(Stroke. 1998;29:2377-2380.)
© 1998 American Heart Association, Inc.
Original Contributions |
Unilateral Saccadic Pursuit in Patients With Sensory Stroke
Sign of a Pontine Tegmentum Lesion
From the Department of Neurology, Urafune Hospital, Yokohama City University, Yokohama (K.J., A.K.); the Department of Neurology, Higashimatsudo Municipal Hospital, Matsudo (S.M.); and the Department of Neurology, Yokohama City University School of Medicine, Yokohama (O.H., Y.K.), Japan.
Correspondence to Ken Johkura, MD, Department of Neurology, Urafune Hospital, Yokohama City University, 3-46 Urafune-cho, Minami-ku, Yokohama 232, Japan. E-mail kjm0502{at}urahp.yokohama-cu.ac.jp
 |
Abstract |
|---|
 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Background and Purpose—Pure hemisensory syndrome can be caused by small strokes occurring in a number of regions, including the thalamus and pons. Differentiation of the pontine sensory syndrome from the thalamic sensory syndrome has generally been made on the basis of distribution of sensory loss and involvement of specific sensory modalities but not without uncertainties and difficulties. Because the pontine tegmentum plays a pivotal role in generating horizontal eye movement, we attempted to discriminate these 2 syndromes by analyzing horizontal eye movements in stroke patients with pure hemisensory syndrome.
Methods—Horizontal saccade, pursuit, vestibulo-ocular reflex (VOR), and VOR cancellation (VORC) were evaluated using electro-oculography in 6 patients with hemisensory syndromes, 3 due to pontine stroke and 3 due to thalamic stroke, and all were verified by MRI or CT. In addition, somatosensory evoked potentials (SEPs) were recorded.
Results—Smooth pursuit and VORC directed toward the side of the lesion were impaired unilaterally in patients with pontine sensory stroke, whereas those 2 movements were intact bilaterally in patients with thalamic sensory stroke. Saccade and VOR were preserved in all patients. SEPs were normal in all patients with pontine and thalamic sensory strokes. No difference was found in the pattern of sensory disturbance between the 2 types of stroke patients.
Conclusions—Ipsilateral impairment of the smooth pursuit system may be a sign of a pontine lesion in patients with hemisensory stroke.
Key Words: eye movements • pons • sensory stroke • thalamus
|
Introduction |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Pure sensory stroke is defined as the presence of mostly hemisensory symptoms without other major neurological signs.1 Although thalamic stroke was the first described and is the most frequent cause of this syndrome,1 2 3 nonthalamic strokes involving the brain stem, internal capsule, or cerebral cortex also have been reported to produce this syndrome.3 Small pontine tegmentum lesions have been reported to be a major cause of pure sensory stroke.4 5 6 Differentiation of the pontine sensory syndrome from the thalamic syndrome was made on the basis of the distribution of sensory loss and involvement of specific modalities of sensation, but was not without difficulties and uncertainties.
The dorsal pons contains most brain stem centers for the horizontal saccades and smooth pursuit eye movements. Premotor commands for the horizontal saccades are generated by burst neurons within the ipsilateral paramedian pontine reticular formation (PPRF).7 The burst neurons project directly to the ipsilateral abducens nucleus to contact abducens motoneurons and internuclear neurons that project up the contralateral medial longitudinal fasciculus to contact the medial rectus subgroup of the contralateral oculomotor nucleus.7 This pathway mediates the horizontal saccades. Smooth pursuit eye movements are thought to be relayed by a double decussation pathway in the brain stem.8 The dorsolateral pontine nucleus (DLPN) in the basal pons is considered to be the major gateway for ipsilateral smooth pursuit–related signals to the cerebellum. The DLPN receives afferences from ipsilateral cortical areas such as the middle temporal and medial superior temporal areas9 and projects mainly to the contralateral flocculus/paraflocculus (the first decussation).10 11 12 13 14 The contralateral medial vestibular nucleus receives afferent projections from the contralateral flocculus/paraflocculus and subsequently projects to the ipsilateral abducens nucleus (the second decussation).8 15 Although other parallel pathways such as projections from the DLPN to the bilateral vermis have been postulated to exist, smooth pursuit eye movements are considered to be controlled mainly by this DLPN-flocculus/paraflocculus-vestibular pathway in the brain stem.8 15 Characterization of the horizontal eye movements was therefore conducted in an attempt to differentiate a pontine sensory syndrome from a thalamic one.
|
Subjects and Methods |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
We examined 3 patients with pontine sensory stroke (2 infarcts and 1 hemorrhage) and 3 patients with thalamic sensory stroke (2 infarcts and 1 hemorrhage) between June 1995 and March 1998. All 6 patients were examined by one of us (K.J.) and then underwent CT scan, MRI, or both within 7 days after onset. Horizontal eye movements were recorded with an alternating current electro-oculography (time constant, 16 seconds) also within 7 days after onset. Saccades and smooth pursuit were elicited with a light-emitting diode (LED) ramp located 100 cm in front of the subject. Horizontal visually-guided saccades were studied by instructing the patient to look as quickly as possible at a suddenly appearing 20° lateral target. Horizontal smooth pursuit was induced by asking the patient to track an LED moving according to a triangular velocity profile (amplitude, 40°; velocity, 16°/s). The gain (defined as the ratio of eye velocity to target velocity) in smooth pursuit was calculated.7 13 We qualitatively evaluated vestibulo-ocular reflex (VOR) and VOR cancellation (VORC; the ability to suppress VOR by visual fixation), because smooth pursuit and VORC both are thought to share a common pathway.16 17 Horizontal VOR was studied on a sinusoidally rotating armchair, and VORC was tested by asking the patient to fixate on a target rotating with the armchair. In addition, somatosensory evoked potentials (SEPs) were recorded by unilateral electrical stimulation of the median nerve at the wrist.
|
Results |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
The MRI/CT scan findings and clinical features of all 6 patients are summarized in the Table
.
|
Neuroradiological Examinations
Results of the imaging studies are shown in the Table
and in
Figure 1. Three patients had small
lesions involving the unilateral dorsal pons, and the other 3 had small
lesions in the thalamus. The pontine lesions seemed to include the
medial lemniscus within the paramedian dorsal pons, at least partially,
and the thalamic lesions were located in the posterolateral part of the
thalamus, very likely including the ventral posterolateral nucleus. The
imaging findings in our patients were consistent with findings
reported previously in sensory stroke
patients.3 6
|
Sensory Patterns and Topography
Although all 6 patients had paresthesia as a main complaint,
examination revealed objective sensory abnormalities in only 1 patient
with pontine sensory stroke (patient 2) and in 2 patients with thalamic
sensory stroke (patients 5 and 6). The pontine stroke patient and 1
thalamic stroke patient (patient 5) showed mildly decreased medial
lemniscal sensation (tactile, vibration, and/or position). The other
thalamic stroke patient (patient 6) showed mildly decreased
spinothalamic sensation (pinprick and/or temperature)
and medial lemniscal sensation; lemniscal sensory deficit was dominant.
None of the patients had painful paresthesia like that observed in
so-called thalamic pain syndrome.
Two pontine stroke patients (patients 2 and 3) and 1 thalamic stroke patient (patient 6) had sensory symptoms limited to the perioral-hand area (cheiro-oral syndrome). The other 3 had hemisensory symptoms involving the arm, leg, trunk, and face. None of the patients had any bilateral sensory symptoms. Besides the hemisensory symptoms, patient 6 experienced transient dysarthria and right-hand clumsiness, which disappeared 3 days after onset. In all pontine and thalamic sensory stroke patients, SEPs were elicited with normal latencies on both sides.
Eye Movements
Eye movements were conjugate, and there was no spontaneous or
gaze-evoked nystagmus in any patient. Horizontal saccades and VOR were
normal in all pontine and thalamic stroke patients. Peak velocities of
horizontal saccades were within normal ranges in all patients (see the
Table).7 In pontine sensory stroke patients,
smooth pursuit eye movements directed toward the side of the lesion
(ipsilateral smooth pursuit) were impaired unilaterally and interrupted
by catch-up saccades (Figure 2). This was
obvious on direct observation without electro-oculographic monitoring.
In contrast, thalamic sensory stroke patients demonstrated almost
normal smooth pursuit bilaterally (Figure 2). These findings were
confirmed by the gain in horizontal smooth pursuit, which showed marked
right-left asymmetry only in the pontine sensory stroke patients
(Table). Ipsilateral VORC (the cancellation of VOR elicited by rotation
in the direction of the lesion) was similarly impaired in the pontine
sensory stroke patients, whereas VORC was preserved in the thalamic
sensory stroke patients (Figure 2).
|
|
Discussion |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
The differentiation between sensory stroke syndromes of pontine or thalamic origin has been based on the distribution of sensory loss and involvement of particular modalities of sensation. In pontine sensory stroke patients, the sensory loss involves mainly medial lemniscal sensation and is frequently distributed bilaterally in the facial area, whereas in thalamic sensory stroke patients it usually involves all sensory modalities and is unilaterally distributed on the face as well as the arm, leg, and trunk.3 6 However, there are reports of selective hemisensory loss of medial lemniscal sensation with a thalamic lesion18 and hemisensory deficits of all sensory modalities with a pontine lesion.6 In the present study, no difference was observed in the patterns of sensory disturbance between the 2 groups, underscoring the difficulty in clinical differentiation between pontine and thalamic sensory stroke based only on the pattern of sensory deficits.
SEPs are considered to depend on the integrity of the dorsal column–medial lemniscal sensory pathway.19 Because a majority of pontine sensory stroke patients show paramedian dorsal pontine lesions involving the medial lemniscus,5 6 SEPs are thought to have diagnostic value especially in patients with pontine sensory stroke.5 In our study, however, SEPs were normal in all pontine and thalamic stroke patients. Robinson et al20 also reported that SEPs are consistently normal in pure sensory stroke. Therefore, SEPs may not be a helpful diagnostic test in pure sensory stroke.20
The present study revealed that smooth pursuit directed toward the side of the lesion was impaired ipsilaterally in all 3 patients with pontine sensory stroke, while both saccades and VOR were spared. The simultaneous impairment of ipsilateral VORC was consistent with this selective impairment of smooth pursuit, because VORC and smooth pursuit are considered to share a common pathway.16 17 Pontine tegmentum lesions in our patients may not have involved the PPRF, abducens nucleus, vestibular efferents to abducens, or medial longitudinal fasciculus, accounting for the normal saccades and VOR.
Unilateral lesions of the pontine tegmentum have reportedly caused deficits of ipsilateral21 22 or contralateral8 23 smooth pursuit eye movements. Defective contralateral smooth pursuit with pontine tegmentum lesions may be associated with several possible mechanisms: (1) disruption of afferent projections to the flocculus/paraflocculus after their decussation; (2) ipsilateral central vestibular damage; and (3) disruption of the ipsilateral vestibular fibers to the abducens nucleus before their decussation.8 24 As for ipsilateral smooth pursuit impairment by the pontine tegmentum lesion as seen in our pontine sensory stroke patients, 4 mechanisms have been postulated: (1) involvement of corticopontine pathways9; (2) disruption of the pontocerebellar mossy fibers to the flocculus/paraflocculus before their decussation across the midline8; (3) impairment of inhibitory projections from the flocculus/paraflocculus to the vestibular nucleus25; and (4) damage to "pursuit neurons," which lie inferior to the abducens nucleus, outside the PPRF, and which are modulated in response to ipsilateral smooth pursuit eye movements.26
A rostral lesion in the pons can destroy the corticopontine pathways that mediate the smooth pursuit, but this is unlikely in our patients because, as verified by MRI/CT, our patients' lesions did not involve the corticopontine pathway that descends through the cerebral peduncle and passes through the ventrolateral pons to terminate pontine nuclei in the pontine base.9 Johnston et al8 suggested that not only contralateral but also ipsilateral pursuit deficits with pontine tegmentum lesions can be caused by damage to the pontocerebellar pathways. However, a recent study by Glickstein et al27 revealed that most pontocerebellar mossy fibers decussated in the pontine base and joined the contralateral middle cerebellar peduncle to enter the flocculus/paraflocculus, suggesting that a pontine tegmentum lesion is unlikely to affect the pontocerebellar fibers before their decussation. One patient who had a lesion adjacent to the fourth ventricle was reported to demonstrate low-velocity ipsilateral smooth pursuit,25 which may be related to a disruption of the inhibitory projections from the flocculus/paraflocculus en route to the vestibular nucleus as they course in the angular bundle of Löwy.28 Pontine lesions in our patients with sensory stroke seem to lie more medially than the angular bundle of Löwy. Unilateral pontine tegmentum damage that abolishes ipsilateral saccades can also paralyze ipsilateral smooth pursuit.21 22 This may be related to "pursuit neurons" located in the vicinity of the abducens nucleus.8 26 Although the existence of "pursuit neurons" is still controversial, damage to such neurons may have led to the defective ipsilateral pursuit in our pontine sensory stroke patients.
In conclusion, although the precise mechanism of the smooth pursuit deficits is unclear, ipsilateral impairment of the smooth pursuit system may be a sign highly suggestive of a pontine tegmentum lesion in patients with sensory stroke.
Received June 15, 1998; revision received August 3, 1998; accepted August 3, 1998.
|
References |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
1. Fisher CM. Pure sensory stroke involving face, arm, and leg. Neurology. 1965;15:76–80.
2.
Fisher CM. Thalamic pure sensory stroke: a pathologic
study. Neurology. 1978;28:1141–1144.
3.
Kim JS. Pure sensory stroke: clinical-radiological
correlates of 21 cases. Stroke. 1992;23:983–987.
4.
Hommel M, Besson G, Pollak P, Borgel F, Le Bas JF,
Perret J. Pure sensory stroke due to a pontine lacune.
Stroke. 1989;20:406–408.
5. Shintani S, Tsuruoka S, Shiigai T. Pure sensory stroke caused by a pontine infarct: clinical, radiological, and physiological features in four patients. Stroke. 1994;25:1512–1515.[Abstract]
6.
Kim JS, Bae YH. Pure or predominant sensory stroke due
to brain stem lesion. Stroke. 1997;28:1761–1764.
7. Leigh RJ, Zee DS. The Neurology of Eye Movements. 2nd ed. Philadelphia, Pa: FA Davis; 1991.
8. Johnston JL, Sharpe JA, Morrow MJ. Paresis of contralateral smooth pursuit and normal vestibular smooth eye movements after unilateral brainstem lesions. Ann Neurol. 1992;31:495–502.[Medline] [Order article via Infotrieve]
9. Tusa RJ, Ungerleider LG. Fiber pathway of cortical areas mediating smooth pursuit eye movements in monkeys. Ann Neurol. 1988;23:174–183.[Medline] [Order article via Infotrieve]
10.
May JG, Kellar EL, Suzuki DA. Smooth pursuit eye
movement deficits with chemical lesions in the dorsolateral pontine
nucleus of the monkey. J Neurophysiol. 1988;59:952–977.
11. Langer T, Fuchs AF, Scudder CA, Chubb MC. Afferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase. J Comp Neurol. 1985;235:1–25.[Medline] [Order article via Infotrieve]
12. Thier P, Bachor A, Faiss J, Dichgans J, Koenig E. Selective impairment of smooth-pursuit eye movements due to an ischemic lesion of the basal pons. Ann Neurol. 1991;29:443–448.[Medline] [Order article via Infotrieve]
13.
Gaymard B, Pierrot-Deseilligny C, Rivaud S, Velut S.
Smooth pursuit eye movement deficits after pontine nuclei lesions in
humans. J Neurol Neurosurg Psychiatry. 1993;56:799–807.
14. Johkura K, Komiyama A, Toda H, Hasegawa O, Kuroiwa Y. Predominantly ipsilateral smooth pursuit impairment associated with a lesion in the basal pons [in Japanese with English abstract]. Clin Neurol. 1994;34:351–355.
15. Keller EL, Heinen SJ. Generation of smooth pursuit eye movements: neuronal mechanisms and pathway. Neurosci Res. 1991;11:79–107.[Medline] [Order article via Infotrieve]
16.
Zee DS, Yamazaki A, Butler PH, Gucer G. Effects of
ablation of flocculus and paraflocculus on eye movements in primate.
J Neurophysiol. 1981;46:878–899.
17. Büttner U, Waespe W. Purkinje cell activity in the primate flocculus during optokinetic stimulation, smooth pursuit eye movements and VOR-suppression. Exp Brain Res. 1984;55:97–104.[Medline] [Order article via Infotrieve]
18.
Sacco RL, Bello JA, Traub R, Brust JCM. Selective
proprioceptive loss from a thalamic lacunar stroke. Stroke. 1987;18:1160–1163.
19. Halliday AM, Wakefield GS. Cerebral evoked potentials in patients with dissociated sensory loss. J Neurol Neurosurg Psychiatry. 1963;26:211–219.
20.
Robinson RK, Richey ET, Kase CS, Mohr JP. Somatosensory
evoked potentials in pure sensory stroke and related conditions.
Stroke. 1985;16:818–823.
21.
Goebel H, Komatsuzaki A, Bender MB, Cohen B. Lesions of
the pontine tegmentum and conjugate gaze paralysis. Arch
Neurol. 1971;24:431–440.
22. Daroff RB, Hoyt WF. Supranuclear disorders of ocular control systems in man: clinical, anatomical and physiological correlations. In: Bach-y-rita P, Collins CC, Hyde JE, eds. The Control of Eye Movements. New York, NY: Academic Press; 1975:175–235.
23. Pierrot-Deseilligny C, Rivaud S, Samson Y, Cambon H. Some instructive cases concerning the circuitry of ocular smooth pursuit in the brainstem. J Neuroophthalmol. 1989;9:31–42.
24. Furman JMR, Hurtt MR, Hirsch WL. Asymmetrical ocular pursuit with posterior fossa tumors. Ann Neurol. 1991;30:208–211.[Medline] [Order article via Infotrieve]
25. Waespe W, Martin P. Pursuit eye movements in a patient with a lesion involving the vestibular nuclear complex. J Neuroophthalmol. 1987;7:195–202.
26. Eckmiller R, Mackeben M. Pre-motor single unit activity in the monkey brain stem correlated with eye velocity during pursuit. Brain Res. 1980;184:210–214.[Medline] [Order article via Infotrieve]
27. Glickstein M, Gerrits N, Kralj-Hans I, Mercier B, Stein J, Voogd J. Visual pontocerebellar projections in the macaque. J Comp Neurol. 1994;349:51–72.[Medline] [Order article via Infotrieve]
28. Langer T, Fuchs AF, Chubb MC, Scudder CA, Lisberger SG. Floccular efferents in the rhesus macaque as revealed by autoradiography and horseradish peroxidase. J Comp Neurol. 1985;235:26–37.[Medline] [Order article via Infotrieve]
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||