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The Eye Movement Disorders of Progressive Supranuclear Palsy
THE EYE MOVEMENT DISORDERS OF PROGRESSIVE SUPRANUCLEAR PALSY FRED C. CHU, MD
and DouGLAS
B.
REINGOLD, MA
BY INVITATION
DAVID
G.
COGAN, MD
and ADRIAN C. WILLIAMS, MB BY INVITATION
BETHESDA, MARYLAND
In addition to the gross disturbances of vertical gaze, patients with progressive supranuclear palsy may show abnormalities in the saccadic and pursuit subsystems of horizontal gaze. Saccades are slower and smaller than normal. An attempt to elicit a large amplitude saccade will often result in a series of "fractionated" saccades. Pursuit eye movements become saccadic. The quick phases of vestibular and optokinetic nystagmus are of low amplitude. In the study presented, eye movements of 13 patients were recorded clinically and by electro-oculography, and data from the two methods, compared.
THE syndrome which has been called progressive supranuclear palsy (PSP) was delineated in 1964 by Steele, Richardson, and Olzewski.l·2 Although having many of the characteristics of parkinsonism, including rigidity, akinesia, and
Submitted for publication Oct 22, 1978. From the National Eye Institute, National Institutes of Health (Drs Chu, Reingold, and Cogan), and the National Institute of Neurological and Com· municative Diseases and Stroke (Dr Williams), Bethesda, Md. Presented at the 1978 Annual Meeting of the American Academy of Ophthalmology, Kansas City, Mo, Oct 22·26. Reprint requests to National Eye Institute, Na· tiona! Institutes of Health, 9000 Rockville Pike, Bethesda, MD 20014 (Dr Chu).
extra pyramidal signs, PSP is distinct in the absence of both idiopathic tremors and "cogwheeling" of the extremities. 1• 3 Ophthalmologically, one of the hallmarks of PSP is downgaze palsy.l-4 For this reason, an ophthalmologist may be the initial physician to see such a patient, who might complain of difficulties in reading or eating, ie, dysfunctions related to downgazing. Over the years, however, disturbances in horizontal gaze also develop. 1 •4- 6 Since the vertical eye movements were compromised in all patients in this study, the observations were directed only to those made horizontally. The detailed clinical and electro-oculographic observations of such eye movements are presented.
METHODS Subjects ABNORMAL.-Nine patients with a group mean age of 57.2 years and the diagnosis of PSP were studied in the Eye Movement Laboratory at the National Eye Institute from 1976 to 1978. The patients had varying degrees of ophthalmoplegia,
VOLUME Hfi MARCH 1979
423
EYE MOVEMENT DISORDERS
vertical eye movements being especially affected. On neurologic examination, prominent features noted were both axial and nuchal rigidity when the head was cast backwards, pseudobulbar palsy, and, in seven of nine patients, mild to moderate dementia (Table 1).
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Saccadic and pursuit eye movements were tested by displaying a dimly lit target on a television monitor that allowed a peak-topeak angular displacement of 26°. The stimulus sequence was preprogrammed so that each patient received the identical stimulus. For the saccade task, the target trajectory was random in both interval and displacement. For the pursuit task, the target moved in both sine and triangular waveforms at five different velocities between 8°I sec and 74°I sec.
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NoRMAL.-Four subjects with a group mean age of 62 years were selected from the normal volunteer population at the National Institutes of Health for the purpose of recording their eye movements. At the time of study, the eye examinations were normal, and the patients had no apparent neurologic illnesses. Eye movements for either eye of each patient were recorded by directcurrent electro-oculograms (E0Gs). 7 Horizontal eye movements were detected placing silver-silver chloride electrodes at the medial and lateral canthi of each eye; the vertical eye movements, by those placed above and below the eyes. A reference electrode was positioned midline above the root of the nose. The head was immobilized as much as possible with a chin rest.
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Each patient's vestibulo-ocular reflexes were tested by rotating sinusoidally the chair he was seated on in the dark. Throughout this task, each patient was kept alert by requiring him to solve mental arithmetic problems frequently. To test the ability of a patient to suppress vestibular eye movements, the experiment was repeated, except that the patient now had a small, red fixation light that was positioned about 24 in from his eyes and that moved when he moved. For optokinetic testing, the patient sat within an illuminated drum that measured 4 ft in diameter, had vertical stripes subtending 7.5°, and was rotated at 80°/sec. Recording and Analysis Three channels of eye movement (generally, OD-horizontal, OD-vertical, and OS-horizontal) were recorded on magnetic tape for eventual analysis by computer and the multiparameter analysis package (MAP) system 7 (S.M.J. Hunt, MD, written communication, 1978). Simultaneously, in order that the experiments could be monitored, the data were displayed on a fourchannel polygraph. Saccades, or fast-phase eye movements, were measured by peak velocity, maximum response amplitude, accuracy, latency, and duration. Peak velocity was derived for 5° and 10° saccades by plotting the ratio of the best curve-fit of peak velocities to the corresponding response amplitudes (Fig 1, Top). Typically, about 100 saccades were analyzed per patient. Accuracy of saccadic eye movements was determined by plotting the ratio of all initial response amplitudes to the amplitude of the target jump
and then calculating the slope of the straight line fitting the data the best (Fig 1, Bottom). Pursuit eye movements were studied for the ability of the eyes to match target displacement. Accuracy of such tracking was calculated by dividing the peak-topeak eye displacement by the peakto-peak target displacement. The fast and slow phases of vestibular nystagmus and optokinetic nystagmus (OKN) were analyzed separately. Fast phases were studied for peak velocities and amplitude. The gain of the vestibular slow phase was calculated as the ratio of the magnitude of maximal ocular displacement, were the fast phases removed, to the magnitude of head rotation. The slow-phase velocities of OKN were averaged for the duration of the test, which lasted about 50 sec. RESULTS Saccades Table 2 shows that the typical saccades recorded for patients with PSP were of lower peak velocity and smaller maximum amplitude, and hence, more inaccurate than comparable eye movements in normal patients. In four patients, the saccadic eye movements evident clinically were, in fact, composed of a series of smaller, consecutive saccadic jumps (Fig 2). Thus "slow" saccades were of two types: those with lower peak velocities and those composed of smaller, but discrete, "fractionated" saccades. Clinically, the patients with PSP would appear to have difficulty mobilizing saccades when asked to look to either side. Yet, EOGs showed that the latency of saccades in the PSP patient group was not significantly different from that
EYE MOVEMENT DISORDERS
VOLUME 86 MARCH 1979
500
NORt1AL:
400
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Fig 1.-Top, Saccadic velocities determined from best curve ftt of peak velocities plotted vs corresponding response amplitudes. Bottom, Accuracy is ratio of response amplitude to the corresponding stimulus displacement.
426
CHU ET AL
,.r f SAC CADES:
(FAST EYE MOVEMENTS)
To 60° TARGETS
NORMAl
l -----'
.,
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Fig 2.-EOGs of saccades in normal patients (top) and in PSP patients (bottom). Note that those made by PSP patients were slower, smaller, and less accurate. A slow saccade seen clinically may have lower peak velocity or be composed of smaller, consecutive "fractionated" saccades.
measured in normal patients (Table 2). Similarly, there was no significant difference in saccadic durations for 5° and 10° eye movements made by either group of patients.
OPHTH AAO
head as it was rotated. The phenomenon was noted clinically ("Doll's head movements") as well as documented by EOGs (Fig 3). When the fast and slow phases of nystagmus were analyzed separately, it was apparent that for the patients with PSP, there were significant decreases in the amplitudes of the fast phases, while the slowphase gains were normaL When instructed to fixate a target moving with the rotation of the test chair, the normal patients suppressed virtually all eye movements, so the eyes tended to remain in -the center of the orbits. On the other hand, the patients with PSP were unable to suppress the drift of the eyes from the target. Consequently, the amplitudes of the fast phases were larger than those noted in the normal patients. EYE MOVEMENTS DUR!tlG HEAD ROTATI:JN IN DARKNESS
Pursuit Eye Movements Clinically, pursuit eye movements were not smooth in the abnormal, or PSP patient group, being replaced by "cogwheel" or "saccadic" pursuit movements. As indicated by EOGs, the ability of a patient with PSP to track a continuously moving target was significantly impaired (P<.OOl) as target velocity or frequency of target reversal increased (Table 3). Furthermore, if saccades were generated in an attempt to match higher target velocity, such eye movements were insufficient to bring the eye on target. Vestibular Nystagmus Vestibular nystagmus was characterized by movement of the eyes in the opposite direction from the
FIXATIONTARGET:PRESENT-
ABSENT,,,,,,,
Fig 3.-EOGs of vestibular nystagmus. During rotation in darkness, eyes deviate opposite to head rotation. If dim fixation target during rotation in otherwise darkness, deviation of eyes from center of the orbit is less.
Optokinetic Nystagmus With target displacement, the normal pattern of nystagmus was replaced by a drift of the eyes in those patients with PSP. Also, if OKN was present, the amplitudes of fast phases were significantly reduced in the patients (Fig 4).
TABLE 2 SACCADE ANALYSIS PATIENTS PARAMETER: Peak velocity* For 5° saccades For 10° saccades Maximum amplitudest Accuracy Latencyt Durationt For 5° saccades For 10° saccades
NORMAL
PSP
t TEST OF DIFFERENCE:
176.00 290.00 19.00 0.64 194.00
123.00 192.00 10.00 0.41 211.00
P<.01 P<.01 P<.01 P<.01
30.00 44.00
46.00 66.00
NS NS
NS
*Degrees per second. tDegrees. tMillisecond.
TABLE 3 PuRSUIT ANALYSIS (ACCURACY OF TRACKING) PATIENTS FREQUENCY (Hz):
0.1 0.3 0.5 0.7 0.9
NORMAL
PSP
0.96 0.90 0.89 0.83 0.83
0.90 0.78 0.58 0.45 0.32
Thirdly, slow-phase velocities in the patients were less than those found in normal patients. Fixation Clinically, fluttering movements of the eyes in two patients were prominent during fixation. Electrooculograms showed these movements to correlate to square waves (Fig 5). Although the other seven patients had steady fixation clinically, four had square waves on their electroencephalographic tracings, while three did not. All four normal patients had square waves on their tracings and steady fixation clinically.
t TEST OF DIFFERENCE: NS NS
P<.OOl P<.OOl P<.OOl
COMMENTS
The obvious defects in vertical and, especially, downgaze eye movements are among the cardinal features of progressive supranuclear palsy. As the disease progresses, gross defects in the horizontal eye movements also appear. These defects involve all major eye movement subsystems. Saccades are slower, smaller, and inaccurate. Moreover, clinically, these slow saccades include both fractionated saccades and saccades with reduced peak velocities. Surprisingly, the apparent difficulties patients with PSP seem to have in initiating saccades are not evident
CHU ET AL
428
OPHTH AAO
patients with the worst tracking also have the poorest saccades. STIMULUS:
Target Velocity: Rightwards -- 80° /sec.
NoRMAL
PSP
Fig 4.-EOGs of optokinetic nystagmus. Top Rightwards target (top). Middle, Normal response Bottom, PSP patient.
when saccadic latencies are studied with EOGs. The reason for this descrepancy is not known. Pursuit eye movements are also abnormal. Normal smooth eye movements are replaced by cogwheel tracking. When compared with normal patients of similar age, patients with PSP are less able to maintain their eyes on a target despite the insertion of saccades during the pursuit maneuver. The
Distinct abnormalities of vestibular nystagmus and OKN are obvious, too, in patients with PSP. In tests for both, a primary defect of fast phases is obvious: compared with the normal patients, fast-phase amplitudes are significantly reduced. Since, in· vestibular nystagmus, the slow-phase gain is normal, eye movement tends to drift in an opposite direction from head movement. Slow-phase velocities in OKN, however, are low because the eye tends to drift in the direction of target displacement without returning towards the center of the orbit. ACKNOWLEDGMENT The authors acknowledge the advice of Donald Calne, MD, and Steven Hunt, MD.
REFERENCES 1. Steele JC, Richardson JC, Olszewski J: Progressive supranuclear palsy. Arch Neurol 10:333-359, 1964.
2. Steele JC: Progressive supranuclear palsy. Brain 95:693-704, 1972. 3. David NJ, Mackey EA, Smith JL: Further observations in progressive supranuclear palsy. Neurology 18:349-356, 1968. 4. Pfaffenbach DD, Layton DD, Jr, Kearns TP: Ocular manifestations in progressive supranuclear palsy. Am J Ophthalmol 74: 1179-1184, 1972.
SQUARE WAVES:
5. NewmanN, Gay AJ, Stroud MH, et al: Defective rapid eye movements in progressive supranuclear palsy: An ocular electromyographic study. Brain 93:775-784, 1970.
lNTERSACCADIC PERIOD:
400
MSEC,
AMPLITUDE:
3-4
DEGREES
Fig 5.-EOGs of square waves in a patient in 'whom flutter-like eye movements were observed.
6. Troost BT, Daroff RB: The ocular motor defects in progressive supranuclear palsy. Ann Neurol 2:397-403, 1977. 7. Baloh RW, Konrad HR, Sills AW, et al: The saccade velocity test. Neurology 25: 1071-1076. 1975.
and DouGLAS
B.
REINGOLD, MA
BY INVITATION
DAVID
G.
COGAN, MD
and ADRIAN C. WILLIAMS, MB BY INVITATION
BETHESDA, MARYLAND
In addition to the gross disturbances of vertical gaze, patients with progressive supranuclear palsy may show abnormalities in the saccadic and pursuit subsystems of horizontal gaze. Saccades are slower and smaller than normal. An attempt to elicit a large amplitude saccade will often result in a series of "fractionated" saccades. Pursuit eye movements become saccadic. The quick phases of vestibular and optokinetic nystagmus are of low amplitude. In the study presented, eye movements of 13 patients were recorded clinically and by electro-oculography, and data from the two methods, compared.
THE syndrome which has been called progressive supranuclear palsy (PSP) was delineated in 1964 by Steele, Richardson, and Olzewski.l·2 Although having many of the characteristics of parkinsonism, including rigidity, akinesia, and
Submitted for publication Oct 22, 1978. From the National Eye Institute, National Institutes of Health (Drs Chu, Reingold, and Cogan), and the National Institute of Neurological and Com· municative Diseases and Stroke (Dr Williams), Bethesda, Md. Presented at the 1978 Annual Meeting of the American Academy of Ophthalmology, Kansas City, Mo, Oct 22·26. Reprint requests to National Eye Institute, Na· tiona! Institutes of Health, 9000 Rockville Pike, Bethesda, MD 20014 (Dr Chu).
extra pyramidal signs, PSP is distinct in the absence of both idiopathic tremors and "cogwheeling" of the extremities. 1• 3 Ophthalmologically, one of the hallmarks of PSP is downgaze palsy.l-4 For this reason, an ophthalmologist may be the initial physician to see such a patient, who might complain of difficulties in reading or eating, ie, dysfunctions related to downgazing. Over the years, however, disturbances in horizontal gaze also develop. 1 •4- 6 Since the vertical eye movements were compromised in all patients in this study, the observations were directed only to those made horizontally. The detailed clinical and electro-oculographic observations of such eye movements are presented.
METHODS Subjects ABNORMAL.-Nine patients with a group mean age of 57.2 years and the diagnosis of PSP were studied in the Eye Movement Laboratory at the National Eye Institute from 1976 to 1978. The patients had varying degrees of ophthalmoplegia,
VOLUME Hfi MARCH 1979
423
EYE MOVEMENT DISORDERS
vertical eye movements being especially affected. On neurologic examination, prominent features noted were both axial and nuchal rigidity when the head was cast backwards, pseudobulbar palsy, and, in seven of nine patients, mild to moderate dementia (Table 1).
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Electro-oculography
Saccadic and pursuit eye movements were tested by displaying a dimly lit target on a television monitor that allowed a peak-topeak angular displacement of 26°. The stimulus sequence was preprogrammed so that each patient received the identical stimulus. For the saccade task, the target trajectory was random in both interval and displacement. For the pursuit task, the target moved in both sine and triangular waveforms at five different velocities between 8°I sec and 74°I sec.
+ + +
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< :::!
NoRMAL.-Four subjects with a group mean age of 62 years were selected from the normal volunteer population at the National Institutes of Health for the purpose of recording their eye movements. At the time of study, the eye examinations were normal, and the patients had no apparent neurologic illnesses. Eye movements for either eye of each patient were recorded by directcurrent electro-oculograms (E0Gs). 7 Horizontal eye movements were detected placing silver-silver chloride electrodes at the medial and lateral canthi of each eye; the vertical eye movements, by those placed above and below the eyes. A reference electrode was positioned midline above the root of the nose. The head was immobilized as much as possible with a chin rest.
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Each patient's vestibulo-ocular reflexes were tested by rotating sinusoidally the chair he was seated on in the dark. Throughout this task, each patient was kept alert by requiring him to solve mental arithmetic problems frequently. To test the ability of a patient to suppress vestibular eye movements, the experiment was repeated, except that the patient now had a small, red fixation light that was positioned about 24 in from his eyes and that moved when he moved. For optokinetic testing, the patient sat within an illuminated drum that measured 4 ft in diameter, had vertical stripes subtending 7.5°, and was rotated at 80°/sec. Recording and Analysis Three channels of eye movement (generally, OD-horizontal, OD-vertical, and OS-horizontal) were recorded on magnetic tape for eventual analysis by computer and the multiparameter analysis package (MAP) system 7 (S.M.J. Hunt, MD, written communication, 1978). Simultaneously, in order that the experiments could be monitored, the data were displayed on a fourchannel polygraph. Saccades, or fast-phase eye movements, were measured by peak velocity, maximum response amplitude, accuracy, latency, and duration. Peak velocity was derived for 5° and 10° saccades by plotting the ratio of the best curve-fit of peak velocities to the corresponding response amplitudes (Fig 1, Top). Typically, about 100 saccades were analyzed per patient. Accuracy of saccadic eye movements was determined by plotting the ratio of all initial response amplitudes to the amplitude of the target jump
and then calculating the slope of the straight line fitting the data the best (Fig 1, Bottom). Pursuit eye movements were studied for the ability of the eyes to match target displacement. Accuracy of such tracking was calculated by dividing the peak-topeak eye displacement by the peakto-peak target displacement. The fast and slow phases of vestibular nystagmus and optokinetic nystagmus (OKN) were analyzed separately. Fast phases were studied for peak velocities and amplitude. The gain of the vestibular slow phase was calculated as the ratio of the magnitude of maximal ocular displacement, were the fast phases removed, to the magnitude of head rotation. The slow-phase velocities of OKN were averaged for the duration of the test, which lasted about 50 sec. RESULTS Saccades Table 2 shows that the typical saccades recorded for patients with PSP were of lower peak velocity and smaller maximum amplitude, and hence, more inaccurate than comparable eye movements in normal patients. In four patients, the saccadic eye movements evident clinically were, in fact, composed of a series of smaller, consecutive saccadic jumps (Fig 2). Thus "slow" saccades were of two types: those with lower peak velocities and those composed of smaller, but discrete, "fractionated" saccades. Clinically, the patients with PSP would appear to have difficulty mobilizing saccades when asked to look to either side. Yet, EOGs showed that the latency of saccades in the PSP patient group was not significantly different from that
EYE MOVEMENT DISORDERS
VOLUME 86 MARCH 1979
500
NORt1AL:
400
cz
PEAK VELOCITY-P.ESPONSE
0
AMPLITUDE RELATIONSHIPS:
300
0
u
w
425
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-5
0
5
10
15
20
25
(RIGHTWARDS) RESPONSE M1PLI TUDE (DEGREES)
25
NORf!IAL:
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--:
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Fig 1.-Top, Saccadic velocities determined from best curve ftt of peak velocities plotted vs corresponding response amplitudes. Bottom, Accuracy is ratio of response amplitude to the corresponding stimulus displacement.
426
CHU ET AL
,.r f SAC CADES:
(FAST EYE MOVEMENTS)
To 60° TARGETS
NORMAl
l -----'
.,
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Fig 2.-EOGs of saccades in normal patients (top) and in PSP patients (bottom). Note that those made by PSP patients were slower, smaller, and less accurate. A slow saccade seen clinically may have lower peak velocity or be composed of smaller, consecutive "fractionated" saccades.
measured in normal patients (Table 2). Similarly, there was no significant difference in saccadic durations for 5° and 10° eye movements made by either group of patients.
OPHTH AAO
head as it was rotated. The phenomenon was noted clinically ("Doll's head movements") as well as documented by EOGs (Fig 3). When the fast and slow phases of nystagmus were analyzed separately, it was apparent that for the patients with PSP, there were significant decreases in the amplitudes of the fast phases, while the slowphase gains were normaL When instructed to fixate a target moving with the rotation of the test chair, the normal patients suppressed virtually all eye movements, so the eyes tended to remain in -the center of the orbits. On the other hand, the patients with PSP were unable to suppress the drift of the eyes from the target. Consequently, the amplitudes of the fast phases were larger than those noted in the normal patients. EYE MOVEMENTS DUR!tlG HEAD ROTATI:JN IN DARKNESS
Pursuit Eye Movements Clinically, pursuit eye movements were not smooth in the abnormal, or PSP patient group, being replaced by "cogwheel" or "saccadic" pursuit movements. As indicated by EOGs, the ability of a patient with PSP to track a continuously moving target was significantly impaired (P<.OOl) as target velocity or frequency of target reversal increased (Table 3). Furthermore, if saccades were generated in an attempt to match higher target velocity, such eye movements were insufficient to bring the eye on target. Vestibular Nystagmus Vestibular nystagmus was characterized by movement of the eyes in the opposite direction from the
FIXATIONTARGET:PRESENT-
ABSENT,,,,,,,
Fig 3.-EOGs of vestibular nystagmus. During rotation in darkness, eyes deviate opposite to head rotation. If dim fixation target during rotation in otherwise darkness, deviation of eyes from center of the orbit is less.
Optokinetic Nystagmus With target displacement, the normal pattern of nystagmus was replaced by a drift of the eyes in those patients with PSP. Also, if OKN was present, the amplitudes of fast phases were significantly reduced in the patients (Fig 4).
TABLE 2 SACCADE ANALYSIS PATIENTS PARAMETER: Peak velocity* For 5° saccades For 10° saccades Maximum amplitudest Accuracy Latencyt Durationt For 5° saccades For 10° saccades
NORMAL
PSP
t TEST OF DIFFERENCE:
176.00 290.00 19.00 0.64 194.00
123.00 192.00 10.00 0.41 211.00
P<.01 P<.01 P<.01 P<.01
30.00 44.00
46.00 66.00
NS NS
NS
*Degrees per second. tDegrees. tMillisecond.
TABLE 3 PuRSUIT ANALYSIS (ACCURACY OF TRACKING) PATIENTS FREQUENCY (Hz):
0.1 0.3 0.5 0.7 0.9
NORMAL
PSP
0.96 0.90 0.89 0.83 0.83
0.90 0.78 0.58 0.45 0.32
Thirdly, slow-phase velocities in the patients were less than those found in normal patients. Fixation Clinically, fluttering movements of the eyes in two patients were prominent during fixation. Electrooculograms showed these movements to correlate to square waves (Fig 5). Although the other seven patients had steady fixation clinically, four had square waves on their electroencephalographic tracings, while three did not. All four normal patients had square waves on their tracings and steady fixation clinically.
t TEST OF DIFFERENCE: NS NS
P<.OOl P<.OOl P<.OOl
COMMENTS
The obvious defects in vertical and, especially, downgaze eye movements are among the cardinal features of progressive supranuclear palsy. As the disease progresses, gross defects in the horizontal eye movements also appear. These defects involve all major eye movement subsystems. Saccades are slower, smaller, and inaccurate. Moreover, clinically, these slow saccades include both fractionated saccades and saccades with reduced peak velocities. Surprisingly, the apparent difficulties patients with PSP seem to have in initiating saccades are not evident
CHU ET AL
428
OPHTH AAO
patients with the worst tracking also have the poorest saccades. STIMULUS:
Target Velocity: Rightwards -- 80° /sec.
NoRMAL
PSP
Fig 4.-EOGs of optokinetic nystagmus. Top Rightwards target (top). Middle, Normal response Bottom, PSP patient.
when saccadic latencies are studied with EOGs. The reason for this descrepancy is not known. Pursuit eye movements are also abnormal. Normal smooth eye movements are replaced by cogwheel tracking. When compared with normal patients of similar age, patients with PSP are less able to maintain their eyes on a target despite the insertion of saccades during the pursuit maneuver. The
Distinct abnormalities of vestibular nystagmus and OKN are obvious, too, in patients with PSP. In tests for both, a primary defect of fast phases is obvious: compared with the normal patients, fast-phase amplitudes are significantly reduced. Since, in· vestibular nystagmus, the slow-phase gain is normal, eye movement tends to drift in an opposite direction from head movement. Slow-phase velocities in OKN, however, are low because the eye tends to drift in the direction of target displacement without returning towards the center of the orbit. ACKNOWLEDGMENT The authors acknowledge the advice of Donald Calne, MD, and Steven Hunt, MD.
REFERENCES 1. Steele JC, Richardson JC, Olszewski J: Progressive supranuclear palsy. Arch Neurol 10:333-359, 1964.
2. Steele JC: Progressive supranuclear palsy. Brain 95:693-704, 1972. 3. David NJ, Mackey EA, Smith JL: Further observations in progressive supranuclear palsy. Neurology 18:349-356, 1968. 4. Pfaffenbach DD, Layton DD, Jr, Kearns TP: Ocular manifestations in progressive supranuclear palsy. Am J Ophthalmol 74: 1179-1184, 1972.
SQUARE WAVES:
5. NewmanN, Gay AJ, Stroud MH, et al: Defective rapid eye movements in progressive supranuclear palsy: An ocular electromyographic study. Brain 93:775-784, 1970.
lNTERSACCADIC PERIOD:
400
MSEC,
AMPLITUDE:
3-4
DEGREES
Fig 5.-EOGs of square waves in a patient in 'whom flutter-like eye movements were observed.
6. Troost BT, Daroff RB: The ocular motor defects in progressive supranuclear palsy. Ann Neurol 2:397-403, 1977. 7. Baloh RW, Konrad HR, Sills AW, et al: The saccade velocity test. Neurology 25: 1071-1076. 1975.