was seen if coma was due to structural damage within
the brainstem. Our data do not refute the observation that in cases of acute metabolic coma, the coma
itself may produce no short-term brainstem response
abnormality. However, our data suggest that a high
incidence of brainstem response abnormality may be
seen in chronic metabolic imbalance, such as uremia.

Acknowledgments
The authors wish to thank Elizabeth Smith for technical assistance, Richard Clement for preparing the statistical data, and
Margaret Geddes and N. Onur for secretarial assistance.
From the Clinical Neurophysiology Unit, University of Aston and Renal
IJnit, East Birmingham Hospital, Birmingham, UK.
Accepted for publication June 2:1,1984
Address correspondence and reprint requests to Dr. Komsuo’glu. T i p
Fakultesi. Cnmlik. Trabzon, Turkey.

References
1. Romano J , Engel GL. Delirium. 1. Electroencephalographic

data. Arch Neurol Psychiat 1944;51:356-77.
2; Kiley J , Hines 0. Electroencephalographic evaluation of
uremia. Arch Intern Mecl 1965;116:67-73.
8. Bourne JR, Ward JW, Teschan P E , Musso M, Johnston HB,
G i n n H E . Quantitative assessment of t h e electroencephalogram in renal disease. Electroencephalogr Clin Neurophysiol 1975;39:305-448.
4. Hughes J R , Roxe DM, d d Greco F, et al. Electrophysiological
studies of uremic patients: comparison of peritoneal dialysis
and hemodialysis. Clin Electroencephalogr 198O;ll:’iZ-82.

“Apraxia” of eyelid
opening: An
involuntary levator
inhibition

5. Lewis EG, Dustman RE, Beck EC. Visual and somatosensory
evoked potential characteristics of patients undergoing hemodialysis and kidney transplantation. Electroencephalogr Clin
Neurophysiol 1978;44:223-31.
6. Hamel 13, Bourne JR, Ward JW, Teschan PE. Visually evoked
cortical potentials in renal failure: transient potentials. Electroencephalogr Clin Neurophysiol 1978;44:606-16.
7. Picton T, Hillyard SA, Galambos R. The effects of attention
on the auditory evoked potential. In: Keidel WD, Neff WD,
eds. Handbook of sensory physiology, vol 3. New York:
Springer 1976:343-90.
8. Davis H. Sedation of young children for electri; response
audiometry (ERA): summary of a symposium. Audiology
1973;12:55-7.
9. Knoll 0, Harbort U, Schulte K, Zimpel F, Losse L. A’neurophysiological bedside technique for monitoring uremic brain
dysfunction. Proc Eur Dial Transplant Assoc 1980;17:714-8.
10. Amadeo M, Shagass C. Brief latency click evoked potentials
during waking and sleeping in man. Psychophysiology
1973;10:244-50.
11. Jewett D. Volume-conducted potentials in response to auditory slimuli as detected by averaging in the cat. Electroencephalogr Clin Neurophysiol 1970;28:609-18.
12. Bolton CF. Electrophysiological changes in uremic neuropathy after successful renal transplantation. Neurology (Minneap) 1976;26:152-61.
13. Ibrahim MM, Barnes AD, Crosland J M , et al. Effect of renal
transplantation on uremic neuropathy. Lancet 1974;2:739-42.
14. Olsen S. The brain in uremia. Acta Psychiat Neurol Scand
[Suppl] 1961;156:36.
15. Mendel MI, Goldstein R. Stability of the early components of
the averaged encephalographic response. J Speech Res
1969;12:351-61.
16. Kiang N Y-S, Crist AH, French MA, Edwards AG. Postauricular electrical response to acoustic stimuli in humans.
Quarterly Progress Report, MIT 1963;2:218-25.
17. Starr A, Achor JI,. Auditory brainstem responses in neurological disease. Arch Neurol 1975;32:761-8.

Article abstract-Apraxia of lid opening was described by Goldstein and
Cogan as “a non paralytic motor abnormality characterized by the patient’s
difficulty in initiating the act of lid elevation.”,’ We studied six such patients
with this finding accompanied by vigorous frontalis contraction and no
evidence of ongoing orbicularis oculi contraction, dysfunction of the
oculomotor nerve, or loss of ocular sympathetic innervation. Four patients
had Parkinson’s disease or atypical parkinsonism, one had progressive
supranuclear palsy, and one had Shy-Drager syndrome. At onset of ocular
symptoms, mean age was 64years, and the mean duration of extrapyramidal
symptoms was 9.7 years. By definition, the motor system must be intact in
any apraxia. Therefore, this disorder of lid opening in patients with extrapyramidal motor dysfunction is not an apraxia, but rather involuntary
levator palpebrae i n h i b i t i o n of supranuclear origin.

NEUROLOGY 1985;35:423-427

Frederick E. Lepore and Roger C. Duvoisin

Disruption of supranuclear control of the
levator palpebrae and orbicularis oculi can make it
impossible for a person to open the eyes. The most
common supranuclear disorder of eye opening is essential blepharospasm, seen alone or with contraction of other facial muscles in the Meige
syndrome.’ Bilateral “cerebral” ptosis, with no in-

volvement of sympathetic or oculomotor nerve pathways, can hamper eye opening after unilateral or
bilateral hemisphere infarction.’ Also, Cogan and
Goldstein,’drew attention to apraxia of lid opening:
“a non paralytic motor abnormality characterized by
the patient’s difficulty in initiating the act of lid
elevation.” They found only three reported cases to
March 1986 NEUROLOGY 35 423

above the superior orbital rim, the eyes would remain
closed until the upper lids slowly elevated. A t times, the
patient opened his mouth to facilitate eye opening (figure
1).

Comment. When unable to open his eyes despite vigorous frontalis contraction, the patient would open his
mouth. This strategy had been noted by Goldstein and
Cogan,,’ and it has been stated that “increased levator
tonus may normally accompany wide opening of the
mouth.”5
Patient 2. This 51-year-old man had progressive slowness
of bodily movement for 7 years with loss of finger dexterity,

Figure 1. Patient is unable to fully open his eyes despite
marked frontalis contraction. Note associated opening of
mouth.
supplement four of their own.
We have studied six patients with the following
combination: (1) transitory inability to initiate lid
opening; (2) n o evidence of ongoing orbicularis oculi
contraction, such as lowering of the brows beneath
the superior orbital margins (Charcot’s eyebrow sign
of blepharospasm)-‘; (3) vigorous frontalis c o n traction during periods of inability to raise eyelids;
a n d (4) no oculomotor or ocular sympathetic nerve
dysfunction and n o ocular myopathy.

Case reports. Patient 1. For 10 years, a 59-year-old man
had been treated for Parkinson’s disease. He had taken
carbidopa-levodopa with benefit for 6 years, followed by
recurrence of bradykinesia. For the last 2 years, he had
noted an increasingly frequent inability to open his eyes.
Examination revealed an alert and cooperative bedridden man with marked bradykinesia and resting tremor.
Confrontation fields were full. Ocular ductions were full,
and orthophoria was present. There were no abnormalities
of fixation, saccades, pursuit movements, suppression of
the vestibulo-ocular reflex, or optokinetic nystagmus.
There was no spontaneous nystagmus. Pupils were 3.5 mm
and reacted to light. Convergence was poor. After eye closure, he could not open his eyes for 20 to 30 seconds.
Despite marked frontalis contraction with eyebrows well

424 NEUROLOGY 35 March 1985

retropulsion, difficulty focusing his eyes, dysphagia, and
dysarthria.
Examination disclosed a slow, broad-based gait. Rapid
alternating movements were performed slowly, and intention tremor was present. Tendon jerks were active and
symmetric. His headwas flexed, and he spoke in a slow, soft
monotone. Horizontal versions of the eyes were full, but
there was limited vertical excursion that improved when
the vestibulo-ocular reflex or Bell’s phenomenon was elicited. Saccades were slow, pursuit movements were intact,
and fixation was normal. End-point nystagmus was present symmetrically, and there was faulty suppression of the
vestibulo-ocular reflex. Pupils were equal and reacted to
light. The fundi were normal. Spontaneous blinking was
decreased. After voluntary eye closure, his eyes remained
closed for seconds despite vigorous frontalis movements
and no apparent orbicularis oculi contraction.
C o m m e n t . T h e combination of progressive supranuclear palsy (PSP) and apraxia of eye opening in this
patient was also reported in three of eight patients with
PSP by Dehaene.6 Some of the sporadic eye-opening difficulty could be due to the constant loss of voluntary upward
gaze, preventing the increased levator tone normally associated with contraction of the superior rectus muscle.’

Patient 3. A 64-year-old man was seen after 25 years of
atypical parkinsonism and violent behavior. Although previously treated with haloperidol and thiothixene, his
bradykinesia and gait disorder persisted despite treatment
with carbidopa-levodopa exclusively.
He was dysarthric and had impassive facies. Bradykinesia and cogwheeling tone were present without resting
tremor. Gait was narrow based, but there was retropulsion.
Posture was erect. Intention tremor was present, and infrequent myoclonic movements of the arms were noted. Tendon jerks were diminished, and there were bilateral
Babinski responses. Ocular movements were full with normal saccades and jerky pursuit movements. There was no
spontaneous nystagmus, and fixation was normal. There
was abnormal suppression of the vestibuio-ocular reflex.
On voluntarily closing his eyes, the patient would sporadically be unable to open them despite vigorous frontalis
contractions (figure 2). Prolonged upward gaze would induce a slow descent of the globes and upper lids, followed by
a period of inability to open his eyes. Edrophonium did not
alter the duration or frequency of these episodes.
Comment. Although this patient with atypical parkinsonism was intermittently unable to open his eyes after
volitional eye closure, upward gaze was invariably followed
by transient immobility of the levator. As in patient 2, a
supranuclear vertical gaze disturbance was associated with
levator dysfunction.

Figure 2. Intermittent inability to raise eyelids is
induced in this patient after looking upward.

Figure 3. Prominent frontalis contraction will not open
eyes of this patient with transient bilateral levator
inhibition and blepharochalasis 0s.

Patient 4. This man, at age 60, noted onset of gait difficulties and slowing of movements. A year later, he became
impotent, and his blood pressure was low. Because of urinary incontinence, a suprapubic catheter was used. His gait
gradually deteriorated, and he began having syncopal episodes; orthostatic hypotension was documented. A t age 67,
he was confined to bed and chair. Medications included
carbidopa-levodopaand benztropine mesylate.
Examination disclosed severe rigidity, bradykinesia,
and low dysarthric speech. Reflexes were normal. There
was no tremor. Ocular movements were full with normal
saccades and no nystagmus. Pupils were 3.5 mm and sluggishly reactive. After eye closure, he could not voluntarily
open his eyes. CT showed dilation of the third and fourth
ventricles, enlargement of the prepontine and perimesencephalic cisterns, and prominent cerebellar folia and mild
cerebral cortical atrophy.
Comment. This patient had apraxia of eyelid opening
and Shy-Drager syndrome. Although atrophy on CT was
not exclusively restricted to the rostral brainstem, this
region was implicated in another supranuclear disorder of
eye opening, blepharospasm.’

dilation of the third ventricle, prominence of the perimesencephalic cisterns, and calcification of the basal ganglia.
Comment. A supranuclear disorder of both upward gaze
and eye opening was seen in this patient with atypical
parkinsonism and lateral medullary infarction. CT revealed rostral brainstem atrophy, less severe than in patient 4.

Patient 5. A 59-year-oldman became mildly ataxic after a
left lateral medullary infarct. He recovered with minimal
residual deficits, but 3 years later began to fall frequently.
At age 63,he had immobile facies, cogwheel rigidity, and
shuffling gait. He has had sporadic difficulty opening his
eyes after they have closed involuntarily in bright light. At
times, he could open his eyes only by prying the lids apart
with his fingers. No improvement of mobility or eye opening was noted with carbidopa-levodopa.
Examination revealed a severely impaired gait and
retropulsion. Succession movements were slowed, and
there was only minimal tremor of the hands. Tendon reflexes were normal. The optic disks were normal. Voluntary upward gaze was reduced, and upward excursion
increased with oculocephalic testing. Fixation, pursuit
m o v e m e n t s , a n d s a c c a d e s were n o r m a l . M i l d
blepharochalasis was present on the left. The patient was
intermittently unable to raise his eyelids despite contraction of the frontalis (figure 3). Convergence was poor,
and the glabellar reflex was persistent. There was abnormal
suppression of the vestibulo-ocular reflex. CT showed mild

Patient 6. For 5 years, this 80-year-old woman had impaired movement of the right arm. The movements became
slower, and she had difficulty cooking and dressing, despite
treatment with carbidopa-levodopa. For 2 years, she had
sporadic inability to open her eyes.
Examination revealed a fixed smile and soft dysarthric
speech. Her gait was broad based with short steps and
decreased arm swing. There was no tremor, but marked
rigidity of the neck was present. The tendon jerks were
symmetric, and plantar responses were flexor. A glabellar
sign was present. The optic fundi appeared normal. Ocular
movements were full with normal saccades, but pursuit
movements were jerky. Small-amplitude nystagmus was
seen at the extremes of lateral gaze, and fixation could not
be maintained for more than 10 seconds. Bell’s phenomenon was absent. The pupils were 4.5 mm OD and 5.0 mm
with an oval shape on the left. The pupils did not react to
light but did constrict after instillation of 1h% pilocarpine
hydrochloride. Sporadic contractions of the orbicularis
oculi were much greater on the right. When she attempted
to open her eyes, the right orbicularis oculi showed sustained contraction while the left eye remained closed, despite relaxation of the orbicularis and ongoing contraction
of the frontalis muscles (figure 4). CT was normal.
Comment. This patient with atypical parkinsonism
demonstrated a striking transition from bilateral blepharospasm to right-sided blepharospasm and apraxia of eyelid
opening on the left. Although this patient did not strictly
meet our criteria for apraxia of eyelid opening because
there was still blepharospasm, she demonstrated that these
two signs may coexist.

Discussion. These six patients with a distinctive
disorder of eyelid opening had extrapyramidal dise a s e that r e q u i r e d t r e a t m e n t w i t h carbidopaMarch 1986 NEUROLOGY 35 426

Figure 4. Top frame: bilateral involuntary orbicularis
contraction is succeeded by (bottom frame) persistent
orbicularis contraction OD and inability to open 0s
despite relaxation of orbicularis and frontalis
contraction on the left.

levodopa or anticholinergic medication. One patient
had Parkinson’s disease; three had atypical parkinsonism (probably representing multiple system atrophy); one had progressive supranuclear palsy, and
one had Shy-Drager syndrome. Goldstein and
Cogan’s four patients also had evidence of extrapyramidal disease.:3Although only one of their pat i e n t s h a d s u p r a n u c l e a r l i m i t a t i o n of eye
movements, three of our six patients had supranuclear vertical gaze palsies. A t the onset of
ocular symptoms, our patients’ mean age was 64
years, and the mean duration of extrapyramidal
symptoms was 9.7 years.
Although Goldstein and Cogan adhered to terminology of an older literature8to designate “apraxia”
of lid opening, “apraxia” may be an inaccurate term.
Heilman and Valenstein9stress that although “basal
ganglia disease may interfere with the performance
of skilled movements, the resulting abnormalities of
movement are not considered to be apraxia.” The
extrapyramidal diseases in our patients disqualify
their eye-opening disorders from consideration as an
apraxia because the motor system was not intact.
Additionally, none of our patients had evidence of
buccolingual or facial apraxia, and patients with facial apraxia do not typically manifest disorders of eye
opening.I0 Wray regarded this disorder as a n
“akinesia of lid function,”I0but since these patients
have a specific and transient inability to contract the
levator palpebrae, it would be more accurate to consider the disorder an involuntary levator palpebrae
inhibition of supranuclear origin.
How parkinsonism disrupts supranuclear control
of eye opening requires elucidation. Although par426 NEUROLOGY 35 March 1985

kinsonian patients have mild supranuclear disorders
of extraocular motility,” infrequently they may have
more marked ocular motor deficits.I2 Similarly,
many patients with Parkinson’s disease have subclinical dysfunction of levator inhibition, as demonstrated by the prolonged period of electrical
inactivity between the orbicularis twitch and the
levator contraction at the end of a voluntary blink.13
This dysfunction may be augmented for unknown
reasons until it becomes clinically apparent as involuntary levator inhibition. The association of Parkinson’s disease and disorders of eye opening gains
credence because apraxia of eyelid opening was seen
in three of four patients with parkinsonism induced
by l-methyl-4 phenyl-1,2,5,6-tetrahydropyridine
(MPTP)-a substance causing neuronal destruction
and Lewy body production in the human substantia
nigra.I4
Are there any common elements in involuntary
levator inhibition and the other supranuclear disorders of eye opening? Our patient 6 simultaneously
exhibited blepharospasm and apraxia of eyelid opening. Although this simultaneous occurrence is uncommon, the sequence of these two clinical signs was
described in essential blepharospasm by Boghen?
“There may be difficulty with lid opening even after
active contraction of the orbicularis muscle has
ceased.” Additionally, facial nerve section for blepharospasm may be followed by complete paralysis of
the orbicularis oculi, yet the eyelids remain closed.16
Although focal contraction of the pretarsal portion of
the orbicularis oculi might mimic levator dysfunction, it appears more likely that there is frequently a
component of involuntary levator inhibition in patients with essential blepharospasm. Although
blepharospasm and involuntary levator inhibition
are both marked by sporadic eyelid closure, the
former can be distinguished by eyebrows lowered
beneath superior orbital margins by contraction of
the pretarsal, preseptal, and orbital fibers of the orbicularis oculi, whereas the latter consists of eyebrows elevated by frontalis action and no contraction
of orbicularis. In contrast to the phasic episodes of
involuntary levator inhibition in our patients, or in
association with blepharospasm, continuous inhibition might account for persistent “cerebral ptosis”
with difficulty initiating lid elevation seen with cortical disease.I7
The neuroanatomic basis of apraxia of eyelid
opening remains to be clarified. Nashold and GillsI8
reported sporadic loss of volitional eye opening in a
patient with a stereotactically placed thermal lesion
of the prerubral fields of Fore1 H and red nucleus. It is
uncertain whether this eyelid disorder was due to the
lesion placed 3 months earlier or simply part of the
progression of the involuntary movement disorder.
Although rubral or prerubral involvement is not specifically demonstrable, two of our patients had rost r a l brainstem atrophy on C T . Since b o t h
corticobulbar and extrapyramidal systems control

tonus of the levator ~ a l p e b r a ewe
, ~ presume that the
extrapyramidal component was disrupted in our patients. Similarly, blepharospasm is often seen in parkinsonism (especially postencephalitic), a n d
extrapyramidal dysfunction may be a factor in this
possibly related supranuclear disorder of lid opening.
However, supranuclear control of eyelid opening can
be compromised by pyramidal motor-system disease,
as demonstrated in cases of cerebral ptosis with no
evidence of basal ganglia disease.*J7Further study is
needed to determine the circumstances in which a
levator subnucleus deprived of corticobulbar or extrapyramidal input causes the signs of involuntary
levator inhibition.

From the Department of Neurology. University of Medicine and Dentistry
of New Jersey, Rutgers Mediral School-Academic Health Science Center,
New Brunswick. Nd.
Accepted for publication June 21, 1984.
Address correspondence and reprint requests to Dr. Lepore, University of
Medicine and 1)entistry of New Jersey. Rutgers Medical Schtnd-Academic
Health Science Center, Department of Neurology, CN19, New Btunswick,
NJ 08903.

References
1. Meige H. Les convulsions de la face, une forme clinique de

convulsion faciale, bilaterale et mkdiane. Rev Neurol (Paris)
1910;10:437-43.
2. Caplan LR. Ptosis. J Neurol Neurosurg Psychiatry
1974;37:1-7.

Accidental
hypothermia
in a healthy
quadriplegic patient

-1

3. Goldstein J E , Cogan DG. Apraxia of lid-opening. Arch
Ophthalmol 1965;73:155-9.
4. Kestenbaum A. Clinical methods of neuro-ophthalmologic examination. New York Grune and Stratton, 1947.
5. Walsh FB, Hoyt WF. Clinical neuro-ophthalmology, 3rd ed.
Baltimore: William and Wilkins, 1969.
6. Dehaene I. Apraxia of eyelid-opening in progressive supranuclear palsy. Ann Neurol 1984;15:115-6.
7. Jankovic J , Havins WE, Wilkins RB. Blinking and blepharospasm: mechanisms, diagnosis and management. JAMA
1982;243:3160-4.
8. Riese W. Apraxie der lidoffnung (analyse einer bewegungsstorung). J Psycho1 Neurol Lpz 1930;40347-55.
9. Heilman KM, Valenstein E, eds. Clinical neuropsychology.
New York: Oxford University Press, 1979.
10. Case records of the Massachusetts General HospiGl: case
32-1975. N Engl J Med 1975;293:346-52.
11. White OB, Saint-Cyr JA, Tomlinson RD, Sharpe JA. Ocular
motor deficits in Parkinson's disease. 11. Control of the saccadic and smooth pursuit systems. Brain 1983;106571-88.
Marsden CD. Reversible supranuclear
12. Guiloff RJ,George W ,
ophthalmoplegia with parkinsonism. J Neurol Neurosurg Psychiatry 1980;43:552-4.
13. Loeffler JD, Slatt B, Hoyt WF. Motor abnormalities of the
eyelids i n P a r k i n s o n ' s disease. Arch O p h t h a l m o l
1966;76:178-85.
14. Langston JW, Ballard P, Tetrud JW, Irwin I. Chronic parkinsonism in humans due to a product of meperidine analog
synthesis. Science 1983;249:979-80.
15. Boghen D. Involuntary movements of the face. American
Academy of Neurology course, Toronto, April 1981.
16. Trobe JD. Blepharospasm. In: Ernest JT, ed. The year book of
ophthalmology 1982. Chicago: Year Book Medical Publishers,
1982.
17. Nutt JG. Lid abnormalities secondary to cerebral hemisphere
lesions. Ann Neurol 1977;1:149-51.
18. Nasbold BS, Gills JP. Ocular signs from brain stimulation and
lesions. Arch Ophthalmol 1967;77:609-18.

Article abstract-An otherwise healthy 28-year-old quadriplegicpatient
was admitted to the hospital with a core temperature of 76 O F secondary to
accidental hypothermia. Her neurologic disability was detrimental to thermoregulation by decreasing her ability to shiver actively and to vasoconstrict. The relationship between shivering and thermoregulation is
discussed.

NEUROLOGY 1985;35:427-428

Philip Altus, MD; Jack W. Hickman, MD; and H. Juergen Nord, MD

In accidental hypothermia, body core temperature falls below 94 O F (34.4 "C) after exposure to
environmental cold. Most are elderly victims, who
are susceptible and vulnerable to the fatal effects of
hypothermia because they cannot shiver actively. In
usually warm climates, poorly insulated housing and
unexpected cold weather may be hazardous. We recently cared for a young quadriplegic patient who
suffered from accidental hypothermia.
In April 1983, this 28-year-old woman suffered a
C-4 fracture in a motor vehicle accident and was left
quadriplegic. She remained at home in Florida at-

tended by her grandmother. On the day before admission, her home heater malfunctioned when
Tampa's low temperature was - 7.2 "C. On the day
of admission, a visiting health nurse found her confused, disoriented, hypotensive, and bradycardic. On
admission, her rectal temperature was 24.4 "C, pulse
was 30 beats per minute and regular, and blood pressure was 110/80 mm Hg. Examination showed clear
lung fields, quadriplegia, and decubitus ulcers on her
right calcaneus and left malleolus. She was disoriented but awake.
Laboratory values included a hemoglobin of 16.7
March 1986 NEUROLOGY 35 427

''Apraxia'' of eyelid opening: An involuntary levator inhibition
Frederick E. Lepore and Roger C. Duvoisin
Neurology 1985;35;423
DOI 10.1212/WNL.35.3.423
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