes slow saccades in monkey.
Ahn BY, Choi KD, Kim JS, et al. Neurology, 2007
PMT : the cell group of the paramedian tracts DLPN : dorsolateral pontine nucleus – initiation (FEF : dorsal vermis)
NRTP : nucleus reticularis tegmenti pontis – maintenance (MT and MST : flocculus and paraflocculus )
Impaired ipsilateral smooth pursuit and gaze evoked nystagmus in paramedian pontine lesion
Damage to DLPN impairs ipsilesional smooth pursuit (May et al., 1988; Ahn et al., 2007), and NRTP lesions cause impairment of vertical smooth pursuit (Suzuki et al., 1999) and vergence eye movements (Gamlin and Clarke, 1995;
Rambold et al., 2004).
Key structures in the control of vertical gaze
riMLF INC PC
3rd nerve/nucleus 4th nerve/nucleus PPRF
MLF
6th nerve/nucleus Vestibular nucleus
Vertical saccades
Vertical gaze holding Vertical gaze Eyelid movements
Nuclear Oculomotor palsy
Oculomotor nuclear complex
Nuclear Oculomotor palsy
Subnuclei of the Oculomotor Nucleus and their Functions
Nuclear Oculomotor palsy
Obligatory lesions
Unilateral 3rd NP with contralateral SR paresis and bilateral partial ptosis Bilateral 3rd NP associated with spared levator function (mydriasis +/-) Possible nuclear lesions
Bilateral total 3rd NP Bilateral ptosis
An isolated weakness of any single muscle except the levator, SR, and MR muscles
Conditions that are not unlikely to be due to nuclear lesions Unilateral 3rd NP, with or without internal involvement, associated with normal contralateral SR function
Unilateral internal ophthalmoplegia Unilateral ptosis
Isolated unilateral or bilateral MR weakness
Fascicular Oculomotor palsy
Syndrome Associated sign Lesion Weber Contralateral hemiplegia Cerebral peduncle Benedict Contralateral hemiplegia
Tremor
Cerebral peduncle Substantia nigra Red nucleus Claude Contralateral ataxia Red nucleus
Superior cerebellar peduncle Cerebral peduncle Substantial nigra Red nucleus
CN III
Trochlear nerve palsy by Midbrain Lesion
Oculosympathetic tract
Superior cerebellar peduncle
Ipsilateral Horner syndrome
Ipsilateral ataxia Medial longitudinal fasciculus
Internuclear ophthalmoplegia
riMLF
Clinical Findings with Lesions of the riMLF
Unilateral Lesion:
• A mild and variable defect of downward saccades
• Loss of ipsitorsional quick phases (e.g., clockwise* quick phases are lost with right riMLF lesions)
• Static, contralesional torsional deviation with torsional nystagmus beating contralesionally
Bilateral lesion:
• More profound defect of vertical saccades that may be more pronounced for downward than upward eye movements
• Vertical gaze-holding, VOR and pursuit, and horizontal saccades are preserved
Unilateral riMLF lesions
INC : 눈돌림신경핵의 등가쪽(dorsolateral)에 위치하며 riMLF와 경계 (1) 수직 및 회선주시에서 신경적분체(neural integrator) (2) roll 평면에서 눈머리협조(eye-head coordination)
INC
Unilateral lesions of the INC
• Ocular counterroll
• Spontaneous torsional nystagmus (ipsitorsional) with downbeat nystagmus
• Gaze-holding deficit for torsional and vertical eye positions (neural integrator failure)
• Vertical oculomotor range decreased (up to 50%) and vertical saccades reduced in amplitude,
• Saccade velocity and horizontal eye movements normal
INC
PC
PC: INC로부터 반대편 INC와 눈운동신경핵(ocular motor nucleus)으로 가는 경로 : upward saccade decussation
Findings with lesions of the PC
• All classes of vertical eye movements impairment – especially upward,
– loss of vertical gaze-holding (neural integrator) function
• “Convergence-retraction nystagmus”
– Evoked by attempted upward or horizontal saccades – asynchronous convergent saccades
• Pathologic lid retraction while looking straight ahead (Collier’s sign)
– M group of neurons
• Mid-dilated pupils and light-near dissociation Mid dilated pupils and light near dissociation
Dorsal Midbrain Syndrome
Limitation of upward eye movements
• Saccades
• Smooth pursuit
• Vestibulo-ocular reflex
• Bell’s phenomenon
Dissociation of lid and eye movements Lid retraction (Collier’s sign), occasionally ptosis Disturbances of downward eye
movements
• Downward gaze preference (“setting sun” sign)
• Downbeating nystagmus
• Downward saccades and smooth pursuit may be impaired, but vestibular movements are relatively preserved
Disturbances of vergence eye movements
• Convergence-retraction nystagmus
• Paralysis of convergence
• Spasm of convergence
• Paralysis of divergence
• “A” or “V”-pattern exotropia
• Pseudo-abducens palsy Fixation instability (square-wave jerks) Skew deviation
Pupillary abnormalities (light-near dissociation)
Convergence excess- pseudoabducens palsy
Medial rectus motoneurons also receive inputs for vergence eye movements from neurons in the mesencephalic reticular formation, which lie dorsolateral to the oculomotor nucleus
• Monocular elevation palsy syndrome
• Supranuclear ‘‘double elevator palsy’’
• Prenuclear syndrome of the oculomotor nucleus
The dissociation between saccades and slow movements and the preservation of oculocephalic reflexes suggests that the monocular elevation palsy is of supranuclear origin. : SR(contra third nu’) + IO(ipsi third nu’) innervation
Crossed vertical gaze paresis
- Monocular elevation paresis and contralateral downgaze paresis from unilateral mesodiencephalic infarction - intact bell’s phenomenon - Subtle bilateral ptosis
- lesion near the oculomotor nucleus affecting ipsilateral downward gaze and contralateral upward gaze fibers, originating in the riMLF SR
IR
Vertical one-and-a-half syndrome
• Conjugate up-gaze palsy & monocular downward paresis
• Conjugate down-gaze palsy with monocular upward palsy
Upgaze palsy:
posterior commisure; oculomotor nucleus
Monocular downgaze palsy:
descending fibres to the subnuclei of the IR and SO just above the level of the oculomotor nucleus.
• downward palsy : bi riMLF
• Upward gaze palsy: Premotor fibers, originating from the ipsilateral riMLF and projecting onto the ipsilateral IO subnucleus and contralateral SR subnucleus.
• Impaired convergence and pupillary reactions to light
