Structure-Function: Central vestibular syndromes
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1 Structure-Function: Central vestibular syndromes Skews Nystagmus Tilts
2 Objectives An introduction to the basic principles of eye movement control An introduction to the types of central vestibular clinical syndromes. Examples of bringing basic physiology to the bedside. Examples of basic science investigations using clinical disorders as the experimental model.
3 The dominance of the fovea G Westheimer Courtesy, Chris Kennard
4 Function of eye movements Serve the needs of vision, and specifically those of the fovea where spatial acuity is best. Bring images onto the fovea (saccades and vergence) Keep images still on the fovea, for best spatial resolution (vestibular, pursuit and vergence)
5 Oculomotor exam
6 Dominant mechanical orbital forces Elastic restoring forces to eye position If not overcome -- defective eccentric gaze holding Viscous restraining forces to eye velocity If not overcome -- slow movements Therefore to compensate for these orbital forces we must develop a phasic-tonic, or velocity-position, or pulse-step change in innervation
7 Innervation to overcome mechanical orbital forces R = oculomotor neuron or nerve discharge rate (or ocular EMG activity) E = eye position
8 David A Robinson Single-unit activity in the oculomotor nucleus (inferior rectus motoneuron)
9 E =Eye Position R = Discharge Rate Pulse Slide Step
10 Premotor commands for saccades Pulse-step Pulse from burst signal (B) neurons Step from tonic signal (T) neuron (neural integrator)
11 Ocular motor integrators Steady gaze-holding requires a tonic level of innervation to hold the eye in eccentric positions of gaze against elastic restoring forces. Ocular motor integrators take velocity commands from the conjugate systems and mathematically integrate them to produce the necessary position commands, e.g. at the end of a saccade the eye is held steadily by the position command.
12 Ocular motor integrators Horizontal integrator -- medial vestibular nucleus (MVN) and nucleus prepositus hypoglossus (NPH). Vertical integrator -- MVN (SVN), NPH, and interstitial nucleus of Cajal (INC) (via medial longitudinal fasciculus (MLF)). Cerebellar flocculus is necessary for optimal performance of both integrators.
13 Gaze-holding networks in medulla MVN (medial vestibular nucleus) and NPH (nucleus prepositus hypoglossus)
14 Gaze-holding networks in the midbrain Interstitial Nucleus of Cajal INC
15 Cerebellar flocculus and paraflocculus (tonsils) Flocculus Paraflocculus
16 Downbeat, gaze-evoked and rebound nystagmus in cerebellar atrophy
17 Downbeat, gaze-evoked and rebound nystagmus in cerebellar atrophy Gaze-evoked nystagmus Rebound nystagmus Remember: As eccentric gaze is maintained: Gaze-evoked nystagmus (GEN) gets Less with cerebellar disease More with myasthenia gravis Stays about the same with congenital nystagmus
18 Central labyrinthine projections SCC rostral vestibular complex VESTIBULOCEREBELLUM OTOLITH caudal vestibular complex SCC / Otolith
19 Central projections from the labyrinth SCC projections are primarily to the rostral portions of the vestibular complex. Otolith projections are primarily to the caudal portions of the vestibular complex. SCC and otoliths also project directly to the cerebellum.
20 The cerebellum and vestibular disorders Flocculus/paraflocculus Nodulus VESTIBULOCEREBELLUM SCC / Otolith
21 Cerebellar flocculus and paraflocculus (tonsils) Flocculus Paraflocculus
22 Pursuit and VOR cancellation abnormalities in cerebellar atrophy
23 Anatomy of cerebellar atrophy
24 Anatomy of cerebellar atrophy Cerebellar atrophy: SCA6
25 Structural cerebellar syndromes Cranial-cervical junction: Chiari
26 Middle aged woman with a few months of rapidly progressive ataxia
27 Velocity-increasing slow phase Blink
28 A simple control systems model of control of vertical gaze-holding by the flocculus Inherently poor brain stem neural gazeholding network (MVN,NPH). Flocculus improves its function by a positive feedback loop ( k ). Too little feedback, poor gaze holding. Too much feedback, instability and runaway slow phases.
29 Abnormal VOR in cerebellar disease: Increased gain
30 Increased VOR GAIN in Cerebellar Disease 15 Horizontal position (deg) HEAD EYE-in-HEAD (inv) Backup Saccades Time (sec)
31 Abnormal VOR in cerebellar disease Abnormal direction
32 Abnormal VOR Direction X-couple into vertical
33 The VOR is a 3D reflex Almost all rotations stimulate (excite or inhibit) all the canals (e.g., vertical canals during yaw) There is no horizontal VOR
34 The 3D VOR (Robinson 1982) E H E = [ M ] [ B] [ C] C canal orientation matrix H - angular head velocity - angular eye velocity M eye muscle orientation matrix B brainstem matrix of connections between canal pairs and eye muscle pairs
35 The brainstem matrix is likely calibrated by the cerebellum Vestibulocerebellar lesions abolish cross-axis adaptation (Schultheis and Robinson, 1981) What is the effect of cerebellar disease on the 3D calibration of the VOR?
36 Abnormal VOR direction Horizontal eye movement exceeds head movement The eyes move up even though there is almost no vertical head movement (negative is up)
37 In the normal subject, there is no vertical eye movement
38 Functional consequence: Foveal stability is impaired in patients Larger gaze position errors at the end of the rotation (fovea taken off target) Larger gaze velocities during the rotation (more retinal slip)
39 Yaw impulses Summary Inappropriate upward eye velocity, greater in the abducting eye, leading to: Larger gaze errors Vertical retinal slip RVOR disconjugacy This is the response one might expect from excitation of the AC contralateral to the direction of rotation (e.g. left AC for rightward yaw)
40 AC excitation Rotation to the right excites the left anterior canal, leading to contraction of the left SR and right IO The SR has a greater vertical pulling direction; thus, the left (abducting) eye would go up more
41 Some old physiology
42 Some old physiology Implications: Upward and convergence bias revealed with floccular lesions
43 Rhesus Monkey Flocculus/Paraflocculus CN VIII Flocculus Paraflocculus Gundez Gucer
44 Downbeat, gaze-evoked, rebound nystagmus in monkey with removal of flocculus and paraflocculus
45 Impaired smooth pursuit in monkey with removal of flocculus and paraflocculus Pre Post
46 Flocculi
47 Paraflocculi (tonsils)
48 VOR learning and the cerebellum Different VOR gains or directions for the two eyes for different corrections for the two eyes (anisometropia) Magnification effects associated with habitual wearing of spectacles require a change in the amplitude or direction of the VOR for stabilization of images during head movements THREE different VOR gains are required (presbyopia (bifocal), hyperopia (far-sighted) and no-glasses OR contacts). Change in VOR direction may be required for astigmatism
49 Loss of VOR gain adaptation after floccular/parafloccular lesions Pre-lesion Increase 4 hrs of training with increasing or decreasing spectacles Pre-lesion Decrease Post-lesion No learning Lisberger, 1984
50 VOR learning in Purkinje Cells Vestib input (head) Visual input (image slip) Ito, NatureNS
51 Periodic Alternating Nystagmus (PAN)
52 Periodic Alternating Nystagmus (PAN) Null every two minutes
53 Anatomical Locus of PAN Nodulus
54 Rotation at a constant speed in darkness Pathophysiology of PAN: Normal vestibular responses gone awry Cupula decay Velocity Storage Mechanism Nystagmus outlasts the displacement of the cupula. Velocity storage perseverates peripheral canal signals and so improves the low-frequency response of the VOR. Increases VOR duration. POTENTIAL FOR INSTABILITY
55 Pathophysiology of PAN: Normal vestibular responses gone awry Onset head rotation Reversal Phase adaptation to sustained nystagmus. POTENTIAL FOR REVERSING NYSTAGMUS
56 PAN: Pathogenesis and Treatment In PAN, instability in central vestibular velocity storage is produced by loss of inhibition from the Purkinje cells of the nodulus onto the vestibular nuclei. Short-term adaptation causes reversals of nystagmus leading to sustained oscillation. How to treat?? Baclofen (GABA-b) provides the missing inhibition and stops the nystagmus.
57 Vestibuloocular abnormalities in cerebellar atrophy Sparing of basic rotational VOR, absent translational VOR
58 Quantification of t-vor: Head sled
59 Vestibular responses on the head sled Normal subject Cerebellar patient
60 The translational VOR and the cerebellar nodulus The role of the cerebellum in generating vestibular responses to linear acceleration (with static otolith-ocular reflexes such as counterroll in response to head tilt or with dynamic otolith-ocular reflexes such as the translational VOR) is unclear. Patients with diffuse cerebellar disease have striking deficits in the translational VOR (and pursuit) The cerebellar nodulus has been implicated in some aspects of the influence of gravity on the sustained (velocity-storage) component of the rotational VOR NO information is known about the specific role of the cerebellum in pure otolith-ocular reflexes (static or dynamic).
61 The paradigm Two monkeys Uvulo-nodulectomy Measured translational VOR
62 Translational VOR After the uvula-nodulus lesion there is a clear loss of the ability to generate a sustained response in the dark. The response in the light was less affected.
63 Fitting the eye velocity response to a combination of head acceleration and head velocity signals Major change is loss of the velocity coefficient
64 What is missing after the lesion? The raw records and the fits to the response suggest that an acceleration to velocity integration is impaired after the lesion. The uvula-nodulus appears to play a key role in integrating raw otolith acceleration signals to velocity signals to permit a sustained response to a translational stimulus. This is a third role of the cerebellum in neural integration for eye movements Velocity-position integrator for all conjugate eye movements. Control of the time constant (and spatial orientation) of the velocity storage integrator for the (low-frequency) rotational VOR. Integration of acceleration to velocity signals for the translational VOR.
65 Nodulus lesion
66 Wallenberg s Syndrome PICA distribution infarct involving the dorsolateral medulla Restiform body (ICP)
67 Wallenberg s Syndrome Skew
68 Otolith-ocular imbalance in the OTR
69 Ocular Tilt Reaction (OTR) Counterroll Skew (vertical ocular misalignment) Head Tilt Thomas Brandt, Lancet 1999
70
71 Evaluation of Skew Deviation Maddox Rod LE RE
72 Ocular Tilt Reaction (OTR) OTR (head tilt, skew deviation, ocular counterroll) is an extremely common finding -- when looked for -- with vestibular and especially central vestibular lesions. It represents an imbalance in otolith-ocular and otolith-collic reflexes, which normally are part of an ocular and head righting response to lateral body tilt. The counterroll acts to maintain the horizontal meridians of the retinas aligned with the horizon, and the skew is a reflection in pathology of a phylogenetically-old reflex that is easily appreciated in lateral-eyed animals, in which a lateral head tilt normally elicits a physiological skew deviation, again to maintain eye alignment along the horizon.
73 A few key references Zee, DS, and Walker, M, Cerebellum and oculomotor control, in Squire, LR (ed), Encyclopedia of Neuroscience, third edition, vol. 2, pp , Elsevier, Press, Leigh and Zee, Neurology of Eye Movements, Edition 4, Chapters 2 and 11, 2006
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