American Journal of Neuroradiology 27:1272-1274, June-July 2006
© 2006 American Society of Neuroradiology
Case Report
FUNCTIONAL
Prominent Activation of the Putamen during Essential Palatal Tremor: A Functional MR Imaging Case Study
S. Hallera,b,
D.T. Winklerb,
C. Gobbib,
P. Lyrerb,
S.G. Wetzela and
A.J. Steckb
a Division of Neuroradiology, Department of Diagnostic Radiology, University Hospital Basel, Basel, Switzerland
b Department of Neurology, University Hospital Basel, Basel, Switzerland
Address correspondence to Sven Haller, MD, Department of Diagnostic Radiology, Division of Neuroradiology, University Hospital Basel, CH-4031 Basel, Switzerland
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Abstract
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Summary: Palatal tremor (PT), also known as palatal myoclonus,
is defined by short rhythmic contractions of the palatal musculature.
Functional MR imaging (fMRI) revealed prominent bilateral neuronal
activation in the putamen associated with essential palatal
tremor (EPT) in a 41-year-old man. This implies a central role
of the putamen in EPT, most likely as a consequence of diminished
inhibition in an afferent pathway. Because fMRI primarily detects
activations, dysfunctional areas remain obscure. The present
functional study complements previous pathologic studies, which
associated PT with lesions to dentate nucleus, red nucleus,
and the inferior olive (Guillain-Mollaret triangle).
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Introduction
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Palatal tremor (PT), formerly also called
palatal myoclonus, is defined by short, mostly rhythmic contractions of the palatal
musculature and may occasionally be stimulus-sensitive. PT can
be associated with synchronous movements of adjacent structures,
including the pharynx, larynx, face, and diaphragm.
1,2 PT has
been subdivided into an essential form (EPT),
3 where no origin
can be found and MR imaging is usually normal,
4 and symptomatic
forms (SPT).
5 In SPT, stroke (46%) is the most common cause,
followed by trauma (11%) and demyelinating lesions (10%).
6,7 Early pathologic studies of PT
2,8 outlined an important role
of lesions affecting the dentatorubral-olivary pathway, or Guillain-Mollaret
triangle.
9 This circular pathway connects the red nucleus to
the inferior olivary nucleus and the contralateral dentate nucleus
of the cerebellum via central tegmental tract (red nucleus–inferior
olive), inferior cerebellar peduncle (inferior olive–dentate
nucleus), and superior cerebellar peduncle (dentate nucleus–red
nucleus).
9,10 Although it is an anatomic triangle, SPT is associated
with lesions in the rubodentate and rubo-olivary fibers, but
not in the olivodentate fibers.
10 Further, hypertrophic degeneration
of the inferior olive was reported in SPT.
7,11 Common radiologic
changes in SPT are an increase in T2 or proton attenuation MR
imaging signal intensity and hypertrophy within the olivary
nucleus.
10 There are generally no structural lesions in EPT,
and, consequently, the MR imaging is usually normal.
10
The pathomechanism generating the rhythmic contractions per se in PT remains unexplained. In the present study, we used functional MR imaging (fMRI) to identify neuronal activations associated with PT in a patient with stimulus-sensitive EPT.
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Case Report
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A 41-year-old man was admitted to our service because of progressive
contractions of the palatal and neck musculature. He reported
being in a minor motor vehicle crash without loss of consciousness
2 years prior to admission. A pulsatile tinnitus of the left
ear evolved several months later and progressed into a rhythmic
ear click. Approximately 2 months before admission, contractions
in the palatal musculature occurred. The further spread of the
contractions with involvement of the larynx lead to a first
neurologic consultation. Physical examination showed intermittent
bilateral short rhythmic contractions of the palatal and inframandibular
musculature, compatible with segmental myoclonus. The segmental
myocloni occurred in clusters of 5 rhythmic contractions, followed
by a variable silent period. The contractions could be triggered
by external sensory stimuli (eg, by touching his left arm).
Head movement to the left transiently suppressed the myoclonus.
The myoclonus was associated with ear clicks in the left ear
and bilateral tinnitus. Otoscopy revealed a high-frequency myoclonus
of the M. levator tympani that was not synchronous with breathing.
The remainder of the general, psychiatric, neurologic, and otorhinolarygologic
examinations—as well as MR imaging scans of the skull,
brain, and brain stem and EEG recordings—were normal.
Time-resolved MR projection angiography showed no signs of dural
AV fistula. The PT did not respond to any medication, including
diazepam and gabapentin in the further course of the disease,
which led to the diagnosis of an EPT. The patient took no medication
before admission and gave written informed consent before inclusion
into the study.
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Functional Imaging
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Blood oxygenation level–dependent (BOLD) fMRI was performed
to take advantage of the stimulus sensitivity of the EPT, by
using a whole-body 1.5T MR scanner (Sonata; Siemens, Erlangen,
Germany). PT occurred spontaneously or could be evoked by tactile
stimulation of the patient’s left arm by a physician inside
the scanning room. During the functional scanning, 22 clusters
of PT occurred, lasting on average 23.4 seconds (minimum, 5
seconds; maximum, 60 seconds). Functional T2*-weighted images
were obtained based on echo-planar single-shot pulse sequence
(EPI)—matrix size, 64
x 64; field of view (FOV), 220 mm
x 220 mm; 25 sections; 4-mm section thickness; 1-mm gap covering
the whole brain; flip angle, 90°; repetition time (TR),
2.5 seconds; echo time (TE), 40 milliseconds; 400 measurements
lasting 16 minutes 40 seconds. After functional scanning, a
high-resolution 1-mm isovoxel T1-weighted magnetization-prepared
rapid gradient echo (MPRAGE) (matrix 256
x 256, 176 sections)
was acquired. To confirm the findings of the first imaging session,
a second functional scanning was performed 3 days later. Appropriate
frequency and duration of PT occurred only during the first
half of the measurement. Therefore, only the first 200 scans
were analyzed, which included 19 clusters of PT lasting on average
9.9 seconds (minimum, 2.5 seconds; maximum, 30 seconds).
Anatomic and functional images were analyzed by using BrainVoyager QX (Brain Innovation, Maastricht, the Netherlands). Preprocessing included 3D motion correction, section-time correction, Gaussian spatial filtering (full width half maximum 4 mm), and high-pass temporal filtering of 3 cycles in time course (removal of low-frequency drifts). The functional images were coregistered to anatomic MPRAGE images. Normalization was not performed. The PT time courses were convolved with a hemodynamic reference function to create basis regressors. All reported activations are based on a fixed-effects general linear model (GLM) of the first run with statistical threshold of P < .01 (corrected Bonferroni; corresponding to t >5.3) and extent threshold of 500 mm3. The first run was re-evaluated with additional motion-correction predictors. No motion-related activation was found in the putamen. The results of the second run are not shown.
Peak activation associated with PT was identified in basal ganglia bilaterally and closely resembled the anatomic boundaries of the putamen. Additional activations were present in the precentral gyrus bilaterally and right superior temporal and angular gyrus (Fig 1). The activation in the putamen bilaterally could be reproduced in a second functional scan at day 3. The level of significance was, however, lower because of different alternation of myoclonus clusters and silent periods (not illustrated). No focal activation could be observed in prefrontal motor cortex, the brain stem, or the cerebellum.
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Fig 1. Neuronal activations associated with the initiation and maintenance of EPT in a 41-year-old patient. Peak activation assessed by fMRI is present in the putamen bilaterally (A). Additional activation is found in precentral gyrus bilaterally (B) and right superior temporal and angular gyrus (not shown). No focal activation could be observed in prefrontal motor cortex, the brain stem, or the cerebellum. The analysis is based on a fixed-effects GLM with statistical threshold of P < .01 (corrected Bonferroni) and spatial threshold of 500 mm3. Radiologic convention: right hemisphere is depicted on the left-hand side.
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Discussion
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fMRI was used to identify neuronal activations associated with
PT in a 41-year-old patient with stimulus-sensitive EPT. PT
was associated with peak neuronal activation in the putamen
bilaterally. No focal activation was detected in structures
of the Guillain-Mollaret triangle, which were previously associated
with PT.
2,8 Initially, the present investigation appears to
contradict these previous investigations; however, these previous
anatomic/pathologic studies identified damaged or dysfunctional
brain areas. We reason that a dysfunctional brain area per se
unlikely evokes overshooting muscular activations in PT. It
seems more plausible that a dysfunctional area modulates another
area—for example, as a consequence of diminished inhibition.
Because fMRI preferentially detects activations, the dysfunctional
structures remain obscure. On the basis of the previous anatomic/pathologic
studies, the damage might reside in the Guillain-Mollaret triangle.
Consistent with these considerations, an inhibitory effect of
the Guillain-Mollaret triangle on the basal ganglia has been
described in the literature.
12,13 The present fMRI study therefore
does not contradict, but complements, previous anatomic/pathologic
studies and implies that disinhibition of the putamen bilaterally
is an essential component of EPT. Of interest, activation of
the putamen was observed during eyelid spasms in patients with
benign essential blepharospasm,
14 which points to an as yet
not precisely understood involvement of the putamen in hyperkinesia.
Additional neuronal activations were present bilaterally in the precentral gyrus, which might be attributed to the motor control of the palatine muscles. In line with involuntary activity, no activity was registered in prefrontal areas. Further, activation was present in the right superior temporal and angular gyrus. This activation may reflect auditory stimulation, which occurs simultaneously with PT in the form of audible ear clicks.
Previous fMRI investigations of PT were limited to the brain stem, including the Guillain-Mollaret triangle, and did not cover the putamen in the investigated volume. Dysfunctional activation was found in the dentate nuclei, the left inferior olivary nucleus and the left red nucleus in a 56-year-old patient with PT.13 This investigation demonstrated dysfunction on the basis of MR images sensitized to changes in cerebral blood oxygenation state. In contrast, the present investigation primarily shows activations. In another functional study, voluntary PT was associated with hyperactivation of the inferior olive, a brain stem region, and the cerebellar dentate nuclei8 in a brother of a patient with EPT who was able to elicit, modulate, and stop rhythmic contractions of the soft palate associated with ear clicks voluntarily. This voluntary control of rhythmic contractions obviously differs from the patient in the present investigation with involuntary EPT.
One limitation of the present study is that it is only a single case description, so further investigations are necessary to confirm the presented findings. A prerequisite for fMRI is several repetitions of activation interleaved with rest periods within a few minutes, which is rarely encountered in PT. Putative motion-related pseudoactivations are unlikely, because of the reproducibility of activations with and without nonexplanatory motion regressors and after 3 days. Also, no significant motion regressor–associated activations were present in the putamen.
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Conclusion
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The present study revealed prominent bilateral activation of
the putamen associated with EPT. These results imply a central
role of the putamen in the generation of EPT. Further studies
will be needed to confirm a putative disinhibition of the putamen
in EPT.
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Footnotes
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S.G.W. was supported, in part, by a grant from the Swiss National
Science Foundation (grant 3200-066634/1).
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References
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Received April 15, 2005;
accepted after revision July 23, 2005.
TOP
Abstract
Introduction