Afternystagmus and Headshaking Nystagmus. David S. Zee
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1 442 `447, 1993 Afternystagmus and Headshaking Nystagmus David S. Zee Departments of Neurology, Ophthalmology and Otolaryngology The Johns Hopkins University School of Medicine Recent advances in vestibular physiology have led to a better appreciation of the pathophysiological significance and the clinical diagnostic implications of various types of "afternystagmus". Afternystagmus will be defined here as a nystagmus that appears after or outlasts any stimulus that leads to a real (e.g. actual body rotation) or perceived (e.g. the feeling of self motion associated with full field optokinetic stimulation) sense of body rotation. We will first briefly review types of afternystagmus that are shown by normal subjects, and then concentrate upon an analysis of two prototypical types of "pathological" afternystagmus that can appear in patients: headshaking induced nystagmus (HSN) and periodic alternating nystagmus (PAN). Key words: headshaking nystagmus, velocity storage, periodic alternating nystagmus, nodulus, Ewald's law, labyrinthectomy Afternystagmus in Normal Subjects Examples of afternystagmus in normal subjects include the reversal phase of caloric nystagmus, the reversal phase of rotational (or post-rotational) nystagmus, optokinetic afternystagmus (OKAN) and the reversal phase of optokinetic afternystagmus. Even though post-rotatory nystagmus occurs in the absence of head rotation it will not be considered an afternystagmus since it is due to direct peripheral stimulation leading to motion of the cupula and endolymph. Short-Term Adaptation Two major mechanisms are responsible for the appearance of afternystagmus in normal subjects. First is short-term adaptation (with a time constant of several minutes) that occurs, for example, in response to a prolonged constant velocity head rotation1)2). Short-term adaptation presumably has both peripheral (e.g. in the vestibular nerve) and central components3)4). It accounts, at least in part, for the reversal phases of caloric and of per and post-rotatory nystagmus. Since a reversal phase also occurs following OKAN, in which case there has been no peripheral vestibular stimulus, there must also be short-term adaptation in visual pathways and/or within more central structures. The latter would act to nullify sustained unidirectional nystagmus from any source. Put in another way, short-term adaptive mechanisms seem designed to help maintain the balance between the vestibular nuclei and so prevent any spontaneous drift of the eyes. In normal subjects, imposed stimuli such as constant-velocity rotations mimic an acquired vestibular lesion with a spontaneous nystagmus. Accordingly, an attempt is made to ( 442 )
2 nullify the "spontaneous" nystagmus. As the rotational nystagmus dies away, the action of the adaptive mechanism is revealed in the reversal phase of rotatory nystagmus. Velocity Storage The second major mechanism that underlies afternystagmus is "velocity storage" ". Velocity storage is a central mechanism that allows for perseveration of activity within the vestibular nuclei after the primary stimulus has been removed. It is the decay of activity in "velocity storage" that leads to an afternystagmus. Velocity storage makes use of visual, otolith, somatosensory and the semicircular inputs themselves to complement and to supplement the raw signals from the semicircular canals. Recall that the mechanical relationships between the cupula and the endolymph are such that for any sustained (low-frequency) stimulus, such as a constant velocity rotation, the cupula gradually returns to its neutral position in spite of continued rotation of the head. Thus, the response of vestibular afferents to head rotation slowly decays and head velocity is progressively underestimated. The velocity storage mechanism, by virtue of a partial, mathematical integration, acts to perseverate the fading peripheral canal signal. In this way, velocity storage provides a form of vestibular memory and acts to improve the ability of the brain to estimate head velocity when the frequency of head rotation is low. Described quantitatively, the time constant of the vestibulo-ocular reflex is prolonged to values roughly three times above that predicted from the mechanical properties of the cupula and endolymph. This action of velocity storage is made use of clinically when evaluating the results of rotational testing in patients with possible vestibular lesions. Velocity storage can be affected by both peripheral and central lesions so that the time constant of the vestibulo-ocular reflex may be increased (above 20 sec) with lesions of the cerebellar nodulus or decreased with unilateral (7-10 sec) or bilateral (below 7 sec) peripheral vestibular loss. The action of velocity storage can also be seen in the generation of optokinetic afternystagmus (OKAN), which follows prolonged full-field optokinetic stimulation. OKAN occurs naturally in the context of a sustained (low-frequency) rotation of the head (body) in the light. In this circumstance, as rotation of the body continues, the canal signal fades away and is supplanted by visual following (optokinetic nystagmus). When the body stops rotating, a post-rotatory nystagmus ensues that will be counteracted by the OKAN that is directed in the opposite direction. The importance of OKAN for nullifying post-rotatory nystagmus in primates and especially in human beings is not clear since other visual-following mechanisms, such as smooth pursuit and fixation mechanisms, can also nullify inappropriate nystagmus. Velocity storage may, however, have uses in vestibulospinal as well as in vestibulo-ocular responses, for example, helping to nullify inappropriate responses from the semicircular canals following prolonged circular locomotioe. Velocity storage appears to be elaborated within the vestibular nuclei themselves. Its action depends on connections between the vestibular complexes on either side of the brain stem since severing of the vestibular commissure markedly impairs or eliminates the velocity storage mechanism8). The cerebellar nodulus inhibits the velocity storage mechanism as nodulectomy leads to an increase in the vestibulo-ocular reflex time constant and occasionally to instability and oscillations (see Periodic Alternating Nystagmus, below)9). GABA-B receptors are important in velocity storage since administration of baclofen, a drug with GABA-B like activity, disengages the velocity storage mechanism10). While short-term adaptation and velocity storage are the main mechanisms underlying after- ( 443 )
3 nystagmus in normal subjects there may also be other mechanisms for afternystagmus in patients. It is possible that physical changes within the labyrinth may interfere with the normal flow of endolymph during and following head movements so as to lead to an afternystagmus. Headshaking Nystagmus Headshaking nystagmus (HSN) -an eye nystagmus occurring after a period of back and forth head oscillation -is a sensitive and not uncommon sign of both peripheral and central vestibular imbalance11)12). In patients with vague and nonspecific complaints of dizziness or imbalance, and in whom the rest of the neurological examination is unrevealing, the finding of HSN may be the only abnormality on examination that allows one to pinpoint the cause of the symptoms to the vestibular system. A characteristic pattern of HSN emerges following a unilateral peripheral vestibular loss13). After high-velocity horizontal headshaking, there is a nystagmus with slow phases directly toward the paretic ear which is followed by a reversal phase with slow phases directly toward the intact ear. After vertical headshaking, nystagmus with horizontal slow phases directed away from the paretic ear appears. Ewald's Second Law The explanation for HSN with a loss of function in one labyrinth relates to three phenomena. First, a single labyrinth responds differently to high-speed rotations of the head toward, than away from the labyrinth. With rotation toward the intact ear there is a relatively greater change in activity (increase above the resting rate) than with rotation toward the paretic ear (decrease below the resting rate). This is Ewald's second law (excitation is more effective than inhibition in changing labyrinthine activity), which can be attributed, at least in part, to the driving of vestibular afferents into inhibitory cutoff when the head rotates at high velocities in the direction opposite that labyrinth. Another cause for Ewald's second law may relate to an acceleration saturation such that at high accelerations, rotation toward a given labyrinth is more effective in changing labyrinthine activity than is rotation away from that labyrinth14). This phenomenon forms the basis of a useful clinical bedside test for detecting unilateral labyrinthine hypofunction15). With rapid head movements, the patient cannot maintain fixation on a straight-ahead target with the head rotating toward the paretic ear, and hence a catchup saccade is needed. It is the appearance of this catchup saccade that is the clue to labyrinthine hypofunction. Since asymmetries in activity due to Ewald's second law are more easily elicited when the head is rotated with the lateral canals in a plane perpendicular to the axis of rotation (so that the head acceleration vector is exclusively sensed by the lateral canal) then one might expect to elicit HSN more easily if the head is pitched slightly forward while being oscillated side to side. For an afternystagmus to appear after headshaking, the asymmetrical activity arising as a result of Ewald's second law must accumulate centrally during headshaking and must decay after headshaking to induce the nystagmus. The accumulation takes place centrally in the velocity storage mechanism in a similar way to the accumulation of activity in velocity storage during unidirectional rotation of the head under natural circumstances. Since the primary phase of HSN is due to velocity storage, any process that interferes with velocity storage per se can alter the pattern of HSN due to a unilateral peripheral lesion. Thus, with bilateral vestibular lesions or in the very early stages of an acute unilateral lesion, when velocity storage is very poor16), the primary phase of HSN may be brief or absent. Since the mechanisms underlying short-term adaptation to a sustained unidirectional nystagmus are also ( 444 )
4 operant during and after headshaking, the "secondary" reversal phase of HSN may appear first or follow just a few beats of "primary" HSN. It follows from these considerations that a proper interpretation of HSN (or its absence) requires an independent assessment of velocity storage, by measuring the time constant of the VOR and/or OKAN17)18). The explanation for the horizonal nystagmus appearing after vertical headshaking is not clear though it may relate to the fact that excitation of the vertical semicircular canals may also lead to horizontal slow phases directed toward the stimulated canal13). HSN and Meniere's Syndrome An exception to the typical pattern of HSN with peripheral lesions often occurs in patients with Meniere's syndrome in whom the slow phase of nystagmus may be directed initially toward. the intact ear. This "wrong way" HSN may be comparable to the "recovery" nystagmus (spontaneous nystagmus with slow phases toward the intact ear) which also occurs in Meniere's syndrome. The "wrong way" HSN might reflect a temporary imbalance in the dynamic sensitivity or "gain" of the vestibulo-ocular reflex such that the response to head rotation is better when rotating toward the involved ear. One prediction of this hypothesis is that "wrong way" HSN should be elicited at much lower velocities of head oscillation than when the lesion is related to a more static loss of function on one side. It is possible, however, that other factors, perhaps related to the changes in the vestibular labyrinth that occur with hydrops, also contribute to "wrong way" HSN in Meniere's syndrome. HSN and Central Lesion HSN may also appear with central lesions. Any asymmetry in central velocity storage can lead to HSN. In this case, however, the HSN need not depend on Ewald's second law and so might appear after relatively low velocities of head oscillations. To detect asymmetries in velocity storage, one must perform rotational and/or optokinetic testing to look for any asymmetry in the time constant of VOR and OKAN17)18). A common pattern of HSN in patients with central lesions is a vertical nystagmus (usually downbeat) after horizontal headshaking. While such a cross coupling of nystagmus usually indicates a central vestibular disturbance, an occasional normal subject may have a beat or two of vertical nystagmus after horizontal headshaking. Periodic Alternating Nystagmus Periodic alternating nystagmus (PAN), in which case a spontaneous nystagmus changes horizontal direction every few minutes, is a rare but dramatic form of pathological spontaneous nystagmus19). The origin of PAN likely relates to lesions of the cerebellar nodulus, which allow the velocity storage mechanism to become unstable. In this way, a vestibular nystagmus slowly increases in velocity until it reaches a saturation level. At this point, central short-term adaptation (which would normally act to nullify any sustained unidirectional nystagmus) causes the nystagmus to slow down and change direction after which it then slowly increases in velocity until it reaches saturation again. A precursor to PAN may be seen in patients who have several reversal phases of rotatory or optokinetic afternystagmue. The velocity storage mechanism of such patients is presumably on the verge of instability which, if it occurs, would lead to the sustained oscillations of PAN. PAN can be successfully treated with baclofen by virtue of disengaging the velocity storage mechanism10)21). Since monkeys with lesions of the cerebellar nodulus show PAN only in the dark, it follows that human patients with PAN in the light must also have lesions that interfere with the visual following and fixation mechanisms that normally suppress spontaneous nystagmus. Presumably, in these patients, coincident lesions in the cerebellar ( 445 )
5 Table 1 Mechanisms of Afternystagmus flocculus lead to the appearance of PAN both in the light and the dark. To summarize, both HSN and PAN are forms of afternystagmus with patterns that reflect the actions of normal physiological mechanisms: velocity storage and short-term adaptation (see Table 1). In the case of HSN, asymmetry in peripheral inputs, or in the central velocity storage mechanism that processes peripheral inputs, leads to an afternystagmus following headshaking. The reversal phase of HSN arises from short-term adaptation. In the case of PAN, velocity storage has become too good, leading to instability, and, coupled with short-term adaptation, gives rise to a sustained afternystagmus. References 1) Young LR, Oman CM : Model for vestibular adaptation to horizontal rotation. Aerospace Medicine 40 : , ) Malcolm R, Melvill Jones G : A quantitative study of vestibular adaptation in humans. Acta Otolaryngol (Stockh) 70 : , ) Goldberg JM, Fernandez C : Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I : Resting discharge and response to constant angular accelerations. J Neurophysiol 34 : , ) Furman JMR, Hain TC, Paige GD : Central adaptation models of the vestibuloocular and optokinetic systems. Biol Cybern 61 : , ) Cohen B, Matsuo V, Raphan T : Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic afternystagmus. J Physiol (Lond) 270 : , ) Raphan T, Matsuo V, Cohen B: Velocity storage in the vestibuloocular reflex arc (VOR). Exp Brain Res 35 : , ) Solomon D, Cohen B : Stabilization of gaze during circular locomotion in darkness. II. Contributions of velocity storage to compensatory eye and head nystagmus in the running monkey. J Neurophysiol 67 : , ) Katz E, DeJong JMBV, Buttner-Ennever JA, Cohen B : Effects of midline medullary lesions on velocity storage and the vestibulo-ocular reflex. Exp Brain Res 87 : , ) Waespe W, Cohen B, Raphan T : Dynamic modification of the vestibulo-ocular reflex by the nodulus and uvula. Science , ) Cohen B, Hetwig D, Raphan T: Baclofen and velocity storage : A model of the effects of the drug on the vestibulo-ocular reflex in the rhesus monkey. J Physiol (Lond) 393 : , 1987 ( 446 )
6 11) Kamei T, Kornhuber HH : Spontaneous and head-shaking nystagmus in normals and in patients with central lesions. Can J Otolaryngol 3 : , ) Takahashi S, Kamei T: The clinical significance of head-shaking nystagmus. In : Vertigo, Nausea, Tinnitus and Hearing Loss in Cardio-vascular Diseases, Claussen C-F and Kirtane MV, eds., Elsevier, pp , ) Hain TC, Fetter M, Zee DS : Head-shaking nystagmus in patients with unilateral peripheral vestibular lesions. Am J Otolaryngol 8 : 36-47, ) Halmagyi GM, Curthoys IS, Cremer PD, et al : Head impulses after unilateral vestibular deafferentation validate Ewald's second law. J Vestib Res 1: , ) Halmagyi GM, Curthoys IS : A clinical sign of canal paresis. Arch Neurol 45 : , ) Fetter M, Zee DS, Koenig E, Dichgans J: Head-shaking nystagmus during vestibular compensation in humans and rhesus monkeys. Acta Otolaryngol 110 : , ) Takahashi S, Fetter M, Koenig E, et al : The clinical significance of head-shaking nystagmus in the dizzy patient. Acta Otolaryngol (Stockh) 109 : 8-14, ) Fetter M, Takahashi S, Koenig E, et al : Head-shaking nystagmus - a clinical tool to detect peripheral and central vestibular asymmetries. In : Oculomotor Control and Cognitive Processes, Schmid R and Zambarbieri D eds., Elsevier, pp , ) Leigh RJ, Robinson DA, Zee DS : A hypothetical explanation for periodic alternating nystagmus : Instability in the optokinetic-vestibular system. Ann NY Acad Sci 374 : , ) Kornhuber HH : Nystagmus and related phenomena in man. An outline of otoneurology. In : Handbook of Sensory Physiogy, Kornhuber HH, ed., Vols 1 and 2, Vestibular System, Part 2, pp , Springer, New York ) Halmagyi GM, Rudge P, Gresty MA, et al : Treatment of periodic alternating nystagmus. Ann Neurol 8 : , 1980 Department Pathology of Neurology The Johns Hopkins Hospital Baltimore, Maryland 21287, USA ( 447 )
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