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Glabella tap sign
Journal of the Neurological Sciences, 1985, 70:257-267
257
Elsevier JNS 2546
Glabella Tap Sign Is it Due to a Lack of R2-Habituation? Nobuhiko Sunohara ~'*, Hideaki Tomi 1, Eijiro Satoyoshi t and Shigekuni Tachibana 2 tNational Centerfor Nervous, Mental and Muscular Disorders, 4-1-10gawa-tfigashi-MachL Kodaira, Tokyo (Japan 187) and 2Department of Neurosurgery, Kitasato University School of Medicine. 1-1 Kitasato-MachL Sagamihara, Kanagawa (Japan 228)
(Received 2 April, 1985) (Revised, received 14 May, 1985) (Accepted 15 May, 1985)
SUMMARY In 30 patients with Parkinson's disease, 55 patients with other neurological disorders and 25 normal subjects, both upper eyelid movements and orbicularis oculi reflexes to repetitive glabella taps were simultaneously recorded using a newly devised apparatus for the measurement of eyelid movement. Upper lid movement during the blink reflex has been thought to correspond to the late component of the two components of the orbicularis oculi reflex, and failure of habituation of the late component to repetitive stimuli has been considered to be responsible for the glabella tap sign. However, the present study showed that the eyelid lowered after the early component (R1), and habituation of the late component (R2) was recognized in 31~o of subjects with the glabeUa tap sign. This shows that there is no direct causual relationship between the glabella tap sign and lack of the habituation of the late component.
Key words: Blink reflex - Eyelid m o v e m e n t - Glabella tap sign - Habituation - Myerson's
sign
INTRODUCTION The glabella tap reflex (Overend 1896) is composed of both the contraction of the orbicularis oculi muscle and the relaxation of the levator palpebrae superioris muscle. * To whomreprint requests shouldbe sent. 0022-510X/85/$03.30 © 1985Elsevier SciencePublishers B.V.(BiomedicalDivision)
258 Electromyograms of the orbicularis oculi muscle during the reflex reveal two distinct components; an early one (R1) and a late one (R2), which are clinically fused into a single blink or twitch (Kugelberg 1952). In addition, activity of the levator palpebrae superioris muscle is completely inhibited during the reflex; reciprocal inhibition of the levator palpebrae superioris muscle (Loeffier et al. 1966). The degree of the lid closure evoked by repetitive glabella taps diminishes rapidly in normal subjects, because they become accustomed to the stimuli (habituation). In patients with Parkinson's disease or Parkinsonism, habituation is absent: "the glabella tap sign" (GuiUain et al. t924; Myerson 1944; Garland 1952), and EMG reveals a persistence of the R2-component, unlike normal subjects in whom the R2-component diminishes or disappeares with the first few taps (R2-habituation) (Rushworth 1962). The failure of the R2-habituation was considered to be responsible for the glabella tap sign (Rushworth 1962). However, the relationship between the eyelid movement and the orbicularis oculi reflex has never been fully studied. The purpose of this paper is to determine the relationship between them during repetitive stimulation. MATERIALS AND METHODS
Thirty patients with Parkinson's disease, 15 men and 15 women, ranged in age from 45 to 82 years (mean age: 60.7 + 11.0 years). Seventeen patients were in the IIIrd stage of the disability score of Hoehn and Yahr (1967) and the remainder in the IVth. Twenty-five patients with spinocerebellar degeneration, 15 of whom were women, ranged in age from 19 to 77 years (mean age: 53.1 + 13.5 years). They consisted of 17 sporadic cases of olivo-ponto-cerebellar atrophy (OPCA), 5 with dominant and 3 with recessive inheritance. Thirty patients with other neurological disorders, 16 of whom were men, consisted of 4 patients with amyotrophic lateral sclerosis, 4 with a choreic syndrome, 4 with senile dementia, 4 with cerebrovascular disorders, 3 with multiple sclerosis, 2 with schizophrenia, 2 with primary lateral sclerosis, 2 with gait apraxia, 1 with syringomyelia, 1 with senile tremor, 1 with a cranial tuberculoma, 1 with oral dyskinesia and 1 with acute pan-dysautonomia. Their ages ranged from 13 to 80 years (mean age: 53.8 + 18.9 years). All patients were free from medication for at least 1 week before the examination. Twenty-five normal control subjects, 13 of whom were women, ranged in age from 15 to 71 years, with a mean of 42.9 + 17.9 years. They were divided into two groups: 21 subjects aged under 50 (means age: 30.9 + 11.1 years) and 14 aged over 50 (mean age: 60.8 + 7.0 years). The latter was used as an age-matched normal group. Subjects sat in a comfortable chair and were asked to relax as much as possible. Then they were asked to look at a wall, 2 meters in front of them, and to maintain fixation on a point. Blink reflexes were elicited by repetitive gentle taps to the glabella with a small hammer or electrical stimuli to the supraorbital nerves with a frequency of one/s. The tap was performed on a metal plate, 10 mm in diameter, over the glabella. The plate was earthed so that the contact of the hammer triggered the weep of a cathode-ray-oscilloscope. Ten responses were recorded individually (i.e. in "Raster"). Electrical pulses were applied through bipolar surface electrodes either bilaterally to the supraorbital
259
A
r
13 Fig. 1. Diagrams to show arrangement for measuringupper lid movementsand orbicularis oculi reflexes. A: records of eyelid movements using DCamplifiers. B: records of orbicularis oculi reflexes using AC amplifiers. RI: the early component of the orbicularis oculi reflex. R2: the late component of the orbicularis oculi reflex. nerves or unilaterally. The pulse was 0.2 ms in duration and of such intensity that reflex responses were just maximum. Five stimuli were repeated. Each subject underwent four trials of repetitive stimulation in the form of the glabella tap, and the right and the left electrical stimulation on the supraorbital nerves at 5-rain intervals. The responses of the upper lids and orbicularis oculi muscles during the blink reflex were simultaneously recorded by a 4-channd amplifier (Medelec MS-6). Eyelid movements were recorded electrically using the principal of a Wheatstone-bridge circuit (Fig. 1). The fine and rigid metal wires, 100 #m in diameter and 150 mm in length, were luted just over the upper eyelashes by an adhesive agent. The attached part of the wire of the upper eyelid was coated with teflon. The water-fried cylinders, 4 turn inside diameter and 50 mm in length, were attached to the cheeks. The change in electrical resistance was amplified by DC amplifiers (Medelec AD-6). Blink reflexes of the orbicularis oculi muscle were recorded with silver-silver chloride surface electrodes of diameter 4 ram, which were placed bilaterally on the outer aspect of the lower lids. Reference electrodes were placed on the lateral surface of the nose. A ground electrode was placed under the chin. The electrical response was amplified by AC amplifiers (Medelec AA-6M or AA-6Mk III). All examinations were recorded by a tape recorder (Sony N F R 3515) and the taped records were played back for the detailed analysis. The latencies of the Rl-component and the ipsilateral R2-component were measured from the beginning of the stimulus artifact on the triggered sweep, to the initial deflection of the evoked potential. The relationship between the eyelid movement and the orbicularis oculi reflex was evaluated, in particular, the relationships between the begi'nning of the upper lid movement and the two components of the orbicularis oculi reflex and between the glabeUa tap sign and the R2-habituation. We defined that the orbicularis oeuli reflex was habituated when the amplitude of the fifth response was 20 ~o less than that of the first one (Rl-habituation or R2-habituation) as proposed by
260 Penders and Delwaide (1971). The glabella tap sign was defmed as positive when the downward movement of the upper lid of the fifth response was 70 ~o or more of the first, because the pupils were completely concealed in all subjects when the downward movement of the upper lid was 70~o or more of the natural eyelid opening. The data from examination of the glabeUa tap and electrical stimulation of both supraorbital nerves were classified into the following four patterns from the analysis of the relationship between the eyelid movement and the orbicularis oculi reflex: (A) persistence of the clinical blink reflex with R2-habituation of the electrical orbicularis oculi reflex; (B) persistent blinking without R2-habituation; (C)no persistent blinking with R2-habituation; and (D)no persistent blinking but without R2-habituation. RESULTS (1) The R I and R2 components of the orbicularis oculi reflex Bilateral R 1-components of the orbicularis oculi reflex were elicited by the glabella tap or the electrical stimulation of the supraorbital nerves bilaterally in all subjects except for one patient with acute pan-dysautonomia, in whom no Rl-components were evoked although R2-components were present. With unilateral electrical stimulation, bilateral Rl-components were detected in two normal and one Parkinsonian subjects. In the examination of the glabella tap, the R2-component was absent in 5 normal subjects, 1 with Parkinson's disease, 1 with spinocerebellar degeneration and 3 with other neurological disorders in the subjects lacking the glabella tap sign, and also absent in 1 with Parkinson's disease and 5 with other neurological disorders in the subjects showing the glabella tap sign. In the examination of the electrical stimulation of supraorbital nerves, the R2-eomponent was absent in only 2 normal subjects without persistent blinking. The mean latencies and standard deviations of the orbicularis oculi reflex elicited by glabella tap or electrical stimulation are shown in Table 1. There was no significant difference between normals, Parkinson's disease, spinocerebellar degeneration and other neurological disorders. With glabella tap nobody except one patient with spinocerebellar degeneration showed R 1-habituation. On the examination of the electrical stimulation of supraorbital nerves bilaterally, a normal subject, 1 with spinocerebellar degeneration and 1 with gait apraxia showed the Rl-habituation. (2) Upper lid movement and the R2-habituation The pattern of the blink reflex elicited by glabella tap or electrical stimulation of the bilateral supraorbital nerves are shown in Table 2. With the glabella tap, the persistent blinking, that is, the glabella tap sign (Patterns A and B) was recognized in 83.3~o, 40~o, 53.4~ and 21.4~o of the patients with Parkinson's disease, spinocerebellar degeneration, other neurological disorders and normal subjects aged over 50, respectively. Seventeen (31 ~o) of 54 subjects showing the glabdla tap sign represented the R2-habituation, i.e. Pattern A. Six. (9~o) of 66 subjects without the giabella tap sign revealed no R2-habituation, i.e. Pattern D. With electrical stimulation of supraorbital nerves, persistent blinking was seen in
261 TABLE 1 LATENCIES OF IPSILATERAL R1 AND R2 COMPONENTS (ms) R1 latency
R2 latency
14.4 + 0.9 (35) 14.4 + 1.3 (30) 14.6 + 1.3 (25)
31.2 _+3.2 (30) 31.1 + 4.4 (28) 31.1 + 3.3 (24)
14.6 + 1.7 (30)
32.3 + 3.0 (22)
10.8 + 0.5 (35) 10.9 + 0.5 (30) 10.7 + 0.6 (25)
30.9 + 3.5 (33) 31.3 + 3.9 (30) 32.9 + 5.1 (25)
10.6 + 0.4 (29)
32.5 + 4.1 (30)
(I) Glabella tap
Normal subjects Parkinson's disease Spinocerebellar degeneration Other neurological disorders (II) Electrical stimulation
Normal subjects Parkinson's disease Spinocerebellar degeneration Other neurological disorders () = number of subjects. TABLE 2
PERSISTENT BLINKING AND R2-HABITUATION A
B
C
D
Total
(1) Glabella tap
Normal subjects aged under 50 Normal subjects aged over 50 Parkinson's disease Spinocerebellar degeneration Other neurological disorders Total
0 (0%) 3 (21.4%) 6 (20%) 0 (0%) 8 (26.7%) 17 (14.2%)
0 (0~o) 0 (0%) 19 (63.3%) 10 (40%) 8 (26.7%) 37 (30.8%)
18 (85.7~o) I0 (71.4%) 5 (16.7~o) 14 (56%) 13 (43.3%) 60 (50%)
3 (14.3%) 1 (7.1%) 0 (0%) 1 (4%) 1 (3.3%) 6 (5%)
21 14 30 25 30 120
0 (0%) 1 (7.1%) 1 (3.3%) 0 (0%) 3 (10%) 5 (4.2%)
0 (0%) 2 (14.3%) 23 (76.7%) 9 (36%) 13 (43.3%) 47 (39.2%)
15 (71.4%) 9 (64.3~o) 4 (13.3%) 8 (32%) 10 (33.3%) 46 (38.3%)
6 (28.6%) 2 (2.3%) 2 (6.7%) 8 (32~'o) 4 (13.3%) 22 (18.3%)
21 14 30 25 30 120
(11) Electrical stimulation
Normal subjects aged under 50 Normal subjects aged over 50 Parkinson's disease Spinoeerebellar degeneration Other neurological disorders Total
A B C D
= = = =
persistent blinking with R2-habituation. persistent blinking without R2-habituation. no persistent blinking with R2-habituation. no persistent blinking without R2-habituation.
80~o, 3 6 ~ , 53.3~o a n d 21.4~o o f p a t i e n t s with P a r k i n s o n ' s disease, spinocerebetlar d e g e n e r a t i o n , other n e u r o l o g i c a l d i s o r d e r s a n d n o r m a l subjects aged over 50, respectively. R 2 - h a b i t u a t i o n w a s p r e s e n t in 5 (10 % ) o f 52 subjects s h o w i n g p e r s i s t e n t b l i n k i n g
262
CONTROL
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orbl, ocull EMG
,oo., 10msec
Oyold~ I
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lOmoe¢
Fig. 2. Downward movements of upper lid and orbicularis oculi reflexes in response to the glabeUa tap in normal subjects. Serial responses from the first (1) to the fifth (5) are shown. A: no persistent blinking with R2-habituation (Pattern C). B: no persistent blinking without R2-habituation (Pattern D).
263 (Pattern A), and was absent in 22 (32 ~ ) of 68 subjects without persistent blinking (Pattern D). The percentage of subjects with persistent blinking on glabella tap examination and that on the study of electrical stimulation were very similar (45 ~o and 43.4 ~o respectively). But, Pattern A was seen more frequently on glabella tap examination, and Pattern D more frequently on examination of electrical stimulation. With unilateral electrical stimulation of a supraorbital nerve, the ipsilateral response was identical to that evoked by bilateral stimulation in every subject. (3) The relationship between the upper lid movement and the orbicularis oculi reflex In subjects showing Pattern C (Fig. 2A), the upper lid began to fall slowly with the appearance of the Rl-component. Subsequently the eyelid shifted rapidly downwards whether the R2-component was present or not. Also the habituation of the blink reflex occurred regardless of whether the amplitude of the Rl-component decreased or
Parkinson A5
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10m11¢
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orbl. OCull EMQ
lOmelo
oou,,
[ ,0o,. lomle¢
Fig. 3. Upper lid movements and orbicularis oculi reflexes to the glabella tap in patients with Parkinson's disease. Serial responses from the first (1) to the ftRh (5) are shown. A: persistent blinking (Glabella tap sign) without R2-habituation (Pattern B). B and C: persistent blinking with R2-habituation (Pattern A).
264 not. The degree of eyelid downward movement was not necessarily proportional to the amplitude of the R1- and/or R2-components. In the subjects showing Pattern D (Fig. 2B), the eyelid movement to the first few taps was similar to that seen in the subjects showing Pattern C. However, the degree of eyelid closure decreased rapidly although distinct R2-components appeared with the successive stimuli. In subjects showing the glabella tap sign (Fig. 3A and B), the eyelid began to lower slowly following the Rl-component and subsequently closed rapidly regardless of whether the R2-habituation of the orbicularis oculi reflex was present (Pattern A) or not (Pattern B). In the subjects showing the glabella tap sign but having a very small or absent R2-component (Fig. 3C), it was clear that the eyelid began to move downwards following the large Rl-component and continued to close in response to each Rl-component. The relationship between eyelid movement and the orbicularis oculi reflex evoked by the electrical stimulation of the bilateral supraorbital nerves bilaterally was similar to that obtained by glabella tap in these subjects. With unilateral stimulation on the supraorbital nerve, the eyelid lowered from the Rl-component on the stimulated side and from the R2-component on the nonstimulated side except for two normal subjects having no R2-component. Eyelid movement on the non-stimulated side was faster than that on the stimulated side, and both upper lids reached the lowest closing position simultaneously. The degree of the eyelid closure on the non-stimulated side was equal to or smaller than that seen on the stimulated side (Fig. 4A and B). Among the subjects showing Pattern B on the stimulated side, a normal subject, 1 with spinocerebellar degeneration, 1 with Parkinson's disease and 1 with schizophrenia showed Pattern C on the non-stimulated side (Fig. 4C). DISCUSSION
In the past, almost all the eyelid movement during the blink reflex has been considered to correspond to the R2- rather than to the Rl-component of the orbicularis oculi reflex (Shahani and Young 1972). It is known, however, that many patients with Parkinson's disease showing the glabella tap sign manifest absence of the R2-habituation. We also obtained the same result. This led to the idea that the glabella tap sign derived from a lack of R2-habituation. The present data, however, cast doubt on this currently accepted hypothesis. The upper lid began to close at a time related to the Rl-component following stimulation of the glabeUa or the supraorbital nerves. Thirtyone percent of the subjects showing the glabella tap sign represented a gradual diminution or no clear appearance of the R2-component (i.e. R2-habituation). This indicates that there is no direct cansual relationship between failure of the R2-habituation and the glabella tap sign. The glabelta tap sign had been thought to be attributed to a release phenomenon or a loss of inhibition of a primitive reflex (Panlson and Gottlieb 1968; Pearce et al. 1968). However, the glabella tap sign is not found in children under 2 months of age
265 Control A
Panrklneon
a
Pamrklneon
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¢ s
S
4
4
3
3
4
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2
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2
2
1
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II. ol'101uellull IEIIIO
..........
n~
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1
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, . . . . . . ,.
~
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Fig. 4. Upper lid movements and orbicularis oculi reflexes to electrical stimulation of the left (.4 and B) or the fight supraorbital nerve (C). Serial responses from the first (1) to the fifth (5) are shown..4: no persistent blinking without R2-habituation; normal subject. B: persistent blinking without R2-habituation; Parkinson's disease. C: persistent blinking on the stimulated side and no persistent blinking on the non-stimulated side; Parkinson's disease.
although it was present in children 1-4 years old (Zametkin et al. 1979). Others (Clay and Ramseyer 1976; Kimura et al. 1977; Vecchierini-Blineau and Guiheneuc 1984) reported that the R2-component of the orbicularis oculi reflex was absent or could be elicited only with difficulty in children under 18 months of age. These observations also deny a direct causual relationship between the R2-habituation of the orbicularis oculi reflex, which is an electrophysiological event, and the habituation of the blink reflex as a clinical manifestation. On the other hand, the hyperexcitability of the Rl-reflex arc has been regarded as another characteristic feature of the orbicularis oculi reflex in Parkinson's disease (Rushworth 1962; Penders and Delwaide 1971; Shahani 1968). However, it is difficult
266 tO explain the occurrence of the glabella tap sign only by the hyperexcitability of the Rl-reflex arc, because all normal subjects showing a distinct and unhibited R1component did not have the glabella tap sign. The present study showed that the eyelid did not close in response to each stimulation in spite of the presence of a distinct Rl-component and sometimes also a distinct R2-component, particularly in the subjects showing no glabella tap sign but no R2-habituation (Pattern D). This finding alone appears to us sufficiently strong evidence to suggest that when the blink responses to repetitive stimuli cease or markedly diminish in amplitude, the levator palpebrae superioris muscle, which is the antagonist of the orbicularis oculi muscle, contracts, i.e. it is not inhibited. We, therefore, speculate that in normal subjects the reciprocal inhibition of the levator palpebrae superioris muscle is most marked only during the blink elicited by the first few stimuli but it is rapidly reduced or abolished during subsequent stimuli. On the other hand, it is suggested that at least in the subjects showing the glabella tap sign but R2-habituation (Pattern A), the reciprocal inhibition of the levator palpebrae superioris muscle is present following each stimulus. Thus, the persistence of reciprocal inhibition of the levator palpebrae superioris muscle seems to play an important pathogenetic role in the glabella tap sign. The discrepancies between the results of glabella tap and those of electrical stimulation of the bilateral supraorbital nerves are considered to be due to the different nature of the stimulus. Glabella tap stimulates sensory receptors directly, while electrical impulse stimulates many sensory nerve fibers within the nerve. From the present study, the R2-reflex seems to be more easily inhibited by repetitive stimuli to the receptor than to the nerve, and Rl-reflex seems to be more easily elicited by the mechanical stimulation to the receptor than by the electrical stimulation to the nerve. Spontaneous blinkings are known to start slowly (Gordon 1951). Moldaver (1973) described that the palpebral component of the orbicularis oculi muscle, which is thin and composed of rapid pale muscle, contracts first and then blinking is accompanied by a relaxation of the levator palpebrae superioris muscle which also is rapid pale muscle. Though this account of blinking also may explain the fact the upper eyelid begins to move slowly downwards after the Rl-component of the orbicularis oculi reflex, further investigations are required. Examination of unilateral stimulation to the supraorbital nerve showed that the upper eyelid on the non-stimulated side shifted downwards after the R2-component more rapidly than the eyelid on the stimulated side did, but both eyelids reached the maximum lower level of the lid closure simultaneously. This suggests that there is a complex coordinating mechanism between both upper lid movements during the blink reflex, presumably based on interaction between the orbicularis oculi reflex and reciprocal inhibition of the levator palpebrae superioris muscle. ACKNOWLEDGEMENTS We wish to thank Dr. G. Rushworth, University of Oxford, for his valuable comments.
267 REFERENCES Clay, S.A. and J. C. Ramseyer (1976) The orbicularis oculi reflex in infancy and childhood, Neurology (NY), 26: 521-524. Garland, H.G. (1952) Parkinsonism, Brit. Med. J., I: 153-155. Gordon, G. (1951) Observations upon the movements of the eyelids, Brit. J. Ophthalmol., 35:339-351. Guillain, G., T. Alajouanine and R. Marqu~zy (1924) L'exag~ration du r6flexe nasopalpgbral dans les syndromes post-encgphalitiques, C.R. Soc. Biol., 91: 364-365. Hoehn, M~H. and M. D. Yahr (1967) Parkinsonism, onset, progression, and mortality, Neurology (Minneap.), 17: 427-442. Kimura, J., J. Bodensteiner and T. Yamada (1977) Electrically elicited blink reflex in normal neonates Arch. Neurol. (Chic.), 34: 246-249. Kugelberg, E. (1952) Facial reflexes, Brain, 75: 385-396. Loeffler, J. D., B. Slatt and W. F. Hoyt (1966) Motor abnormalities of the eyelids in Parkinson's disease - Electromyographic observations, Arch. Ophthalmol., 76: 178-185. Moldaver, J. (1973) Some comments on blink reflexes. In: J.E. Desmedt (Eds.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 3, Karger, Basel, pp. 658-659. Myerson, A. (1944)Tap and thrust responses in Parkinson's disease, Arch. Neurol. Psychiat., 61: 480. Overend, W. (1896) Preliminary note on a new cranial reflex, Lancet, i: 619. Paulson, G. and G. Gottlieb (1968) Development reflexes - - The reappearance of foetal and neonatal reflexes in aged patients, Brain, 91: 37-52. Pearce, J., H. Aziz and J.C. Gallagher (1968) Primitive reflex activity in primary and symptomatic Parkinsonism, J. Neurol. Neurosurg. Psychiat., 31: 501-508. Penders, C.A. and P.J. Delwaide (1971) Blink reflexes in patients with Parkinsonism before and during therapy, J. Neurol. Neurosurg. Psychiat., 34: 674-678. Rushworth, G. (1962) Observation on blink reflexes, J. NeuroL Neurosurg. Psychiat., 25: 93-108. Shahani, B. (1968) Effects of sleep on human reflexes with a double component, J. Neurol. Neurosurg. Psychiat., 31: 574-579. Shahani, B. T. and R. R. Young (1972) Human orbicularis oculi reflexes, Neurology (Minneap.), 22:149-154. Vecchierini-Blineau, M. F. and P. Guiheneuc (1984) Maturation of the blink reflex in infants, Europ. NeuroL, 23: 449-458. Z ametkin, A.J., J.R. Stevens and R. Pittman (1979) Ontogeny of spontaneous blinking and of habituation of the blink reflex, Ann. Neurol., 5: 453-457.
257
Elsevier JNS 2546
Glabella Tap Sign Is it Due to a Lack of R2-Habituation? Nobuhiko Sunohara ~'*, Hideaki Tomi 1, Eijiro Satoyoshi t and Shigekuni Tachibana 2 tNational Centerfor Nervous, Mental and Muscular Disorders, 4-1-10gawa-tfigashi-MachL Kodaira, Tokyo (Japan 187) and 2Department of Neurosurgery, Kitasato University School of Medicine. 1-1 Kitasato-MachL Sagamihara, Kanagawa (Japan 228)
(Received 2 April, 1985) (Revised, received 14 May, 1985) (Accepted 15 May, 1985)
SUMMARY In 30 patients with Parkinson's disease, 55 patients with other neurological disorders and 25 normal subjects, both upper eyelid movements and orbicularis oculi reflexes to repetitive glabella taps were simultaneously recorded using a newly devised apparatus for the measurement of eyelid movement. Upper lid movement during the blink reflex has been thought to correspond to the late component of the two components of the orbicularis oculi reflex, and failure of habituation of the late component to repetitive stimuli has been considered to be responsible for the glabella tap sign. However, the present study showed that the eyelid lowered after the early component (R1), and habituation of the late component (R2) was recognized in 31~o of subjects with the glabeUa tap sign. This shows that there is no direct causual relationship between the glabella tap sign and lack of the habituation of the late component.
Key words: Blink reflex - Eyelid m o v e m e n t - Glabella tap sign - Habituation - Myerson's
sign
INTRODUCTION The glabella tap reflex (Overend 1896) is composed of both the contraction of the orbicularis oculi muscle and the relaxation of the levator palpebrae superioris muscle. * To whomreprint requests shouldbe sent. 0022-510X/85/$03.30 © 1985Elsevier SciencePublishers B.V.(BiomedicalDivision)
258 Electromyograms of the orbicularis oculi muscle during the reflex reveal two distinct components; an early one (R1) and a late one (R2), which are clinically fused into a single blink or twitch (Kugelberg 1952). In addition, activity of the levator palpebrae superioris muscle is completely inhibited during the reflex; reciprocal inhibition of the levator palpebrae superioris muscle (Loeffier et al. 1966). The degree of the lid closure evoked by repetitive glabella taps diminishes rapidly in normal subjects, because they become accustomed to the stimuli (habituation). In patients with Parkinson's disease or Parkinsonism, habituation is absent: "the glabella tap sign" (GuiUain et al. t924; Myerson 1944; Garland 1952), and EMG reveals a persistence of the R2-component, unlike normal subjects in whom the R2-component diminishes or disappeares with the first few taps (R2-habituation) (Rushworth 1962). The failure of the R2-habituation was considered to be responsible for the glabella tap sign (Rushworth 1962). However, the relationship between the eyelid movement and the orbicularis oculi reflex has never been fully studied. The purpose of this paper is to determine the relationship between them during repetitive stimulation. MATERIALS AND METHODS
Thirty patients with Parkinson's disease, 15 men and 15 women, ranged in age from 45 to 82 years (mean age: 60.7 + 11.0 years). Seventeen patients were in the IIIrd stage of the disability score of Hoehn and Yahr (1967) and the remainder in the IVth. Twenty-five patients with spinocerebellar degeneration, 15 of whom were women, ranged in age from 19 to 77 years (mean age: 53.1 + 13.5 years). They consisted of 17 sporadic cases of olivo-ponto-cerebellar atrophy (OPCA), 5 with dominant and 3 with recessive inheritance. Thirty patients with other neurological disorders, 16 of whom were men, consisted of 4 patients with amyotrophic lateral sclerosis, 4 with a choreic syndrome, 4 with senile dementia, 4 with cerebrovascular disorders, 3 with multiple sclerosis, 2 with schizophrenia, 2 with primary lateral sclerosis, 2 with gait apraxia, 1 with syringomyelia, 1 with senile tremor, 1 with a cranial tuberculoma, 1 with oral dyskinesia and 1 with acute pan-dysautonomia. Their ages ranged from 13 to 80 years (mean age: 53.8 + 18.9 years). All patients were free from medication for at least 1 week before the examination. Twenty-five normal control subjects, 13 of whom were women, ranged in age from 15 to 71 years, with a mean of 42.9 + 17.9 years. They were divided into two groups: 21 subjects aged under 50 (means age: 30.9 + 11.1 years) and 14 aged over 50 (mean age: 60.8 + 7.0 years). The latter was used as an age-matched normal group. Subjects sat in a comfortable chair and were asked to relax as much as possible. Then they were asked to look at a wall, 2 meters in front of them, and to maintain fixation on a point. Blink reflexes were elicited by repetitive gentle taps to the glabella with a small hammer or electrical stimuli to the supraorbital nerves with a frequency of one/s. The tap was performed on a metal plate, 10 mm in diameter, over the glabella. The plate was earthed so that the contact of the hammer triggered the weep of a cathode-ray-oscilloscope. Ten responses were recorded individually (i.e. in "Raster"). Electrical pulses were applied through bipolar surface electrodes either bilaterally to the supraorbital
259
A
r
13 Fig. 1. Diagrams to show arrangement for measuringupper lid movementsand orbicularis oculi reflexes. A: records of eyelid movements using DCamplifiers. B: records of orbicularis oculi reflexes using AC amplifiers. RI: the early component of the orbicularis oculi reflex. R2: the late component of the orbicularis oculi reflex. nerves or unilaterally. The pulse was 0.2 ms in duration and of such intensity that reflex responses were just maximum. Five stimuli were repeated. Each subject underwent four trials of repetitive stimulation in the form of the glabella tap, and the right and the left electrical stimulation on the supraorbital nerves at 5-rain intervals. The responses of the upper lids and orbicularis oculi muscles during the blink reflex were simultaneously recorded by a 4-channd amplifier (Medelec MS-6). Eyelid movements were recorded electrically using the principal of a Wheatstone-bridge circuit (Fig. 1). The fine and rigid metal wires, 100 #m in diameter and 150 mm in length, were luted just over the upper eyelashes by an adhesive agent. The attached part of the wire of the upper eyelid was coated with teflon. The water-fried cylinders, 4 turn inside diameter and 50 mm in length, were attached to the cheeks. The change in electrical resistance was amplified by DC amplifiers (Medelec AD-6). Blink reflexes of the orbicularis oculi muscle were recorded with silver-silver chloride surface electrodes of diameter 4 ram, which were placed bilaterally on the outer aspect of the lower lids. Reference electrodes were placed on the lateral surface of the nose. A ground electrode was placed under the chin. The electrical response was amplified by AC amplifiers (Medelec AA-6M or AA-6Mk III). All examinations were recorded by a tape recorder (Sony N F R 3515) and the taped records were played back for the detailed analysis. The latencies of the Rl-component and the ipsilateral R2-component were measured from the beginning of the stimulus artifact on the triggered sweep, to the initial deflection of the evoked potential. The relationship between the eyelid movement and the orbicularis oculi reflex was evaluated, in particular, the relationships between the begi'nning of the upper lid movement and the two components of the orbicularis oculi reflex and between the glabeUa tap sign and the R2-habituation. We defined that the orbicularis oeuli reflex was habituated when the amplitude of the fifth response was 20 ~o less than that of the first one (Rl-habituation or R2-habituation) as proposed by
260 Penders and Delwaide (1971). The glabella tap sign was defmed as positive when the downward movement of the upper lid of the fifth response was 70 ~o or more of the first, because the pupils were completely concealed in all subjects when the downward movement of the upper lid was 70~o or more of the natural eyelid opening. The data from examination of the glabeUa tap and electrical stimulation of both supraorbital nerves were classified into the following four patterns from the analysis of the relationship between the eyelid movement and the orbicularis oculi reflex: (A) persistence of the clinical blink reflex with R2-habituation of the electrical orbicularis oculi reflex; (B) persistent blinking without R2-habituation; (C)no persistent blinking with R2-habituation; and (D)no persistent blinking but without R2-habituation. RESULTS (1) The R I and R2 components of the orbicularis oculi reflex Bilateral R 1-components of the orbicularis oculi reflex were elicited by the glabella tap or the electrical stimulation of the supraorbital nerves bilaterally in all subjects except for one patient with acute pan-dysautonomia, in whom no Rl-components were evoked although R2-components were present. With unilateral electrical stimulation, bilateral Rl-components were detected in two normal and one Parkinsonian subjects. In the examination of the glabella tap, the R2-component was absent in 5 normal subjects, 1 with Parkinson's disease, 1 with spinocerebellar degeneration and 3 with other neurological disorders in the subjects lacking the glabella tap sign, and also absent in 1 with Parkinson's disease and 5 with other neurological disorders in the subjects showing the glabella tap sign. In the examination of the electrical stimulation of supraorbital nerves, the R2-eomponent was absent in only 2 normal subjects without persistent blinking. The mean latencies and standard deviations of the orbicularis oculi reflex elicited by glabella tap or electrical stimulation are shown in Table 1. There was no significant difference between normals, Parkinson's disease, spinocerebellar degeneration and other neurological disorders. With glabella tap nobody except one patient with spinocerebellar degeneration showed R 1-habituation. On the examination of the electrical stimulation of supraorbital nerves bilaterally, a normal subject, 1 with spinocerebellar degeneration and 1 with gait apraxia showed the Rl-habituation. (2) Upper lid movement and the R2-habituation The pattern of the blink reflex elicited by glabella tap or electrical stimulation of the bilateral supraorbital nerves are shown in Table 2. With the glabella tap, the persistent blinking, that is, the glabella tap sign (Patterns A and B) was recognized in 83.3~o, 40~o, 53.4~ and 21.4~o of the patients with Parkinson's disease, spinocerebellar degeneration, other neurological disorders and normal subjects aged over 50, respectively. Seventeen (31 ~o) of 54 subjects showing the glabdla tap sign represented the R2-habituation, i.e. Pattern A. Six. (9~o) of 66 subjects without the giabella tap sign revealed no R2-habituation, i.e. Pattern D. With electrical stimulation of supraorbital nerves, persistent blinking was seen in
261 TABLE 1 LATENCIES OF IPSILATERAL R1 AND R2 COMPONENTS (ms) R1 latency
R2 latency
14.4 + 0.9 (35) 14.4 + 1.3 (30) 14.6 + 1.3 (25)
31.2 _+3.2 (30) 31.1 + 4.4 (28) 31.1 + 3.3 (24)
14.6 + 1.7 (30)
32.3 + 3.0 (22)
10.8 + 0.5 (35) 10.9 + 0.5 (30) 10.7 + 0.6 (25)
30.9 + 3.5 (33) 31.3 + 3.9 (30) 32.9 + 5.1 (25)
10.6 + 0.4 (29)
32.5 + 4.1 (30)
(I) Glabella tap
Normal subjects Parkinson's disease Spinocerebellar degeneration Other neurological disorders (II) Electrical stimulation
Normal subjects Parkinson's disease Spinocerebellar degeneration Other neurological disorders () = number of subjects. TABLE 2
PERSISTENT BLINKING AND R2-HABITUATION A
B
C
D
Total
(1) Glabella tap
Normal subjects aged under 50 Normal subjects aged over 50 Parkinson's disease Spinocerebellar degeneration Other neurological disorders Total
0 (0%) 3 (21.4%) 6 (20%) 0 (0%) 8 (26.7%) 17 (14.2%)
0 (0~o) 0 (0%) 19 (63.3%) 10 (40%) 8 (26.7%) 37 (30.8%)
18 (85.7~o) I0 (71.4%) 5 (16.7~o) 14 (56%) 13 (43.3%) 60 (50%)
3 (14.3%) 1 (7.1%) 0 (0%) 1 (4%) 1 (3.3%) 6 (5%)
21 14 30 25 30 120
0 (0%) 1 (7.1%) 1 (3.3%) 0 (0%) 3 (10%) 5 (4.2%)
0 (0%) 2 (14.3%) 23 (76.7%) 9 (36%) 13 (43.3%) 47 (39.2%)
15 (71.4%) 9 (64.3~o) 4 (13.3%) 8 (32%) 10 (33.3%) 46 (38.3%)
6 (28.6%) 2 (2.3%) 2 (6.7%) 8 (32~'o) 4 (13.3%) 22 (18.3%)
21 14 30 25 30 120
(11) Electrical stimulation
Normal subjects aged under 50 Normal subjects aged over 50 Parkinson's disease Spinoeerebellar degeneration Other neurological disorders Total
A B C D
= = = =
persistent blinking with R2-habituation. persistent blinking without R2-habituation. no persistent blinking with R2-habituation. no persistent blinking without R2-habituation.
80~o, 3 6 ~ , 53.3~o a n d 21.4~o o f p a t i e n t s with P a r k i n s o n ' s disease, spinocerebetlar d e g e n e r a t i o n , other n e u r o l o g i c a l d i s o r d e r s a n d n o r m a l subjects aged over 50, respectively. R 2 - h a b i t u a t i o n w a s p r e s e n t in 5 (10 % ) o f 52 subjects s h o w i n g p e r s i s t e n t b l i n k i n g
262
CONTROL
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4
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orbl, ocull EMG
,oo., 10msec
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lOmoe¢
Fig. 2. Downward movements of upper lid and orbicularis oculi reflexes in response to the glabeUa tap in normal subjects. Serial responses from the first (1) to the fifth (5) are shown. A: no persistent blinking with R2-habituation (Pattern C). B: no persistent blinking without R2-habituation (Pattern D).
263 (Pattern A), and was absent in 22 (32 ~ ) of 68 subjects without persistent blinking (Pattern D). The percentage of subjects with persistent blinking on glabella tap examination and that on the study of electrical stimulation were very similar (45 ~o and 43.4 ~o respectively). But, Pattern A was seen more frequently on glabella tap examination, and Pattern D more frequently on examination of electrical stimulation. With unilateral electrical stimulation of a supraorbital nerve, the ipsilateral response was identical to that evoked by bilateral stimulation in every subject. (3) The relationship between the upper lid movement and the orbicularis oculi reflex In subjects showing Pattern C (Fig. 2A), the upper lid began to fall slowly with the appearance of the Rl-component. Subsequently the eyelid shifted rapidly downwards whether the R2-component was present or not. Also the habituation of the blink reflex occurred regardless of whether the amplitude of the Rl-component decreased or
Parkinson A5
B
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t ~
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10m11¢
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orbl. OCull EMQ
lOmelo
oou,,
[ ,0o,. lomle¢
Fig. 3. Upper lid movements and orbicularis oculi reflexes to the glabella tap in patients with Parkinson's disease. Serial responses from the first (1) to the ftRh (5) are shown. A: persistent blinking (Glabella tap sign) without R2-habituation (Pattern B). B and C: persistent blinking with R2-habituation (Pattern A).
264 not. The degree of eyelid downward movement was not necessarily proportional to the amplitude of the R1- and/or R2-components. In the subjects showing Pattern D (Fig. 2B), the eyelid movement to the first few taps was similar to that seen in the subjects showing Pattern C. However, the degree of eyelid closure decreased rapidly although distinct R2-components appeared with the successive stimuli. In subjects showing the glabella tap sign (Fig. 3A and B), the eyelid began to lower slowly following the Rl-component and subsequently closed rapidly regardless of whether the R2-habituation of the orbicularis oculi reflex was present (Pattern A) or not (Pattern B). In the subjects showing the glabella tap sign but having a very small or absent R2-component (Fig. 3C), it was clear that the eyelid began to move downwards following the large Rl-component and continued to close in response to each Rl-component. The relationship between eyelid movement and the orbicularis oculi reflex evoked by the electrical stimulation of the bilateral supraorbital nerves bilaterally was similar to that obtained by glabella tap in these subjects. With unilateral stimulation on the supraorbital nerve, the eyelid lowered from the Rl-component on the stimulated side and from the R2-component on the nonstimulated side except for two normal subjects having no R2-component. Eyelid movement on the non-stimulated side was faster than that on the stimulated side, and both upper lids reached the lowest closing position simultaneously. The degree of the eyelid closure on the non-stimulated side was equal to or smaller than that seen on the stimulated side (Fig. 4A and B). Among the subjects showing Pattern B on the stimulated side, a normal subject, 1 with spinocerebellar degeneration, 1 with Parkinson's disease and 1 with schizophrenia showed Pattern C on the non-stimulated side (Fig. 4C). DISCUSSION
In the past, almost all the eyelid movement during the blink reflex has been considered to correspond to the R2- rather than to the Rl-component of the orbicularis oculi reflex (Shahani and Young 1972). It is known, however, that many patients with Parkinson's disease showing the glabella tap sign manifest absence of the R2-habituation. We also obtained the same result. This led to the idea that the glabella tap sign derived from a lack of R2-habituation. The present data, however, cast doubt on this currently accepted hypothesis. The upper lid began to close at a time related to the Rl-component following stimulation of the glabeUa or the supraorbital nerves. Thirtyone percent of the subjects showing the glabella tap sign represented a gradual diminution or no clear appearance of the R2-component (i.e. R2-habituation). This indicates that there is no direct cansual relationship between failure of the R2-habituation and the glabella tap sign. The glabelta tap sign had been thought to be attributed to a release phenomenon or a loss of inhibition of a primitive reflex (Panlson and Gottlieb 1968; Pearce et al. 1968). However, the glabella tap sign is not found in children under 2 months of age
265 Control A
Panrklneon
a
Pamrklneon
B
¢ s
S
4
4
3
3
4
3
2
'1 ......
2
2
1
,.g. R2 ,-'--I""
II. ol'101uellull IEIIIO
..........
n~
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1
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Ra
eo
~!,-~lOl
, . . . . . . ,.
~
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~
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fl, IIlll.
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~.____[,-I1¢
Fig. 4. Upper lid movements and orbicularis oculi reflexes to electrical stimulation of the left (.4 and B) or the fight supraorbital nerve (C). Serial responses from the first (1) to the fifth (5) are shown..4: no persistent blinking without R2-habituation; normal subject. B: persistent blinking without R2-habituation; Parkinson's disease. C: persistent blinking on the stimulated side and no persistent blinking on the non-stimulated side; Parkinson's disease.
although it was present in children 1-4 years old (Zametkin et al. 1979). Others (Clay and Ramseyer 1976; Kimura et al. 1977; Vecchierini-Blineau and Guiheneuc 1984) reported that the R2-component of the orbicularis oculi reflex was absent or could be elicited only with difficulty in children under 18 months of age. These observations also deny a direct causual relationship between the R2-habituation of the orbicularis oculi reflex, which is an electrophysiological event, and the habituation of the blink reflex as a clinical manifestation. On the other hand, the hyperexcitability of the Rl-reflex arc has been regarded as another characteristic feature of the orbicularis oculi reflex in Parkinson's disease (Rushworth 1962; Penders and Delwaide 1971; Shahani 1968). However, it is difficult
266 tO explain the occurrence of the glabella tap sign only by the hyperexcitability of the Rl-reflex arc, because all normal subjects showing a distinct and unhibited R1component did not have the glabella tap sign. The present study showed that the eyelid did not close in response to each stimulation in spite of the presence of a distinct Rl-component and sometimes also a distinct R2-component, particularly in the subjects showing no glabella tap sign but no R2-habituation (Pattern D). This finding alone appears to us sufficiently strong evidence to suggest that when the blink responses to repetitive stimuli cease or markedly diminish in amplitude, the levator palpebrae superioris muscle, which is the antagonist of the orbicularis oculi muscle, contracts, i.e. it is not inhibited. We, therefore, speculate that in normal subjects the reciprocal inhibition of the levator palpebrae superioris muscle is most marked only during the blink elicited by the first few stimuli but it is rapidly reduced or abolished during subsequent stimuli. On the other hand, it is suggested that at least in the subjects showing the glabella tap sign but R2-habituation (Pattern A), the reciprocal inhibition of the levator palpebrae superioris muscle is present following each stimulus. Thus, the persistence of reciprocal inhibition of the levator palpebrae superioris muscle seems to play an important pathogenetic role in the glabella tap sign. The discrepancies between the results of glabella tap and those of electrical stimulation of the bilateral supraorbital nerves are considered to be due to the different nature of the stimulus. Glabella tap stimulates sensory receptors directly, while electrical impulse stimulates many sensory nerve fibers within the nerve. From the present study, the R2-reflex seems to be more easily inhibited by repetitive stimuli to the receptor than to the nerve, and Rl-reflex seems to be more easily elicited by the mechanical stimulation to the receptor than by the electrical stimulation to the nerve. Spontaneous blinkings are known to start slowly (Gordon 1951). Moldaver (1973) described that the palpebral component of the orbicularis oculi muscle, which is thin and composed of rapid pale muscle, contracts first and then blinking is accompanied by a relaxation of the levator palpebrae superioris muscle which also is rapid pale muscle. Though this account of blinking also may explain the fact the upper eyelid begins to move slowly downwards after the Rl-component of the orbicularis oculi reflex, further investigations are required. Examination of unilateral stimulation to the supraorbital nerve showed that the upper eyelid on the non-stimulated side shifted downwards after the R2-component more rapidly than the eyelid on the stimulated side did, but both eyelids reached the maximum lower level of the lid closure simultaneously. This suggests that there is a complex coordinating mechanism between both upper lid movements during the blink reflex, presumably based on interaction between the orbicularis oculi reflex and reciprocal inhibition of the levator palpebrae superioris muscle. ACKNOWLEDGEMENTS We wish to thank Dr. G. Rushworth, University of Oxford, for his valuable comments.
267 REFERENCES Clay, S.A. and J. C. Ramseyer (1976) The orbicularis oculi reflex in infancy and childhood, Neurology (NY), 26: 521-524. Garland, H.G. (1952) Parkinsonism, Brit. Med. J., I: 153-155. Gordon, G. (1951) Observations upon the movements of the eyelids, Brit. J. Ophthalmol., 35:339-351. Guillain, G., T. Alajouanine and R. Marqu~zy (1924) L'exag~ration du r6flexe nasopalpgbral dans les syndromes post-encgphalitiques, C.R. Soc. Biol., 91: 364-365. Hoehn, M~H. and M. D. Yahr (1967) Parkinsonism, onset, progression, and mortality, Neurology (Minneap.), 17: 427-442. Kimura, J., J. Bodensteiner and T. Yamada (1977) Electrically elicited blink reflex in normal neonates Arch. Neurol. (Chic.), 34: 246-249. Kugelberg, E. (1952) Facial reflexes, Brain, 75: 385-396. Loeffler, J. D., B. Slatt and W. F. Hoyt (1966) Motor abnormalities of the eyelids in Parkinson's disease - Electromyographic observations, Arch. Ophthalmol., 76: 178-185. Moldaver, J. (1973) Some comments on blink reflexes. In: J.E. Desmedt (Eds.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 3, Karger, Basel, pp. 658-659. Myerson, A. (1944)Tap and thrust responses in Parkinson's disease, Arch. Neurol. Psychiat., 61: 480. Overend, W. (1896) Preliminary note on a new cranial reflex, Lancet, i: 619. Paulson, G. and G. Gottlieb (1968) Development reflexes - - The reappearance of foetal and neonatal reflexes in aged patients, Brain, 91: 37-52. Pearce, J., H. Aziz and J.C. Gallagher (1968) Primitive reflex activity in primary and symptomatic Parkinsonism, J. Neurol. Neurosurg. Psychiat., 31: 501-508. Penders, C.A. and P.J. Delwaide (1971) Blink reflexes in patients with Parkinsonism before and during therapy, J. Neurol. Neurosurg. Psychiat., 34: 674-678. Rushworth, G. (1962) Observation on blink reflexes, J. NeuroL Neurosurg. Psychiat., 25: 93-108. Shahani, B. (1968) Effects of sleep on human reflexes with a double component, J. Neurol. Neurosurg. Psychiat., 31: 574-579. Shahani, B. T. and R. R. Young (1972) Human orbicularis oculi reflexes, Neurology (Minneap.), 22:149-154. Vecchierini-Blineau, M. F. and P. Guiheneuc (1984) Maturation of the blink reflex in infants, Europ. NeuroL, 23: 449-458. Z ametkin, A.J., J.R. Stevens and R. Pittman (1979) Ontogeny of spontaneous blinking and of habituation of the blink reflex, Ann. Neurol., 5: 453-457.