Brainstem Stroke Annegret Dahlmann-Noor Consultant in Paediatric Ophthalmology and Strabismus Wales and West Vision Conference 26 June2015

Eye movement problems after stroke Background Incidence: Each year in England, approximately 110,000 people have a first or recurrent stroke and a further 20,000 people have a transient ischaemic attack Wales: 11,000 have a first or recurrent stroke per year, of which 6,000 new stroke events More than 900,000 people in England are living with the effects of stroke, with half of these being dependent on other people for help with everyday activities

Vision and eye movement problems after stroke Sensory (afferent): visual field defects Ocular motility (efferent): double vision from limitation of eye movements jumping images from nystagmus head turns to compensate for gaze palsy Processing: Charles Bonnet, palinopsia

Background Most strokes are ischaemic (80-85%), some are haemorrhagic Eye movement problems after stroke Background Most strokes are ischaemic (80-85%), some are haemorrhagic Two main blood supplies to the brain: Carotid Vertebral/basilar arteries

Eye movement problems after stroke Background 27% of ischaemic strokes affect the vertebral/basilar arteries Symptoms of brainstem stroke: vertigo - dizziness double vision/binocular visual disturbance generalised weakness

Blood supply to brainstem and cerebellum Eye movement problems after stroke Blood supply to brainstem and cerebellum Posterior cerebral artery Branches of bifurcation of basilar artery: III ncl/fasc Superior cerebellar artery: IV ncl/fasc Anterior inferior cerebellar artery: VI ncl/fasc Posterior inferior cerebellar artery Vertebral artery

Superior cerebellar artery Eye movement problems after stroke Superior cerebellar artery Branches of basilar artery

Branches of basilar artery and of anterior inferior cerebellar artery Eye movement problems after stroke Branches of basilar artery and of anterior inferior cerebellar artery Paramedian branches of basilar artery

Eye movements Smooth pursuit: eyes follow a moving target Eye movement problems after stroke Eye movements Smooth pursuit: eyes follow a moving target Saccades: gaze rapidly jumps from one fixation point to another Vergence eye movements: eyes do not move in parallel, but in relation to each other: convergence: when looking at something close up Vestibulo-ocular reflex (VOR): the signal triggering eye movements comes from the balance organ (labyrinth), which keps the image of the visual surroundings stable on the retina during head movements Optokinetic reflex: triggered by moving visual targets, consists of smooth pursuit and saccades Gaze holding: ability to keep the eyes in an eccentric position

The players: the team on the ground Eye movement problems after stroke The players: the team on the ground Six muscles on each eye Move eye horizontally, vertically, and tilt it in- and outwards

The players: the middle management Eye movement problems after stroke The players: the middle management Vertical eye movements Interstitial nucleus of Cajal (INC) Rostral interstitial nucleus of the MLF (riMLF) Horizontal eye movements Parapontine reticular formation (PPRF) Abducens nucleus The runner: Medial longitudinal fasciculus (MLF)

The players Vertical eye movements Interstitial nucleus of Cajal Eye movement problems after stroke The players Vertical eye movements Interstitial nucleus of Cajal Rostral interstitial nucleus of the MLF Horizontal eye movements Paramedian pontine reticular formation Abducens nucleus

The players: the supreme controls Eye movement problems after stroke The players: the supreme controls Frontal eye field: sends signals to the third nerve nucleus on the same side, and the paramedian pontine formation on the opposite side: horizontal saccades, and to the rostral interstitial nucleus of the MLF (riMLF) for vertical saccades Parietal eye field: production of smooth pursuit eye movements, also participates in the production of saccades (more to novel visual stimuli rather than to remembered targets) Paramedian pontine reticular formation: excitatory burst neurons that start the “pulse” From: Oculomotor Dysfunction in Amyotrophic Lateral Sclerosis:  A Comprehensive Review Arch Neurol. 2011;68(7):857-861. doi:10.1001/archneurol.2011.130

The action: midbrain Oculomotor nucleus Trochlear nucleus Eye movement problems after stroke The action: midbrain Oculomotor nucleus Trochlear nucleus Rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF)

Presentation title to go here Fourth cranial nerve

Fourth cranial nerve MRI courtesy of Dr Indran Davagnanam Presentation title to go here Fourth cranial nerve MRI courtesy of Dr Indran Davagnanam

Third cranial nerve infarct Presentation title to go here Third cranial nerve infarct

Oculomotor nerve paresis Presentation title to go here Oculomotor nerve paresis lack of adduction: eye deviated outwards lack of elevation: eye deviated downwards lid droop (ptosis)

Midbrain Control of vertical and torsional eye movements Eye movement problems after stroke Midbrain Control of vertical and torsional eye movements Input from cortex (vertical and torsional saccadic commands and vertical gaze-holding signal) Input from lower brainstem (vestibular and pursuit signals) Generation of vertical saccades: rostral interstitial nucleus of the MLF (riMLF): projects bilaterally for eye elevation (superior rectus and inferior oblique), ipsilaterally for eye depression, also projects to the interstitial nucleus of Cajal (INC) From: T.C. Frohman et al. Neurology 2008;70:e57-e67

Midbrain Example: left head tilt Eye movement problems after stroke Midbrain Example: left head tilt Otoliths (balance organ) trigger signal to extorters (inferior oblique and inferior rectus muscles) in the right eye (cross midline) and to intorters of left eye (superior oblique and superior rectus muscles) in the left eye (double crossing) plus: torsional fast phases mediated by riMLF INC: neural integration of vertical and torsional gaze, eye-head coordination during roll movements, and inhibitory burst neurons for vertical eye movements lesions: intorsion and elevation of the right eye and extorsion and depression of the left eye = skew deviation From: T.C. Frohman et al. Neurology 2008;70:e57-e67

Lesions of vestibular nuclei Eye movement problems after stroke Lesions of vestibular nuclei Lesions of vestibular nuclei, for example lateral medullary infarction (Wallenberg syndrome): Vestibular imbalance: nystagmus or skew deviation and impairment of gaze holding for all types of conjugate eye movement Ocular tilt reaction (OTR): skew deviation, hypotropia on same side, lower eye extorsion and head tilt towards side of lesion Lateropulsion: eyes deviate conjugately towards the side of the lesion if lids are closed, or with saccades Top: isolated vestibular nucleus infarct. Bottom: different patient - marked skew deviation T.C. Frohman et al. Neurology 2008;70:e57-e67

Dorsal midbrain syndrome Eye movement problems after stroke Dorsal midbrain syndrome Lesions of the riMLF: loss of upward gaze (vestibulo-ocular reflex and Bell phenomenon may be spared) slowing of vertical saccades below the horizontal meridian, convergence weakness, convergence-retraction nystagmus, light-near dissociation of pupils, lid retraction Patient with dorsal midbrain syndrome T.C. Frohman et al. Neurology 2008;70:e57-e67

Eye movement problems after stroke Stop and recap 1. Strokes affecting the basilar artery or its brances can affect eye movements, causing double vision and jumping images 2. There are different types of eye movements – smooth pursuit, saccades, vergences, and eye movements in response to changes in head or body position 3. Areas in the cortex trigger saccades (fast eye movements) and pursuits. 4. Centres in the midbrain forward signals to the cranial nerves which innervate the eye muscles that move the eyes vertically and in torsion. 5. Lesions in these pathways can cause loss of saccades and vertical eye movements, and a complex change in vertical and torsional eye movements (skey deviation)

Now the easy stuff: horizontal eye movements Eye movement problems after stroke Now the easy stuff: horizontal eye movements Abducens nucleus

Horizontal eye movements Eye movement problems after stroke Horizontal eye movements Two types of nerve fibres in the abducens nerve: a) motoneurons to lateral rectus muscle on the same side b) internuclear neurons, which project up the contralateral medial longitudinal fasciculus to contact medial rectus motoneurons of the oculomotor nucleus => Conjugate, horizontal eye movements . Details of the descending projection involved in the volitional control of horizontal saccadic eye movements. Excitatory pathways are shown in orange and the reciprocal inhibitory pathways are shown in blue. T.C. Frohman et al. Neurology 2008;70:e57-e67

Eye movement problems after stroke Abducens nucleus Inputs: vestibular and optokinetic inputs from vestibular nuclei Saccadic commands originate from burst neurons of the pontine and medullary reticular formation Descending smooth pursuit pathway via cerebellar nuclei to abducens nucleus . Projections involved in the activation of the left lateral semicircular canal. This figure illustrates the projections involved during the activation of the left lateral semicircular canal. T.C. Frohman et al. Neurology 2008;70:e57-e67

Eye movement problems after stroke Stop and recap From the abducens nucleus, signals go the lateral rectus muscle on the same side and medial rectus on the opposite side Those signals are triggered by messages from the vestibular nuclei (tilting head), cerebellar nuclei (moving body), burst neurons in the PPRF, and the frontal and parietal eye fields.

How things can go wrong in brainstem stroke Eye movement problems after stroke How things can go wrong in brainstem stroke Abducens nucleus lesions Medial longitudinal fasciculus lesions Combined lesions of MLF and abducens nucleus PPRF lesion

How things can go wrong in brainstem stroke Eye movement problems after stroke How things can go wrong in brainstem stroke 1. Abducens nucleus lesions: paralysis of lateral rectus muscle on the same side and medial rectus muscle on the opposite side (vergence spared) Usually associated with involvement of adjacent structures: facial nerve fascicle, MLF, paramedian pontine reticular formation

How things can go wrong in brainstem stroke Eye movement problems after stroke How things can go wrong in brainstem stroke 1. Abducens nucleus lesions: paralysis of lateral rectus on same side and medial rectus muscle on opposite side, vergence spared Usually associated with involvement of adjacent structures: facial nerve fascicle, MLF, paramedian pontine reticular formation MRI courtesy of Dr Indran Davagnanam

MLF 2. MLF lesions: Internuclear ophthalmoplegia (INO): Eye movement problems after stroke MLF 2. MLF lesions: Internuclear ophthalmoplegia (INO): paresis of adduction on the side of the lesion, abduction overshoot of the contralateral eye Often accompanied by skew deviation (disruption of the otolithic-ocular connections), gaze-evoked vertical nystagmus, impaired vertical pursuit, decreased vertical vestibular responses, small-amplitude saccadic intrusions Volitional saccadic pathway with a lesion in the right medial longitudinal fasciculus (MLF) that results in an internuclear ophthalmoparesis (INO). Volitional saccadic pathway with a lesion in the right MLF that results in an INO during an attempted saccade to the patient's left. T.C. Frohman et al. Neurology 2008;70:e57-e67

Eye movement problems after stroke INO INO continued: Usually orthotropic (straight eyes) or exophoric (latent outward drift) in primary position, except when associated with skew deviation Occasionally exotropia (manifest outward strabismus) in bilateral INO (wall-eyed bilateral INO, WEBINO) T.C. Frohman et al. Neurology 2008;70:e57-e67

Eye movement problems after stroke One and a half Right internuclear ophthalmoparesis (INO) upon attempted gaze to the left. T.C. Frohman et al. Neurology 2008;70:e57-e67 3. Combined lesion of one MLF and the adjacent abducens nucleus, or its inputs: paresis of all conjugate movements except for abduction of the eye on side opposite the lesion: one and a half syndrome If acute, may present with marked exotropia Deviated eye (opposite the side of the lesion) may show marked nystagmus

Eye movement problems after stroke PPRF lesions 4. Lesions of the PPRF Loss of saccadic burst neurons: loss of saccades and quick phases of nystagmus to the side of the lesion Pontine lesions may cause unilateral defect of smooth pursuit

Eye movement problems after stroke Stop and recap Abducens nucleus lesions: loss of abduction same side, loss of adduction opposite side; often involve PPRF as well, so horizontal gaze palsy Medial longitudinal fasciculus lesions: impaired adduction on the side of the lesion, abduction overshoot of the opposite eye Combined lesions of MLF and abducens nucleus: affects all horizontal eye movements except for abduction on the side opposite the lesion PPRF lesion: loss of saccades to the side of the lesion

The last part of the talk: cerebellum and cortex stroke Eye movement problems after stroke The last part of the talk: cerebellum and cortex stroke

Cerebellar infarct Three arteries from the posterior circulation: Eye movement problems after stroke Cerebellar infarct Superior cerebellar artery Anterior inferior cerebellar artery Posterior inferior Three arteries from the posterior circulation: Posterior-inferior cerebellar artery Anterior-inferior cerebellar artery Superior cerebellar artery Infarcts often associated with brainstem infarcts, so mixed clinical picture

Eye movement problems after stroke Cerebellar infarct Posterior-inferior cerebellar artery: acute vertigo and nystagmus, possibly gaze-evoked nystagmus Anterior-inferior cerebellar artery: vertigo, vomiting, hearing loss, facial palsy, ipsilateral limb ataxia Superior cerebellar artery: ataxia of gait and limbs and vertigo, saccadic contrapulsion (overshooting of contralateral saccades, undershooting of ipsilateral saccades; attempted vertical saccades are oblique)

Cerebral hemispheric lesions Eye movement problems after stroke Cerebral hemispheric lesions acute lesion: eyes often deviated conjugately toward the side of the lesion; often after large stroke involving right post-rolandic cortex; associated with visual hemineglect

Cerebral hemispheric lesions Eye movement problems after stroke Cerebral hemispheric lesions chronic lesion: no resting deviation; persistence of gaze deviation Small-amplitude nystagmus Deficit of horizontal pursuit when tracking targets moving towards the side of the lesion (OKN)

Bilateral Frontoparietal lesions Eye movement problems after stroke Bilateral Frontoparietal lesions Acquired Ocular Motor Apraxia Loss of voluntary control of eye movements Preservation of reflex movements, including vestibulo-ocular reflex and quick phases of nystagmus Can be associated with difficulty in lid opening Balint syndrome: loss of voluntary eye movements plus disturbance of visual attention

Management of ocular motility problems Eye movement problems after stroke Management of ocular motility problems Prism treatment Occlusion Ptosis props Surgery/botulinum toxin

Eye movement problems after stroke Principles of surgery Enhance muscle action by shortening a paretic muscle, or by transposing a different muscle towards the insertion of a paralytic muscle Create a matching defect by weakening a muscle, to reduce double vision

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