Acute Pseudobulbar or Suprabulbar Palsy G. Besson, MD; J. Bogousslavsky, MD; F. Regli, MD; P. Maeder, MD \s=b\ We studied 13 patients with supranuclear lower cranial nerve ("pseudobulbar" or "suprabulbar") palsy of acute onset. While seven patients had had a prior stroke, six patients had no history of stroke. Eight patients experienced a complete bilateral supranuclear lower cranial nerve palsy, which was isolated in five patients and associated with hemiplegia and with hemiparesis in three patients. Pseudobulbar palsy was partial in five patients. Only one patient had neuropsychologic impairment. The pseudobulbar features improved or recovered within a few weeks in all patients. The common characteristic of the lesions on computed to- mography or magnetic resonance imaging was the interruption of the corticonuclear pathways contrasting with marked sparing of the corticospinal pathways in both hemispheres. These lesions were either an opercular infarct, or a deep infarct in the corona radiata or internal capsule, or a lenticular hemorrhage. Hypertension was the most prevalent concomitant. Our findings suggest that acute pseudobulbar or suprabulbar palsy has rather stereotyped anatomic-vascular correlates and time course. (Arch Neurol. 1991;48:501-507) rpiie term pseudobulbar palsy was coined in 1877 by Lépine1 to differ¬ entiate lower cranial nerve palsy in¬ duced by supranuclear lesions from bulbar palsy related to bulbar nuclei lesions. Supranuclear lesions included corticobulbar and corticopontine path¬ way lesions. However, in 1837, Mag¬ nus2 reported the first case of pseudo¬ bulbar palsy due to multiple infarcts and a few other cases have also been reported.3,4 Several clinical and ana¬ tomic studies were performed at the beginning of the 20th century, and in his 1929 thesis ThureP summarized the current knowledge at that time. He di¬ vided pseudobulbar palsy into three forms. The cortical form (Foix-Chavany-Marie syndrome6) was charac¬ terized by a faciopharyngoglossomasticatory diplegia with automatic vol¬ untary dissociation. In the striatal form, the same features were associ¬ ated with pyramidal signs, emotional lability, and intellectual impairment. The pontine form was characterized by faciopharyngoglossomasticatory di¬ plegia associated with emotional labil¬ ity, pyramidal and sometimes cerebel¬ lar signs, and by a lack of dementia. The term pseudobulbar was descrip¬ tive. In 1940, Langworthy and Hesser7 coined the term supranuclear bulbar paralysis with reference to the supra¬ bulbar location of lesions. Because the facial nucleus and the trigeminal mo¬ tor nucleus are in the pons and pa¬ tients may present facial diplegia or masticatory palsy, the terms supranu¬ clear pontobulbar palsy or corticobul- bopontine palsy are more appropriate. Accepted for publication August 8, 1990. From the Departments of Neurology (Drs Besson, Bogousslavsky, and Regli) and Radiology (Dr Maeder), Centre Hospitalier Universitaire Vau- dois, Lausanne, Switzerland. Dr Besson is on leave from the Clinique Neurologique, Centre Hospitalier Universitaire, Grenoble, France. Reprint requests to the Department of Neurology, Centre Hospitalier Universitaire Vaudois, 1011 Lausanne, Switzerland (Dr Bogousslavsky). It may be easier to use the term su¬ prabulbar palsy, as suggested by Loeb et al.8 However, contrary to pseudo¬ bulbar all these terms fail to identify the bulb as the location of the symp¬ toms. Also due to historic reasons, the term pseudobulbar is more widely used than suprabulbar. In most patients, pseudobulbar Downloaded From: http://archneur.jamanetwork.com/ by a New York University User on 04/30/2015 palsy developed by fits and starts in relation to multiple recurrent strokes. We studied 13 patients in whom pseudobulbar palsy developed acutely. PATIENTS AND METHODS Patients were identified among 1800 stroke patients from the prospective Lau¬ sanne (Switzerland) Stroke Registry.' Seven patients had had a stroke prior to acute pseudobulbar palsy (group 1), while in six patients, acute pseudobulbar palsy de¬ veloped without prior stroke (group 2). Computed tomography (CT) or magnetic resonance imaging (MRI) were performed in all patients, as well as extracranial Dop¬ pler ultrasound, electrocardiogram, stan¬ dard blood tests, and neuropsychologic ex¬ amination with a standard battery of tests.10 Transcranial Doppler ultrasounds were performed in seven patients and cere¬ bral angiography (Seldinger technique) was performed in one patient. Bidimensional echocardiography was performed in three patients. Vascular concomitants, such as hypertension (blood pressure higher than 160/90 mm Hg at least twice before the stroke), diabetes mellitus (fast¬ ing serum glucose concentration higher than 5.6 mmol/L), hypercholesterolemia (cholesterol higher than 6.5 mmol/L), and history of cigarette smoking were analyzed following the guidelines of the Lausanne Stroke Registry.9 REPORT OF CASES Case 1.—A 79-year-old man with a his¬ tory of hypertension, atrial fibrillation, and aortic valve prosthesis experienced a left central facial paresis, which recovered over 1 month. A year later, he suddenly devel¬ oped dysphagia and dysarthria. On admis¬ sion, his blood pressure was 250/130 mm Hg. A left lower facial weakness was noted, while facial sensation was normal and cor¬ neal reflexes were symmetrical. We noted that his soft palate drooped bilaterally and the gag reflex was absent. Tongue move¬ ments were slowed with impaired protru¬ sion. Examination of the sternocleidomas- t.oid and trapezius muscles was normal. Jaw reflex was brisk. The patient was dysarthric and had a hypernasal voice. He chewed and swallowed with difficulty. No motor or sen¬ sory deficit was present in the limbs and trunk. Plantar responses were flexor. Re¬ sults of a neurologic examination, 2 weeks after the onset, were normal. Case 2.—A 71-year-old hypertensive and diabetic woman experienced right-sided weakness lasting for 30 minutes. A month later, she suddenly developed right-sided weakness and numbness that improved during the following day. The next morn¬ ing, she lost consciousness and fell down. On awakening, she had a left-sided sensorymotor hemiparesis. On admission, her blood pressure was 210/100 mm Hg. Left lower facial weakness was noted. Sensory examination of her face and mouth was normal and corneal reflexes were symmet¬ rical. The voice was low pitched, but there was no Table 1.—Radiologie Findings* Patient Right Hemisphere Left Hemisphere SDI in rostral part of posterior limb of IC SDI in rostral part of posterior limb of IC Opercular superficial MCA infarcì Multiple SDI SDI in medial part of CR SDI in anterior part of CR Lenticulocapsular hemorrhage SDI in rostral part of posterior limb of IC SDI in rostral part of posterior limb of IC Opercular superticial MCA infarct Multiple SDI SDI in medial part of CR SDI in medial part of CR Opercular superficial MCA infarct SDI in posterior part of CR SDI in rostral part of posterior limb of IC Opercular superficial MCA infarct Opercular superficial MCA infarct SDI in genu limb of internal capsule SDI in medial part of CR SDI in medial part of CR SDI in rostral part of posterior limb of IC SDI in medial part of CR SDI in medial part of internal capsule SDI in genu of internal capsule Opercular superficial MCA infarct Group 1 1 Group 2 10 13 * SDI indicates small, deep infarct; CR, corona radiata; IC, internal capsule; MCA, middle cerebral artery; and new lesion is italicized. dysarthria. Pharyngeal motility, gag reflex, and swallowing were normal. Tongue movements were slowed and lim¬ ited in range. Examination of the sterno¬ cleidomastoid and trapezius muscles was unremarkable. Jaw and palmomental re¬ flexes were brisk. Left-sided spastic hemi¬ paresis with brisk tendon reflexes and Ba¬ binski's sign was present. Sensation was decreased for touch, pinprick, position sense, graphesthesia, and pallesthesia on the left side. The patient was discharged after 2 weeks with only a persisting left hemiparesis. Case 3.—A 40-year-old woman suffered a stroke with left hemiplegia. One year later, she was hospitalized in another institution for clonic movements of the lips followed by a generalized tonicoclonic seizure. On ad¬ mission, 5 days after the seizure, her blood pressure was 130/80 mm Hg. Neurologic examination showed a severe facial diple¬ gia, the mouth was open and she dribbled. Jaw reflex was brisk. Facial and buccal sensation were normal. The soft palate was immobile and the gag reflex was absent. She was unable to chew, to swallow, to speak, or to protrude her tongue. The sternocleido¬ mastoid muscle was bilaterally weak. She had episodes of laughing and crying. The rest of the neurologic examination showed a left spastic hemiparesis with brisk tendon reflexes and Babinski's sign. She was dis¬ charged 6 weeks after the onset with only a mild improvement of the facial diplegia. Case 4.—A 70-year-old hypertensive woman was admitted for sudden headaches followed by dysphagia and dizziness. Eight years before, she had experienced a left hemiplegia with left-sided sensory impair¬ ment. The hemiplegia had completely re¬ covered, but she continued to complain of pins and needles sensation on the left side. On admission, her blood pressure was 190/ 120 mm Hg. Corneal reflex and facial pain and temperature sensation were decreased on the left side. Left lower facial weakness was present. Examination of the palate and tongue was normal, but she was unable to swallow and frequently coughed on her sa¬ liva. The gag reflex was present. The ster¬ nocleidomastoid and trapezius muscles were normal. The remainder of the neuro- logic examination showed mild weakness of the left arm and leg, brisk tendon reflexes, and left-sided Babinski's sign. The patient was discharged 4 weeks after the onset with a mild dysphagia. Case 5.—A 74-year-old man with a his¬ tory of hypertension, diabetes mellitus, and hypercholesterolemia was admitted for sudden dysarthria and dysphagia. Two years before, he had been seen in our department for a right ataxic hemiparesis. On cranial nerve examination at that time, he had rightward deviation of the tongue on protrusion. Computed tomography showed a small, deep infarct in the left capsulothalamic area. Six months later, he was read¬ mitted for a right motor hemiparesis. Com¬ puted tomography showed a second small infarct in the medial part of the left corona radiata. Clinical recovery was complete and the patient remained asymptomatic for 18 months. On the present admission, his blood pressure was 170/100 mm Hg. Left lower facial weakness was present, while sensory examination of face was normal. He had severe dysphagia and dysarthria. The soft palate was weak bilaterally. Ex¬ amination of the tongue, trapezius, and sternocleidomastoid muscles was normal. He had left mild hemiparesis without Ba¬ binski's sign. The patient recovered from the hemiparesis within 2 months, while the other signs persisted. Case 6.—A 76-year-old hypertensive dia¬ betic man with a history of shunted hydro¬ cephalus developed a right hemiparesis. Cranial nerve examination was normal, CT showed a left capsular infarct. He was left with mild hemiparesis until 4 years later when he was admitted for sudden dyspha¬ gia and dysarthria. On admission, his blood pressure was 160/100 mm Hg. Neurologic examination showed facial diplegia without facial sensory abnormality or corneal re¬ flex asymmetry. The jaw reflex was very brisk. The soft palate drooped bilaterally, more so on the left side, and the gag reflex was abolished. The patient was unable to chew and to swallow, and he had severe dysarthria. On protrusion, the tongue devi¬ ated to the left. The left hemiparesis was Downloaded From: http://archneur.jamanetwork.com/ by a New York University User on 04/30/2015 still present and plantar response was ex¬ bilaterally. The patient was dis¬ charged after 2 months with persisting fa¬ cial diplegia, bilateral soft-palate weak¬ ness, and dysarthria. tensor Case 7.—A 73-year-old hypertensive man with a history of myocardial infarction suffered a left middle cerebral artery in¬ farction with right sensory motor hemiple¬ gia and aphasia. Angiography showed a 50% stenosis of the left internal carotid ar¬ tery. Five years later, left internal carotid occlusion was discovered on a Doppler checkup. Nine years later, he was admitted for sudden mutism. On admission, his blood pressure was 170/90 mm Hg. Neurologic examination showed facial diplegia. Eye closure was weak, while the corneal reflex was asymmetric but present. The mastica¬ tory muscles were weak bilaterally. The patient's mouth remained open and he drib¬ bled. He was mute and could not swallow. The jaw reflex was brisk. The palate was immobile and drooped. The gag reflex was absent. Tongue protrusion was markedly weak without deviation. Bilateral weakness of the sternocleidomastoid and trapezius muscles was present. The remainder of the neurologic examination was normal, in¬ cluding plantar responses. Two months af¬ ter the onset, the patient could swallow and speak. His voice was dysarthric and all other signs persisted. Case 8.—A 77-year-old hypertensive woman was admitted for sudden left hemi¬ plegia. On admission, her blood pressure was 140/80 mm Hg. She had a vertical gaze paresis, while her horizontal gaze was nor¬ mal. There was a left lower facial paresis without abnormal facial sensation. The soft palate was immobile and the gag reflex was absent. There was a leftward deviation of the tongue on protrusion. The left trapezius and sternocleidomastoid muscles were weak. Swallowing was impaired and the voice was hoarse. Left hemiplegia and right hemiparesis were present. Tendon reflexes were brisk and plantar responses were ex¬ tensor bilaterally. The patient was dis¬ charged after 4 weeks. The left hemiplegia persisted unchanged, while the right hemi- Fig 1.—Group 1. Computed tomographic or magnetic resonance imaging findings (R indicates right; L, left; and arrows point to the lesions). Number 1 through 7 refer to patients 1 through 7 mentioned in Table 1. paresis and other signs improved. Case 9.—A 55-year-old man experienced mild head trauma without loss of conscious¬ ness, but he subsequently complained of dysphagia and dysarthria. On admission, 8 days later, his blood pressure was 240/130 mm Hg. A right lower facial paresis was noted. Sensory examination of the face and soft palate was normal. Tongue movements were slowed and decreased in amplitude. Swallowing was difficult, but pharyngeal motility and gag reflex were normal. The patient had dysarthria and his voice was hypernasal. The remainder of the neuro¬ logic examination was normal, including plantar responses. The patient improved over 2 weeks and was discharged with per¬ sisting dysarthria. Case 10.—A 71-year-old hypertensive woman experienced transient dysarthria. Two days later, she developed progressive left hemiparesis. One day later, she devel¬ oped sudden dysarthria and severe dyspha¬ gia. On admission, her blood pressure was Downloaded From: http://archneur.jamanetwork.com/ by a New York University User on 04/30/2015 140/90 mm Hg. Severe facial diplegia was present. The jaw reflex was brisk. Left facial hypesthesia for touch, pain, and tem¬ perature was present. The left corneal re¬ flex was absent. The soft palate drooped bi¬ laterally and the gag reflex was abolished. Tongue protrusion was slow and weak. The patient was dysarthric, with a low-pitched voice. She was unable to chew and to swal¬ low. Left hemiparesis with brisk tendon re¬ flexes and left-sided Babinski's sign was present. Pinprick and temperature sensa- Fig 2.—Group 2. Computed tomographic or magnetic resonance imaging findings (R indicates right; L, left; and arrows point to the lesions). Number 8 through 13 refer to patients 8 through 13 as mentioned in Table 1. Neurologie Findings* Table 2. — Patient/Sex/ Age, y History FP GR TP DP DR JR 1/M/68 2/F/71 3/F/40 Left facial paralysis Brisk Transient left hemiparesis Brisk 4/F/70 Left hemiparesis Normal 6/M/66 Right Right PMH Right hemiparesis Brisk 7/M/73 XI Left hemiparesis 8/F/78 9/M/55 10/F/70 11/F/63 12/M/74 13/M/81 Brisk Normal Brisk Brisk Brisk 'FP indicates facial paralysis; PP, palate paralysis; GR, gag reflex; TP, tongue paralysis; DR, dysarthria; DP, , ataxic hem paresis; PMH, pure motor hemiparesis; M, male; dysphagia; JR, jaw reflex; XI, Xlth nerve palsy; F, female; A, abolished; B, bilateral; P, present; L, left; N, none; R, right; plus sign, present; and minus sign, absent. tion were reduced on the left side. The dys¬ phagia completely recovered within 2 months, while mild hemiparesis and the other signs persisted. Case 11.—A 63-year-old hypertensive woman had a 46-year history of left partial motor seizures starting in the left arm and sometimes followed by generalized clonic movements. She was admitted for sudden dysphagia and dysarthria. On admission, her blood pressure was 140/90 mm Hg. There was a facial diplegia. Her mouth re- Downloaded From: http://archneur.jamanetwork.com/ by a New York University User on 04/30/2015 mained open and she dribbled. The mas¬ seter muscles were weak. The jaw reflex was brisk. The soft palate drooped and she had decreased sensation on the right side. The gag reflex was absent. Motility of the vocal cords was normal on laryngeal examina¬ tion. Tongue movements were severely lim¬ ited in range and in strength. The patient was unable to chew and to swallow and her voice was low pitched and hypernasal. The rest of the neurologic examination was normal except for a mild left pronator drift. Plantar responses were bilaterally flexor. The patient improved over 3 weeks and was discharged with only a moderate left palate and lower facial paresis. Case 12.—A 74-year-old hypertensive man with a history of myocardial infarction was admitted for sudden dysarthria and dysphagia. On admission, his blood pres¬ sure was 150/90 mm Hg. There was a bilat¬ eral lower facial paresis. The j aw reflex was brisk. Sensory examination of the face was unremarkable and the corneal reflex was normal. The soft palate was weak on the left side. The gag reflex was abolished. No tongue, trapezius, or sternocleidomastoid muscle weakness was present. Swallowing and chewing were impaired. His voice was dysarthric and low pitched. The rest of the neurologic examination was normal, in- Table 3.—Vascular Concomitants* Patient 1 Cardiac Hyper¬ Disease Prosthetic aortic tension Diabetes Elevated Doppler Doppler Smoking Cholesterol Extracranial Transcranial cranial Doppler ultrasound results showed no detection of the right ante¬ rior cerebral artery in one patient and was normal in six patients. Not done + COMMENT valve, AF No Normal Not done Normal Normal Not done No No Normal No detection Old myocardial infarction Left ICA Normal Normal right ACA 7 occlusion No 10 No 12 No Old myocardial infarction Normal Right ICA occlusion Normal Normal Normal Not done Normal Not done No Normal Not done *AF indicates atrial fibrillation; ACA, anterior cerebral artery; ICA, Internal carotid artery; plus sign, present; and minus sign, absent. eluding plantar responses. The patient im¬ proved over 2 weeks and was discharged with persisting mild dysarthria. Case 13.—An 81-year-old hypertensive man was admitted for sudden dysarthria. On admission, his blood pressure was 180/ 80 mm Hg. Bilateral facial paresis was present. He could not close his eyes volun¬ tarily, while corneal reflex was normal. The jaw reflex was brisk. No sensory deficit was noted over the face. The soft palate was paralyzed, and the gag reflex was abolished. The patient was unable to speak, to swal¬ low, to chew, or to move his tongue. The rest of the neurologic examination showed a right hemiplegia with right-sided Babin¬ ski's sign. The patient improved over 5 weeks and was left with mild paresis of the right hand and dysarthria. RESULTS CT and MRI Findings (Table 1) In group 1 (Fig 1), bilateral small, deep infarcts were found in four pa¬ tients, involving the rostral part of the posterior limb of the internal capsule in patients 1 and 2, and the corona ra¬ diata in patients 5 and 6. A bilateral superficial middle cerebral artery ter¬ ritory infarct involving the opercular region was found in patient 3. A su¬ perficial middle cerebral artery terri¬ tory infarct was associated with a con¬ capsulolenticular hemor¬ patient 7. In patient 4, multiple periventricular small, deep infarcts were found. The old previously asymptomatic lesion was a deep in¬ farct in five patients (patients 1, 2,4,5, and 6) and was a superficial middle ce¬ rebral artery territory infarct in two patients (patients 3 and 7). In group 2 (Fig 2), bilateral deep in¬ farcts were found in three patients, involving the corona radiata in patient tralateral rhage in 8, the rostral part of the posterior limb of the internal capsule in patient 9, and the genu of the internal capsule in pa¬ tient 12. A superficial middle cerebral artery infarct involving the opercular region was associated with a con¬ tralateral deep infarct in patients 10, 11, and 13. Clinical Features (Table 2) There were seven men and six ranging in age from 40 to 81 years old. Five patients experienced an isolated complete faciopharyngoglossomasticatory palsy (patients 1, 6, 7,11, and 12). Three patients experi¬ enced a faciopharyngoglossomasticatory palsy with hemiparesis (patients 3,10, and 13). In five patients (patients 2,4,5,8, and 9), the pseudobulbar palsy was only partial. One patient had in¬ voluntary laughing and crying (pa¬ tient 3). None had trismus. examination10 Neuropsychologic was normal except in patient 2. This patient was unable to realize Luria conflicting tasks and sequential rhythms. The results of Raven PM 38 were abnormal (14 points). Recogni¬ tion of face was impaired (15/27, Ben¬ ton). Visual learning was severely im¬ paired (23 of 40, learning of faces; 8 of 40, learning of countries). women The most common vascular concom¬ itant was hypertension (11 of 13) (Ta¬ ble 3). Symptomatic heart disease was present in three patients, diabetes mellitus in three patients, and hyper¬ cholesterolemia in four patients. Ex¬ tracranial Doppler ultrasound results showed internal carotid artery occlu¬ sion in two patients and was unre¬ markable in all other patients. Trans- Downloaded From: http://archneur.jamanetwork.com/ by a New York University User on 04/30/2015 Pseudobulbar or suprabulbar palsy developed acutely in all our patients. Although some patients have been presented,1117 the acute onset of pseudobulbar palsy is considered un¬ usual. This acute onset may be ex¬ plained by an acute damage to corticonuclear fibers on one side when con¬ tralateral corticonuclear fibers have been previously interrupted. This pre¬ vious lesion may have been symptom¬ atic (group 1) or asymptomatic (group 2). Actually, unilateral stroke limited to corticonuclear pathways may be asymptomatic if it is small and re¬ spects the corticospinal tract. When symptomatic, unilateral corticonu¬ clear pathway damage usually pro¬ duces only lower facial weakness. This may be explained by the classic notion that corticonuclear pathways project bilaterally toward cranial nerve nu¬ clei, except to the lower facial nucleus. Supranuclear innervation of the tongue may also be mainly unilateral. After his first stroke, patient 5 had a supranuclear palsy of the right Xllth cranial nerve associated with a small infarct in the medial part of the left corona radiata. Some other cases of deep lesions producing a supranuclear palsy of the Xllth cranial nerve have been described previously,1821 and 10% of small, deep infarcts of the carotid artery territory may have contralat¬ eral tongue paresis.21 More uncom¬ monly, patients with unilateral palatal palsy22 or unilateral vocal cord palsy23 have been described in association with a deep infarct involving cortico¬ nuclear pathways in the internal cap¬ sule or corona radiata. Trapezius or sternocleidomastoid muscle palsy has rarely been reported in pseudobulbar palsy.24 Three of our patients had Xlth cra¬ nial nerve palsy, which was bilateral in two (patients 3 and 7) and unilateral in one (patient 8). In both patients with bilateral Xlth cranial nerve palsy, one had superficial middle cerebral artery territory infarction on both sides and the other had a superficial middle ce¬ rebral artery territory infarct associ¬ ated with a contralateral capsulolenticular hemorrhage. In the patient with unilateral left supranuclear Xlth cranial nerve palsy, MRI showed a deep infarct in the posterior part of the right corona radiata near the lateral ventricule and a small, deep infarct in the medial part of the contralateral . corona radiata. The supranuclear in¬ nervation to the Xlth cranial nerve is controversial. Either a direct un¬ crossed innervation25 or a double decussation26 have been suggested. Pa¬ tients with hemiplegia due to hemi¬ spheric lesions had weakness of the sternocleidomastoid muscle ipsilat¬ eral to the lesion,27 which suggested that this muscle is controlled by the ipsilateral hemisphere. This is in con¬ tradiction with reports of presumed unilateral opercular syndrome with unilateral contralateral pseudobulbar palsy of the fifth, seventh, and ninth through Xllth cranial nerves.24·2831 However, none of these patients un¬ derwent autopsy, CT, or MRI studies. Rousseaux et al32 have described a pa¬ tient with unilateral facial, masseter, palatal, and pharyngeal palsy induced by a small infarct in the genu of the contralateral internal capsule. How¬ ever the authors did not find sterno¬ cleidomastoid or trapezius muscle weakness, suggesting that the supra¬ nuclear pathway of the Xlth cranial nerve was either spared or came from the ipsilateral hemisphere. Five patients experienced an iso¬ lated faciopharyngoglossomasticatory palsy that has been mainly reported in bilateral frontal operculum le¬ sions.6·3339 However, none of our pa¬ tients had a bilateral operculum lesion on CT or MRI. In three patients, a bilateral deep infarct was found (patients 1, 6, and 12). A superficial middle cerebral artery infarct was as¬ sociated with a contralateral deep in¬ farct in one patient (patient 11) and with a contralateral lenticulocapsular hemorrhage in another patient (patient 7). A sixth patient experi¬ enced a faciopharyngoglossomastica¬ tory palsy with unilateral mild hemi¬ paresis in relation to a superficial mid¬ dle cerebral artery infarct involving the operculum and contralateral deep infarct (patient 10). Bilateral facio¬ pharyngoglossomasticatory palsy has rarely been reported with nonopercular lesions. In 1884, Raymond and Artaud40 presented a 67-year-old man with faciopharyngoglossomasticatory palsy and mental impairment; a bilat¬ eral hemorrhage involved the lateral part of both lenticular nuclei and the anterior arm of both internal capsules. In 1898, Tournier41 described a patient with bilateral faciopharyngoglosso¬ masticatory palsy associated with trismus and left arm monoplegia; at au¬ topsy, he found a right opercular in¬ farct and two left deep infarcts involving the superomedial part of the thalamus and the lenticular nucleus. In 1979, Fisher42 presented a patient (case 5) with faciopharyngoglosso¬ masticatory palsy and mild right hemiparesis; at autopsy, he found bi¬ lateral deep infarcts situated in the genu of the internal capsules. In 1985, Leys et al14 described a patient with bilateral faciopharyngoglossomasti¬ catory palsy due to an infarct in the upper part of the genu of the internal capsule on both sides on CT. In 1988, Starkstein et al43 presented a patient with bilateral faciopharyngoglosso¬ masticatory palsy, aphemia, left hemi¬ paresis, and left hemineglect; at au¬ topsy, they found a unilateral infarct involving the right insula, while the left hemisphere, the brain stem, and the cerebellum appeared normal. These previous reports and our find¬ ings confirm that bilateral faciopha¬ ryngoglossomasticatory palsy may re¬ sult from bilateral frontal operculum involvement, but they also suggest that bilateral damage to corticonu¬ clear pathways sparing pyramidal pathways may not be uncommon. Six patients had a pseudobulbar palsy produced by bilateral deep in¬ farcts. However, only one had neu¬ ropsychologic impairment (patient 2) and none had forced laughing and cry¬ ing, which have been usually reported in chronic pseudobulbar palsy from striatocapsular involvement. On the other hand, involuntary laughing and crying was present in one patient who had bilateral cortical infarcts (patient 3). Involuntary laughing and crying is uncommon in the chronic form of pseudobulbar palsy due to cortical lesions.44 Involuntary laughing and crying is supposed to result from de¬ creased inhibition over centers con¬ trolling emotional facial movements.45 Centers and pathways involved in laughing and crying are yet unknown. Yarnell46 postulated that involuntary laughing and crying in right-handed patients corresponded to a lesion in¬ terrupting connections between the right middle cerebral artery territory and the left pons. Recently, a patient with isolated involuntary laughing and crying induced by a small brainstem vascular malformation was de¬ scribed.47 Lack of pseudobulbar sign suggested that corticonuclear tract le¬ sions are not necessary to produce these symptoms. The most prominent vascular con¬ comitant was hypertension in our pa¬ tients. Three patients (patients 1, 7, and 12) had a potential cardiac source of embolism. These three patients were also hypertensive, one had hyper¬ cholesterolemia (patient 1) and one was a smoker. Among these three pa¬ tients, two had bilateral small, deep Downloaded From: http://archneur.jamanetwork.com/ by a New York University User on 04/30/2015 infarcts (patients 1 and 12) and one had a superficial middle cerebral ar¬ tery territory infarct associated with a contralateral lenticulocapsular hem¬ orrhage. Extracranial vascular abnor¬ malities were found in two patients (patients 7 and 10) who were also hy¬ pertensive. Therefore, acute pseudo¬ bulbar palsy may identify a subgroup of patients in whom large-artery dis¬ ease and cardioembolism are an un¬ likely cause for stroke. Our findings suggest that acute pseudobulbar palsy, either with or without prior stroke, may be more common than what the recent litera¬ ture suggests. It may be associated with infarct or hemorrhage involving the frontal opercular region or the corticonuclear pathways in both cere¬ bral hemispheres, but largely sparing the corticospinal pathways. This study was supported by grants from the Conseil Regional de la Région Rhône-Alpes, France. We thank Jean Claude Gautier, MD; C. Miller Fisher, MD; and Louis R. Caplan, MD, for their helpful comments on the manuscript. References 1. L\l=e'\pineR. Note sur la paralysie glosso-labi\l=e'\e c\l=e'\r\l=e'\brale\l=a`\forme pseudo-bulbaire. Rev Mens Med Chir. 1877;1:909-922. 2. Magnus A. Fall von Aufhebung des Willenseinflusses auf einige Hirnnerven. M\l=u"\ller Arch. 1837:258-266. 3. Jolly F. Ueber multiple Hirnsklerose. Arch Psychiatr Nerv. 1872:711-730. 4. Joffroy A. Sur un cas de paralysie labio-glosso-laryng\l=e'\e\l=a`\forme apoplectique d'origine bulbaire. Gaz Med Paris. 1872:494-496. 5. Thurel R. Les Pseudobulbaires: Etude Clinique et Anatomopathologique. Paris, France: Jouve; 1929. Thesis. 6. Foix C, Chavany JA, Marie J. Dipl\l=e'\giefacio\x=req-\ linguo-masticatrice d'origine cortico sous-corticale. Rev Neurol. 1926;33:214-219. 7. Langworthy OR, Hesser FH. Syndrome of pseudobulbar palsy: an anatomic and physiologic analysis. Arch Intern Med. 1940;65:106-121. 8. Loeb C, Gandolfo C, Caponnetto C, Del Sette M. Pseudobulbar palsy: a clinical computed tomography study. Eur Neurol. 1990;30:42-46. 9. Bogousslavsky J, Van Melle G, Regli F. The Lausanne stroke registry: analysis of 1000 consecutive patients with first stroke. Stroke. 1988;19:1083-1092. 10. Assal G. Examen fonctionnel des zones c\l=e'\r\l=e'\bralesdu langage: de l'examen au syndrome anatomo-clinique. Med Hyg. 1980;38:3358-3370. 11. Buge A, Escourolle R, Hauw JJ, Rancurel G, Gray F, Tempier P. Syndrome pseudobulbaire aigu par infarctus bilat\l=e'\rallimit\l=e'\du territoire des art\l=e`\reschoro\l=i"\diennesant\l=e'\rieures.Rev Neurol. 1979;135:313-318. 12. Cambier J, Viader F, Paquelin F, Poullot B, Pariser P. Dyspn\l=e'\elaryng\l=e'\ep\l=e'\riodiqueau cours d'un syndrome bi-operculaire. Rev Neurol. 1983; 139:531-533. 13. Villa G, Caltagirone C. Speech suppression without aphasia after bilateral perisylvian softenings (bilateral rolandic operculum damage). Ital J Neurol Sci. 1984;5:77-83. 14. Leys D, Lejeune JP, Bourgeois P, Blond S, Petit H. Syndrome pseudo-bulbaire aigu: infarctus bilateral de la jonction capsule interne-corona radiata. Rev Neurol. 1985;141:814-818. 15. Helgason C, Wilbur A, Weiss A, Redmond KJ, Kingsbury NA. Acute pseudobulbar mutism due to discrete bilateral capsular infarction in the territory of the anterior choroidal artery. Brain. 1988;111:507-524. 16. Boulay G. Des pseudo-paralysies bulbaires. Gaz Med Paris. 1891:793-800. 17. Dej\l=e'\rineJ. La paralysie pseudo-bulbaire. Rev Gen Clin Ther. 1914;28:406-408. 18. Fisher CM, Curry HB. Pure hemiplegia of vascular origin. Arch Neurol. 1965;13:30-44. 19. Bogousslavsky J, Regli F. H\l=e'\mipar\l=e'\sieavec atteinte linguale: h\l=e'\matomedu genou de la capsule interne. Rev Neurol. 1984;140:587-590. 20. Bogousslavsky J, Regli F. Capsular genu syndrome. Neurology. 1990;10:1499-1502. 21. Ghika J, Bogousslavsky J, Regli F. Infarcts in the territory of the deep perforators from the carotid system. Neurology. 1989;39:507-512. 22. Iwata M. Unilateral palatal paralysis caused by lesion in the corticobulbar tract. Arch Neurol. 1984;41:782-784. 23. Garel J, Dor L. Du centre cortical moteur laryng\l=e'\et du trajet intra-c\l=e'\r\l=e'\braldes fibres qui en \l=e'\manent.Ann Mal Oreil Larynx. 1890;16:209\x=req-\ 235. 24. Schott B, Boulliat G, Cotte L, Vauterin C. Le syndrome operculaire bilat\l=e'\ralet unilat\l=e'\ral. Lyon Med. 1961;261:365-377. 25. Balagura S, Katz RG. Undecussated inner- vation to the sternomastoid muscle: a reinstatement. Ann Neurol. 1980;7:84-85. 26. Geschwind N. Nature of the decussated innervation of the sternomastoid muscle. Ann Neurol. 1981;10:495. 27. Mastaglia FL, Knezevic W, Thompson PD. Weakness of head turning in hemiplegia: a quantitative study. J Neurol Neurosurg Psychiatry. 1986;49:195-197. 28. Alajouanine T, Boudin G, Pertuiset B, P\l=e'\pinB. Le syndrome unilat\l=e'\ralde l'opercule rolandique avec atteinte controlat\l=e'\raledu territoire des V, VII, IX, X, XI, XIIe nerfs cr\l=a^\niens.Rev Neurol. 1959;101:168-171. 29. Pertuiset B, Perrier F. Le syndrome unilat\l=e'\ral(rolandique inf\l=e'\rieur)d'origine vasculaire. Rev Neurol. 1960;103:63-64. 30. Boudin G, P\l=e'\pinB, Wiart JP. Le syndrome operculaire unilat\l=e'\rald'origine vasculaire. Rev Neurol. 1960;103:65. 31. Rebucci GG, Gambetti P, Bottazzi G. Le syndrome unilat\l=e'\ralde l'opercule rolandique: \l=a`\ propos de trois observations cliniques. Acta Neurol Psychiatr Belg. 1964;64:1267-1278. 32. Rousseaux M, Lesoin F, Quint S. Unilateral pseudobulbar syndrome with limited capsulothalamic infarction. Eur Neurol. 1987;27:227-230. 33. Foix C, Chavany JA. Dipl\l=e'\giesfaciales (facio-linguo-pharyngo-masticatrices), d'origine corticale, avec quelques consid\l=e'\rationssur les paralysies pseudo-bulbaires et la localisation des centres corticaux de l'extr\l=e'\mit\l=e'\c\l=e'\phalique.Ann Med. 1926;20:480-498. 34. Alajouanine T, Thurel R. La dipl\l=e'\giefaciale c\l=e'\r\l=e'\brale,forme corticale de la paralysie pseudo\x=req-\ bulbaire (contribution \l=a`\l'\l=e'\tudede la dissociation des activit\l=e'\svolontaires et r\l=e'\flexes).Rev Neurol. 1933;40:441-458. 35. Schwob RA, Gruner J, Mamo H. Trois cas de trismus c\l=e'\r\l=e'\bralpar l\l=e'\sionscortico-sous-corticales. Rev Neurol. 1956;94:410-411. 36. Ch\l=a^\teauR, Fau R, Groslambert R, Perret J, Boucharlat J, Ch\l=a^\telainR. A propos de trois observations de dipl\l=e'\gielinguo-facio-masticatrice d'origine corticale: la forme de l'adulte et celle de l'enfant. Rev Neurol. 1966;114:390-395. 37. Ferrari G, Boninsegna C, Beltramello A. Foix-Chavany syndrome: CT study and clinical report of three patients. Neuroradiology. 1979; 18:41-42. Downloaded From: http://archneur.jamanetwork.com/ by a New York University User on 04/30/2015 38. Mariani C, Spinnler H, Sterzi R, Vallar G. Bilateral perisylvian softenings: bilateral anterior opercular syndrome (Foix-Chavany-Marie syndrome). J Neurol. 1980;223:269-284. 39. Mao CC, Coul BM, Golper LAC, Rau MT. Anterior operculum syndrome. Neurology. 1989; 39:1169-1172. 40. Raymond F, Artaud G. Contribution \l=a`\ l'\l=e'\tudedes localisations c\l=e'\r\l=e'\brales(trajet intra\x=req-\ c\l=e'\r\l=e'\bralde l'hypoglosse). Arch Neurol. 1884; 7:145-172. 41. Tournier C. Double h\l=e'\mipl\l=e'\gie:trismus persistant: syndrome de paralysie glosso-labio\x=req-\ faciale pseudo-bulbaire d'origine c\l=e'\r\l=e'\brale:ophtalmopl\l=e'\giene portant que sur les mouvements volontaires avec conservation des mouvements r\l=e'\flexes.Rev Med. 1898;18:671-679. 42. Fisher CM. Capsular infarcts: the underlying vascular lesions. Arch Neurol. 1979;36:65-73. 43. Starkstein SE, Berthier M, Leiguarda R. Bilateral opercular syndrome and crossed aphemia due to a right insular lesion: a clinicopathological study. Brain Lang. 1988;34:253-261. 44. Bruyn GW, Gathier JC. The operculum syndrome. In: Vinken PJ, Bruyn GW, eds. Handbook of Clinical Neurology. Amsterdam, the Netherlands: North-Holland; 1969;2:776-783. 45. Poeck K. Pathophysiology of emotional disorders associated with brain damage. In: Vinken PJ, Bruyn GW, eds. Handbook of Clinical Neurology. Amsterdam, the Netherlands: North-Hol- land; 1969;3:355-367. 46. Yarnell PR. Pathological crying localization. Ann Neurol. 1987;22:133-134. 47. Asfora WT, De Salles AAF, Abe M, Kjellberg RN. Is the syndrome of pathological laughing and crying a manifestation of pseudobulbar palsy? J Neurol Neurosurg Psychiatry. 1989; 52:523-525.