Movement Disorders

Vol. 4, No. 4, 1989, pp. 291-302

0 1989 Movement Disorder Society

‘Eyelid.Movement Abnormalities in
Progressive Supranuclear Palsy
Lawrence I. Golbe, *Patricia H. Davis, and Frederick E. Lepore
Department of Neurology, University of Medicine and Dentistry of New Jersey-Robert
Wood Johnson Medical School, New Brunswick, New Jersey, and *Department of
Neurology, Louisiana State University Medical School, Shreveport, Louisiana, U.S.A.

Summary: We systematically videotaped eyelid movements in a community-

based series of 38 patients with progressive supranuclear palsy (PSP). Ten
patients (26%) had blepharospasm, “apraxia” of lid opening a n d o r “apraxia”
of lid closing. These patients as a group had more severe upgaze paresis but no
greater disease duration than the patients without supranuclear lid dysfunction.
Patients used a variety of synkinetic movements to overcome lid-movement
abnormalities. One patient displayed “slow blinks,” a phenomenon not pre-
viously described in PSP. Blink rate in PSP, 3.0/min, was markedly lower than
that in patients with Parkinson’s disease (PD), 12.5/min, and patients with PSP
but not PD increased their blink rate during command versional eye move-
ments. Key Words: Progressive supranuclear palsy-Eyelid movement-
Supranuclear lid dysfunction-Blepharospasm-Lid apraxia-Blink rate.

Dysfunction of vertical gaze is a cardinal feature of progressive supranuclear

palsy (PSP) (1,2). Closely allied with vertical gaze, both phenomenologically and
physiologically, are attention in the vertical plane (3) and eyelid function. The
latter has been briefly described in series of selected cases (4-7) usually as an
addendum to a discussion of eye movement abnormalities or in small anecdotal
reports. Blink frequency, similarly, has been studied only in a small, selected
series of patients with PSP (8,9).
Therefore, we systematically videotaped eyelid movement in a relatively large
community-based series of patients with PSP to assess the prevalence of supra-
nuclear lid dysfunction (SNLD) and to measure blink frequency. We also assessed
the effect of voluntary horizontal eye movement on blink frequency, because
anecdotal experience suggests that blinks may facilitate saccades as a synkinetic
phenomenon (10).

I Videotape segments accompany this article.

Presented in part at the 39th Meeting of the American Academy of Neurology, April 8, 1987, New
York City.
Address correspondence and reprint requests to Dr. L. I. Golbe at Department of Neurology,
CN-19, UMDNJ-Robert Wood Johnson Medical School, New Brunswick, NJ 08903, U.S.A.

297
298 L. I . GOLBE ET AL.

PATIENTS AND METHODS

As part of a separately reported epidemiological study (11,121 we attempted to

ascertain all cases of PSP residing in central New Jersey. We confirmed the
diagnosis in 41 living patients by personal examination using our defined diagnos-
tic criteria (2,ll). Three patients could not be videotaped-two because permis-
sion was denied, one because of recent cataract surgery.
Two of the authors (L.I.G. and P.H.D.) videotaped the remaining 38 patients.
We first videotaped gait, speech, and eye movements. We then positioned the
camera for the lid-movement protocol in (what would have been) the line of
primary gaze at a distance of 1-1.5 m.
We first asked the patients to fix gaze on the camera lens (to the extent possible)
for 1 min. We announced 15-s intervals. If gaze wandered from the camera, we
urged the patient to refixate. We then instructed the patient to perform alternate
horizontal ocular versions for 1 min at intervals of 5 s , which we called out. The
patient was vocally corrected if head movement occurred. Some patients required
repetition of the vocal instruction to change direction of gaze, because we were
often unsure of whether a hesitancy was due to poor comprehension or inattention
rather than to gaze paresis.
Finally, with subjects looking at a target away from the camera, we asked them
to forcibly close their eyes and immediately upon command open them, and
repeat the maneuver once.
We defined “apraxia” of lid opening by these criteria: (a) transient inability to
initiate lid opening, (b) no evidence of ongoing orbicularis oculi contraction, (c)
vigorous frontalis contraction during periods of inability to raise eyelids, and (d)
no oculomotor or ocular sympathetic nerve dysfunction and no ocular myopathy
(13). We defined “apraxia” of lid closure as the inability to close the lids on
command with preservation of normal reflex closure (14). These phenomena are
not true apraxias, which by definition occur despite an intact motor system. They
are more properly described as an abnormal inhibition of voluntary movement.
However, we chose to use the term “apraxia” here for its familiarity and brevity.
We defined blepharospasm as an involuntary, intermittent, and forceful con-
traction of the orbital, preseptal, and pretarsal portions of the orbicularis oculi.
Tapes were reviewed by two authors (L.I.G. and F.E.L.) using slow-motion
and single-frame stop action when necessary to determine whether an equivocal
lid movement constituted a blink. For present purposes a blink was defined as a
unilateral or bilateral lid movement of any speed that covered at least half the
pupil. When taping was limited to less than 1 min by poor cooperation, the per-
min blink rate was calculated using the segment of evaluable tape available.
We performed the same taping protocol for 10 patients with idiopathic Parkin-
son’s disease (PD) and 10 similar-age controls, usually spouses of patients with
PD. All the patients with PD, like those with PSP, were taking levodopa and/or
bromocriptine and had never had dopa-induced dyskinesias (which might have
produced blepharospasm or increased the blink rate).
The mean age of the 38 patients with PSP was 69.6 (SD 5.7, range 55-80), of the

Movement Disorders, Vol. 4, No. 4, 1989

 EYELIDS IN PSP 299

10 patients with PD, 65.9 (SD 13.3, range 54-76), and of the 10 normal controls
66.7 (SD 4.9,range 62-77).

RESULTS
Ten patients (26%) had one or more lid motility problems. Blepharospasm
occurred in six patients and produced visual disability in all. In four the blepha-
rospasm could be overcome only by the emotional relaxation that followed with-
drawal of the examiner. In three patients, presentation of a simple visual task
(finger counting) could overcome the blepharospasm when a direct command to
open the eyes, however gentle or forceful, could not. In two patients “apraxia”
of lid opening could be lessened by concomitant contraction of frontalis, neck
extension, andlor jaw opening with contraction of orbicularis oris. These phe-
nomena are illustrated by the five patients in the videotape (videotape segments
1-5).
“Apraxia” of lid opening (ALO) (lid levator inhibition) was present in seven
patients, of whom three also had blepharospasm. Three patients had “apraxia” of
lid closing (ALC), all of whom also had ALO. One patient had all three phenom-
ena-blepharospasm, ALO, and ALC.
One patient with ALO also had what we can only call “slow blinks.” His
eyeblinks exclusively consisted of a 0 5 s closing phase, a 4-sclosed phase, and a
0 5 s opening phase. They occurred one to two times per minute.
The mean disease duration (from onset of initial symptom) was 8.0 years (SD
2.4,range 4-12) for the 10 patients with SNLD and 6.5 years (SD2.8,range 1-16)
for the other 28 patients (difference NS). Patients with SNLD were more likely to
have moderate or severe upgaze paresis than were those without SNLD (p < .05,
Fisher’s exact test) (Table 1). There was no statistically significant relationship
between severity of downgaze paresis and presence or absence of SNLD.
Mean spontaneous blink rate for patients with PSP was 3.0lmin (Table 2). Blink
rate did not correlate with duration of symptoms of PSP (Pearson r = .09).During
the horizontal versional task in those 31 PSP patients able to perform it, blink rate
increased from 2.6 to a mean of 5.3 (p C .05, paired t test). In the controls with
PD, the blink rate in primary gaze averaged 12.5 and increased to 14.8 during the
gaze task (difference NS). In the normal controls, the blink rate in primary gaze
averaged 15.7 and decreased to 9.1 during the gaze task (difference NS).

TABLE 1. Severity of supranuclear voluntary gaze disturbances in progressive

supranuclear palsy patients with and without supranuclear lid dysfunction (SNLD)
Upgaze disturbance Downgaze disturbance
Absent or Moderate or Absent or Moderate or
mild severe mild severe
+ SNLD 0 10 1 9
- SNLD 9 19 5 23
Fisher’s exact test p< .os NS

Movement Disorders. Vol. 4, No. 4, 1989

300 L . I . GOLBE ET AL.

TABLE 2. Blink rates as mean blinkslminute (SD) in progressive supranuclear palsy

{PSP), Parkinson’s disease (PO), and age-matched normals
~ ~ ~~ ~ ~~

N Mean age Primary gaze During horizontal versions“

PSP 38 69.6 3.0 (4.8) 5.3 (6.7)***
PD 10 65.9 12.5 (12.5)* 14.8 (13.1)
Controls 10 66.7 15.7 (13.4)** 9.1 (7.9)****

a See text.
Using Student’s t test: *differed from PSP (p < 301); **differed from PSP (p < .MH)l); ***differed
(p < .05) from the group of PSP patients who were capable of voluntary horizontal versions, for whom
N = 31 and mean blink rate = 2.6 blinkshin; ****differed from primary gaze (p < .05).

DISCUSSION
Our results in a community-based series of patients with PSP suggest that
supranuclear disorders of lid motility are common in that disorder and occur in
combinations more often than not. We also found that blink rate in PSP is much
lower than in PD.
To our knowledge, PSP is the most common diagnosis in patients with
“apraxia” of lid movement. Other conditions in which ALO can occur include
Parkinson’s disease, parkinsonism secondary to methyl-phenyl-tetrahydro-
pyridine, Shy-Drager syndrome, Huntington’s disease, Wilson’s disease, olivo-
ntocerebellar atrophy, hypoxic encephalopathy (adult-onset or congenital),
hemispheric infarction, neuroacanthocytosis, cerebral diplegia, and bi-
frontotemporal trauma. ALC has been reported in Creutzfeldt-Jakob disease,
amyotrophic lateral sclerosis, and static encephalopathies. Blepharospasm occurs
commonly as an isolated idiopathic entity or as part of larger syndromes.
To our knowledge, neither “slow blinks” nor amelioration of ALO or blepha-
rospasm by visual tasks has been described in PSP. Combinations of SNLDs in
PSP have been reported only in summary form (15).
In the review by Brusa et al. (16) of all 310 cases clinically reported to 1979,
blepharospasm was noted in only 30 (9.7%). Lid “apraxias” are mentioned but no
specific statistic is given. Pfsenbach et al. (4), in a review of Mayo Clinic
records, reported blepharospasm in 8 of 4 4 patients (18%) with PSP and do not
mention “apraxias” of lid function. Dehaene (17) found ALO in three of eight
patients. Jackson et al. (5) mention blepharospasm but not other supranuclear lid
abnormalities in their review of 16 patients with PSP but subsequently (15) report
apraxia of lid opening and/or closing in five of 25 patients. The most recent update
of that series by Jankovic (18) found blepharospasm in 28% and “apraxia” of lid
opening in 30% of 87 referred patients. That series’ high prevalence of blepharo-
spasm in PSP may be explained by the activity of that institution as a blepharo-
spasm referral center.
The anatomic correlate of ALO, like that of vertical gaze paresis, has not been
localized more specifically than to the dorsal midbrain and ALC has not been
localized at all. ALO has been reported in a patient who received a thermal lesion
in the prerubral fields of Fore1 H and cephalic portion of the red nucleus for a
hyperkinetic movement disorder (19). Jankovic and Pate1 (20) reported six cases

Movement Disorders, Vol. 4, No. 4, 1989

 EYELIDS IN PSP 301

of blepharospasm (none with PSP) with clinical and/or computed tomography

evidence of rostra1 brainstem pathology. They could make no more specific and
cons.istent localization in that series of living patients.
We are aware of only three carefully autopsied cases of PSP in which SNLD
was present (21-23). Pathologic findings were widespread and typical for PSP and
provided no clue as to the specific locus of the lid dysfunction. A patient whose
only neurologic abnormality was blepharospasm was found by Gibb et al. (24) to
have a 5-mmangioma in the left pontine central tegmental tract. However, other
autopsied cases of isolated blepharospasm had no identifiable or consistent his-
tologic pathology (24).
The low blink rates in PD and PSP and the high blink rates in Huntington’s
disease and dystonia have been interpreted (8,9) as the result of proportionate
abnormalities in dopaminergic function. However, although we found a marked
difference between PD and PSP blink rates, Bokobza et al. (25) found no signif-
icant difference in striatal dopamine or homovanillic acid between PD and PSP.
This suggests that blink rate is determined by something other than, or in addition
to, nigrostriatal dopaminergic tone.
We found that patients with PSP increase their very low blink rate during
versional tasks in an apparent attempt to facilitate those tasks and can overcome
“apraxia” of lid opening by contracting other facial muscles. The use of synki-
netic movements to overcome a motor deficit is not unique to PSP, but has not
previously been described in patients with that disease.
We conclude that PSP includes a richness of clinical SNLD that has not been
widely appreciated. Additional carefully autopsied cases and neurochemical stud-
ies are needed, however, before an anatomical locus or chemical lesion account-
ing for SNLD can be identified.

LEGENDS TO VIDEOTAPE
All patients have progressive supranuclear palsy. Examiner’s commands are
audible.

SEGMENT 1. “Apraxia” of lid opening.

SEGMENT 2. “Apraxia” of lid opening ameliorated by visual task. “Apraxia”
of lid closing.
SEGMENT 3. Slow blinks, square-wave jerks. Blepharospasm, “apraxia” of
lid opening-both ameliorated by visual task.
SEGMENT 4. “Apraxia” of lid opening ameliorated by rapid retroflexion of
neck and by visual task.
SEGMENT 5. “Apraxia” of lid opening ameliorated by frontalis contraction
and jaw opening, but not by addition of visual task.

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Movement Disorders, Vol. 4 , No. 4. 1989