Eur. Neurol. 18: 157 165 (1979)
Reciprocal Reflex Activity in Ocular Muscles: Implications in Spontaneous Blinking and Bell’s Phenomenon1 Angel Esteban and Emilio Salinero Laboratory of Clinical Neurophysiology, Ciudad Sanitaria Provincial, Madrid
Key Words. Blinking • Blink reflex • Bell’s phenomenon • Levator palpebrae muscle • Rectus
superior muscle • Orbicularis oculi muscle
Introduction
Ever since ocular electromyography (EMG) was introduced by Bjork and Kugelberg (1953a, b) as a technique with clinical applications in man, a great number of papers have been published in which this method has been used to study a wide range of oculomotor disorders. The anatomical proximity and functional synergism of the levator palpebrae (m. lev. palp.) and rectus superior (m. rect. sup.) mus cles during voluntary vertical ocular movements ' Read in part at the 9th International Congress of Electroencephalography and Clinical Neurophysiolo gy, Amsterdam, September 1977.
make their precise identification difficult dur ing EMG recordings. Usually, however, their antagonistic behavior during blinking and voluntary eyelid occlusion (Bjork, 1954b) is enough to differentiate them. In some oculomotor disorders, however, very specific problems of eyelid motility are observed, such as blepharospasm vs. blepharocholisis, in diseases of the basal ganglia (Esteban and Gimênez-Roldàn, 1973) or disorders in synkinetic upward ocular displacement such as the abolition of Bell’s phenomenon in amyo trophic lateral sclerosis (Esteban et ai, 1978). In these instances, the aforementioned differen tiation methods prove practically useless.
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Abstract. Levator palpebrae (m. lev. palp.) and rectus superior (m. rect. sup.) are two synergistic muscles in vertical gaze movements. However, they show an antagonistic behavior during electrically induced blink and glabellar reflexes. This can be considered as an easy and useful method for their differentiation in the electrophysiological study of certain oculopalpebral motor disorders. Blinking consists of a series of reflex activities, the most outstanding ones being an early m. lev. palp, basal activity inhibition, followed by the activation of the orbicularis oculi muscle and a brief increase in m. rect. sup. activity (reflex Bell phenomenon). This coordinated reflex organization could be perfectly related to that known in other human nociceptive reflexes.
Esteban/Salincro
158
Material and Method 17 patients have been studied, all of whom pre sented some disorder in their oculopalpebral move ments: 2 patients with peripheral idiopathic facial palsy and 2 with myotonic dystrophy who showed a weakness or paralysis of the musculus orbicularis oculi (m. orb. oc.); 6 patients with amyotrophic lateral sclerosis and 1 with pseudobulbar palsy in which there was an alteration of Bell’s phenomenon; 3 with pro gressive supranuclear palsy, 1 with postencephalitic parkinsonism, and 2 with mesencephalic lesions, of tumoral and vascular etiology, respectively, who showed conjugate vertical gaze disorders associated in some cases with eyelid motility impairment, such as spasmodic m. orb. oc. contraction (blepharospasm) or prolonged m. lev. palp, inhibition (blcpharocholisis). In each case, the following tests were performed: (a) eye movement in pursuit of a moving target in the vertical plane; (b) forced eyelid occlusion; (c) sponta neous blinking; (d) blink reflex elicited by a supra orbital electrical stimulus, and (e) blink reflex caused by a glabellar tap. The recordings have been obtained by means of coaxial needle electrodes. In m. orb. oc., the electrode was inserted into the external portion of the lower eyelid; for m. lev. palp, and m. rect. sup., the needle was inserted through the skin in the middle portion of the upper eyelid and directed towards the roof of the orbit, resting on the superior part of the equator of the eyeball. The position of the electrode in each one of these muscles was controlled by observing their maximum electric activity on the oscilloscope; the
cable of the electrode was then secured in that position. All the recordings were carried out with the subject in supine position. Electrical percutaneous shocks of quadrangular-wave stimuli of 0.5 msec dura tion and varying intensity were given on the internal supraorbital area. For the mechanical stimulus, finger tapping on the glabella was used. Signals were ampli fied by means of a two-channel clinical Mcdelec EMG MS-5 recorder.
Results
Pursuit o f a Moving Target in the Vertical Plane During the primary gaze position, both m. lev. palp, and m. rect. sup. show a very intense activity, which progressively increases in ampli tude and intensity when a slow upward pursuit movement is carried out and diminishes gently and progressively with the opposite movement (fig. 1). A total absence of activity is very difficult to obtain, even with extreme infravergence, especially in m. rect. sup. In this muscle, brief phasic bursts have been observed, general ly appearing during the initial and final mo ments of the movement, which probably corre spond to microsaccades of steady fixation. These impulses do not appear in m. lev. palp.; in this muscle, a brief and abrupt interruption of its basal activity has been observed only incidentally (see spontaneous blinking). No activity has been recorded in m. orb. oc. during these manoeuvres. Forced Eyelid Occlusion When the patient is asked to perform a forced sustained contraction of m. orb. oc. (fig. 2), m. rect. sup. shows a sudden intensifi cation of its activity, which begins soon after the closing of the eyelids and continues until after their opening, and which corresponds to the clinically upward displacement of the eye-
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The aim of this study is to demonstrate that in every case, the electrically or mechanically elicited blink reflex behaves in opposite and systematically different ways in m. lev. palp, and m. rect. sup.; it can, therefore, be consid ered in every instance as an easy, clear-cut, differentiation method. This behavior can ex plain some details in the physiological mecha nism of spontaneous blinking and Bell’s phe nomenon and why they must both be consid ered as essential parts of a general coordinated reflex of ocular protection.
Ocular Retlcx Activity in Blinking
159
m.rect sup.
m. orb oc._____________ __________
m.rect. sup.
m lev palp.
V#
^=0
m orb. oc
m rect. sup.
-
- 500 msec
mm-
1 mV m. lev palp.
m orb.-oc.
• m. orb. oc.
m. rect. sup
m. lev. palp.
m. orb o c ____________________ ____________________
m. orb. oc.
- 500 msec
m.lev. palp -------500 msec m. rect. sup. . — . >, ■>
m. orb.oc.
Fig. 1. EMC recordings from m. rect. sup. (a) and m. lev. palp, (b) during movements on vertical gaze. Basal activity on primary position gaze progressively increases during slow upward movement and decreases
with the downward gaze. M. rect. sup. shows brief superimposed discharges in initial (bottom trace) and final phases of movement. In m. orb. oc., no activity is seen in any position of the gaze.
balls during this manoeuvre (Bell’s phenome non). Conversely, an abrupt interruption of the activity of m. lev. palp, is observed, with a slight delay regarding the beginning of the activity of m. orb. oc. which is usually total at first, but with potentials which gradually begin to group, until recovery of the basal activity. This occurs suddenly and, contrary to what happens in m. rect. sup., it usually precedes slightly the ceasing of activity of m. orb. oc. In spite of Bjork and Kugelberg's(\953b) opinion we have neither found evidence of a dimin
ishing of the density prior to the closing of the eyelid nor of intensified postinhibition activity. Spontaneous Blinking The modifications which occur in the basal activity during spontaneous blinking are inverse in m. lev. palp, and m. rect. sup. (fig. 3). In m. lev. palp., there is an inhibition which begins and ends abruptly and which, as in the case of voluntary eyelid occlusion, is only complete in its first part. Its duration varies between 70 and 100 msec. During this inhibition period, a dis-
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m orb, oc
160
Esteban/Salincro
m. re c t sup
mm
m orb. oc
m reef sup
m orb
m. orb. oc
300 m sec m. lev. palp. «
m
é ^ ----------- —
~-‘— r— ■«-
m orb. oc. .......................................................... M M
' -------------------------- i - W
* . ........
m. lev. palp.
*TnryT>!rp^ a . « » n i » l i » n < iin t» '» i« iim n . . . iw )()|ii> n n iiillllin t » i » .b ■
Fig. 2. Sustained voluntary occlusion of the eyes. In m. rect. sup., increase in activity is observed corresponding to Bell’s clinical phenomenon (a); in m.
lev. palp., inhibition of basal activity is obtained (b). These same manoeuvres are repeated several times (c, d). See text.
charge can be registered in m. orb. oc., of equal duration only when m. orb. oc. detection is performed in the pars palpebralis of the muscle. The potential is smaller, or even absent, when the recording is made in the pars orbitaria. It is also absent in the cases studied with peripheral idiopathic facial palsy. In m. rect. sup., each spontaneous blinking action induces a phasic overactivation.
The alternate recording of m. lev. palp, and m. rect. sup. simultaneously with m. orb. oc. during this electrically induced blink reflex has produced the following results: the R 1 and R2 m. orb. oc. reflex discharges are correlated with m. lev. palp, basal activity inhibition (fig. 4). A remarkable fact, however, is that this m. lev. palp, inhibition has systematically preceded the appearance of m. orb. oc. potentials. When the intensity of the electrical stimulus was progres sively increased, it was observed that the lowest strength produced a decrease in m. lev. palp, activity, coinciding precisely with the future Rl and R2 orbicular responses, not yet present. The inhibition gradually becomes complete as the potentials of m. orb. oc. become more apparent. The eyelid activity which exists be tween the two reflex inhibitions is evident at
Electrically Induced Blink Reflex The electrical stimulation of the supraorbital nerve induces a reflex contraction of m. orb. oc. This reflex has two components: an early, ipsilateral potential, known as R l, and a later, bilateral response, known as R2 (Kugelberg, 1952; Rushworth, 1962).
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m. orb. oc.
Ocular Reflex Activity in Blinking
first, and then disappears, producing a zone of continuous inhibition which goes from the be ginning of the R1 potential to beyond the end of the R2 (fig. 5). As for m. rect. sup., no trace of inhibition of its activity with the orbicular potentials has been observed in any of the cases. Neither have we been able to demonstrate any reflex over activation effect (fig. 4). The basal activity of this muscle has remained unmodified, even when we have tried to bring about its facilita tion by means of voluntary eyelid occlusion. The possibility that a reflex response might be concealed by the intense electrical activity of the muscle in primary position is a problem we have tried to avoid by infravergence;but in this case we have not either observed any increases
1mV
m. orb.
Fig. 4. Electrically induced blink reflex. M. orb. oc responses coincide with an inhibition of m. lev. palp, activity (a); there is no modification in m. rect. sup. activity (b). Several superimposed traces.
which could be related to reflex orbicular potentials. Glabellar Reflex With a mechanical stimulus in the region of the glabella, orbicular responses are produced similar to the R1 and R2 potentials of the
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Fig. 3. EMG recording of spontaneous blinking. Simultaneous recording of m. lev. palp, and m. orb. oc. (a), and m. rect. sup. and m. orb. oc. (b). Duration of burst in m. orb. oc. is of same duration as m. lev. palp, inhibition when recording is from its pars palpcbralis (a; left), is smaller in the pars orbitaria (a; middle) or, even, is absent as in facial palsy (a; right). In m. rect. sup. each blinking movement causes a brief increase in activity (arrows).
161
Esteban/Saiinero
162
Vv
vf«r^'S
2
»
v '; .
4
V ~ v */V/' • y
5 m/*
7 m>4
9 mA
Fig. 5. Two examples of blink reflex in m. lev. palp. Weakstrength stimuli give rise to inhibi tion pauses in m. lev. palp, activi ty prior to the appearance of m. orb. oc. potentials. This inhibition progressively increases in relation to the rise in intensity of electri cal shocks and the consecutive output of m. orb. oc. reflex responses. M. lev. palp, in upper traces; m. orb. oc. in lower traces. Discussion
M. lev. palp, acts as an antagonist mucle for m. orb. oc. M. rect. sup., on the other hand, acts synergistically with this muscle. However, both m. lev. palp, and m. rect. sup. must not be considered as antagonists in all situations; their behavior is synergistic during vertical rotation movements of the eyeball, in which case the electric recordings are practically impossible to differentiate.
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electrically induced blink reflex (Rushworth, 1962). In m. lev. palp., a systematic phasic inhibition is produced coinciding with the or bicular potentials which it usually outlasts. In m. rect. sup., contrary to what occurs with the electrical stimulus, we have been able to ob serve an increase of activity in direct relation with the m. orb. oc. discharge. The duration, as in the case of the inhibition of m. lev. palp., is also greater than that of the m. orb. oc. poten tial (fig. 6).
Fig. 6. Glabellar tapping causes an m. orb. oc. discharge related to an inhibition of m. lev. palp, ac tivity (a) and an overactivation of the m. rcct. sup. (b).
All the tests which have been used in this study and in which m. orb. oc. took part have shown differential values in the EMG detection of these two muscles. However, in some partic ular situations, in the oculopalpebral pathology we have studied, especially those which includ ed alteration of the eyelid activity in excess (blepharospasm) or defect (ptosis and blepharocholisis), the only method that has proved to be definitely trustworthy has been the blink re flex, whether induced electrically or mecanically. In our opinion it must be stressed as an easy, useful method in ocular electrophysiological studies. During spontaneous blinking, there is an abrupt interruption in m. lev. palp, activity. Its duration is apparently independent of the dura tion of the normally associated discharge of m. orb. oc. Both phenomena, however, coincide very precisely when the m. orb. oc. potential has been recorded in the pars palpebralis of the
163
muscle. This portion is made up of fibers of histochemical type 2 (phasic), and is the part that normally acts as a complement of the inhibition of m. lev. palp, during spontaneous blinking, giving it a greater efficiency (Moldaver, 1973). However, it has been well known since Sherrington (1898) that complete periph eral facial palsy does not prevent the paralyzed eyelid from falling a few milimeters during blinking. In this lesion, we have found that a normal inhibitory pause in m. lev. palp, does exist, in spite of the absence of any type of orbicular activity. Furthermore, as we have been able to dem onstrate, an inhibitory reflex effect in m. lev. palp, systematically precedes the reflex activa tion of m. orb. oc. During low-strength stimuli, inhibitory pauses can be obtained which coin cide with the latent periods of the reflex orbic ular potentials, not yet present; with higher intensities, when the orbicular potentials have appeared, the total inhibition of m. lev. palp, extends from the beginning of the R1 response to beyond the ending of R2. In agreement with
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Ocular Reflex Activity in Blinking
Esteban/Salinero
164
participation of both sides of the brain (Bender, 1960; Pasik et al„ 1969). Blinking must be considered in its ultimate purpose as an ocular defense mechanism. Its organization is perfectly comparable to that demonstrated in other human nociceptive re flexes such as those of tire abdominal and erector spinae {Kugelberg and Hagbarth, 1958), and plantar and withdrawal reflexes in the lower limb {Kugelberg et al, 1960; Hagbarth, 1960). Just as in these, a coordinated response for protection is made by means of a segmental reflex mechanism following the principle of reciprocal innervation {Creed et al, 1972). The central control of this activity could probably be organized in certain brainstem zones as would suggest the results of Szentagothai's (1950) experimental studies, in which the stimulation of Cajal’s interstitial and Darkschewitsch’s nuclei produces coordinated activi ties in the different extrinsic ocular muscles. References Bender, M.B.: Comments on the physiology and pathology of eye movements in the vertical plane. J. nerv. ment. Dis. 130: 456-466 (1960). Bender, M.B.: Disorders of eye movements; in Vinken and Bruyn, Handbook of clinical neurology, vol. 1, pp. 574-630 (North-Holland, Amsterdam 1969). Bjork, A.: Electromyographic study of conditions involving limited mobility of the eye, chiefly due to neurogenic pareses. Br. J. Ophthal. 38: 528-544 (1954a). Bjork, A.: Electromyographic studies on the coordina tion of antagonistic muscles in cases of abducens and facial palsy. Br. J. Ophthal. 38: 605-615 (1954b). Bjork, A. and Kugelberg, E.: Motor unit activity in the human extraocular muscles. Electroenceph. clin. Neurophysiol. 5: 271-278 (1953a). Bjork, A. and Kugelberg, E.: The electrical activity of the muscles of the eye and eyelids in various position and during movement. Electroenceph. clin. Neurophysiol. 5: 595-602 (1953b).
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Bjork's (1954b) suggestion, we believe that the reflex contraction of m. orb. oc. is fastest and with the least resistance during blinking because of the early inhibitory reflex in m. lev. palp., which has a lower threshold of induction. During sustained voluntary closing of the eyes, the resulting modifications in m. lev. palp, and m. rect. sup. activities show different fea tures. M. lev. palp, basal activity is suddenly blocked; by means of an irregular addition of potentials, blocking is progressively reduced to the point where it returns abruptly, shortly before the ceasing of m. orb. oc. activity. On the contrary, m. rect. sup. shows an increase in its activity which appears soon after the begin ning of m. orb. oc. activity and disappears shortly after its completion. These facts, first described by Bjork (1954b) represent the EMG counterpart of the clinically well-known synkinetic upward ocular deviation associated with forced closing of the eyes (Bell’s phenomenon). But this same m. rect. sup. overactivation has also been obtained during spontaneous blinking {Bjork, 1954a) and glabellar tapping, although we have never been able to find it during electrically induced blink reflex. This reflex Bell phenomenon could confirm Bell's observa tion in his classic description ( Wilkins and Brody, 1969), later corroborated by Bender (1960, 1969), of a brief, upward movement of the eyeballs in spontaneous blinking. Its sys tematic absence in the electrical blink reflex does not have an easy explanation; it is possible that the unilateral stimulus used was not appro priate or sufficient to induce this vertical ocular movement. Bell’s clinical phenomenon cannot be obtained with the voluntary occlusion of just one eye, not even by impeding fixation of the gaze in a dark chamber, and it is also well known that conjugate ocular motility in the vertical plane, both of voluntary and reflex types (vestibular caloric tests), requires the
165
Ocular Reflex Activity in Blinking
Moldaver, J.: Some comments on blink reflexes', in Desmedt, New developments in electromyography and clinical neurophysiology, vol. 3, pp. 658-659 (Kargcr, Basel 1973). Pasik, P.; Pasik, T., and Bender, M.B.: The pretectal syndrome in monkeys. I. Disturbances of gaze and body posture. Brain 92: 521—534 (1969). Rushworth, G.: Observations on blink reflexes. J. Neurol. Neurosurg. Psychiat. 25: 93-109 (1962). Sherrington, C.S.: On the reciprocal innervation of antagonistic muscles. Proc. R. Soc. 64: 179-181 (1898). Szentagothai, J.: Recherches experimentales sur les voies oculogyres. Sem. Hop. Paris 63: 2989-2995 (1950). Wilkins, R.H. and Brody, LA.: Neurological classics. XXVI. Bell’s palsy and Bell’s phenomenon. Archs Neurol., Chicago 21: 661-699 (1969). Received: June 9,1978 Accepted: June 30, 1978 Dr. A. Esteban, Laboratory of Clinical Neurophysiology, Ciudad Sanitaria Provincial, c/o Dr. Esquerdo, 46, Madrid 30 (Spain)
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Creed, R.S.; Denny-Brown, D.; Eccles, J.C.; Liddell, E.G.T., and Sherrington, C.S.: Reflex activity of the spinal cord (Oxford University Press, London 1972). Esteban, A. and Gimenez-Roldan, S.: Intermittent blepharocholisis; a study of its mechanism in a certain striatal disorder. Excerpta Med. Int. Congr. Ser., No. 296, p. 130 (1973). Esteban, A.; De Andres, C., and Gimenez-Roldan, S.: Abnormalities of Bell’s phenomenon in amyotro phic lateral sclerosis. A clinical and electrophysiological evaluation. J. Neurol. Neurosurg. Psychiat. 41: 690 698 (1978). Hagbarth, K.E.: Spinal withdrawal reflex in the human lower limbs. J. Neurol. Neurosurg. Psychiat. 23: 222 -227 (1960). Kugelberg, E.: Facial reflexes. Brain 75: 385 - 396 (1952). Kugelberg, E. and Hagbarth, K.E.: Spinal mechanism of the abdominal and erector spinae skin reflexes. Brain 81: 290-304 (1958). Kugelberg, E.; Eklund, K., and Grimby, L.: An elec tromyographic study of the nociceptive reflexes of the lower limb. Mechanism of the plantar re sponses. Brain 83: 394-410 (1960).
Reciprocal Reflex Activity in Ocular Muscles: Implications in Spontaneous Blinking and Bell’s Phenomenon1 Angel Esteban and Emilio Salinero Laboratory of Clinical Neurophysiology, Ciudad Sanitaria Provincial, Madrid
Key Words. Blinking • Blink reflex • Bell’s phenomenon • Levator palpebrae muscle • Rectus
superior muscle • Orbicularis oculi muscle
Introduction
Ever since ocular electromyography (EMG) was introduced by Bjork and Kugelberg (1953a, b) as a technique with clinical applications in man, a great number of papers have been published in which this method has been used to study a wide range of oculomotor disorders. The anatomical proximity and functional synergism of the levator palpebrae (m. lev. palp.) and rectus superior (m. rect. sup.) mus cles during voluntary vertical ocular movements ' Read in part at the 9th International Congress of Electroencephalography and Clinical Neurophysiolo gy, Amsterdam, September 1977.
make their precise identification difficult dur ing EMG recordings. Usually, however, their antagonistic behavior during blinking and voluntary eyelid occlusion (Bjork, 1954b) is enough to differentiate them. In some oculomotor disorders, however, very specific problems of eyelid motility are observed, such as blepharospasm vs. blepharocholisis, in diseases of the basal ganglia (Esteban and Gimênez-Roldàn, 1973) or disorders in synkinetic upward ocular displacement such as the abolition of Bell’s phenomenon in amyo trophic lateral sclerosis (Esteban et ai, 1978). In these instances, the aforementioned differen tiation methods prove practically useless.
Downloaded by: Karolinska Institutet, University Library 130.237.122.245 - 7/7/2017 7:13:57 AM
Abstract. Levator palpebrae (m. lev. palp.) and rectus superior (m. rect. sup.) are two synergistic muscles in vertical gaze movements. However, they show an antagonistic behavior during electrically induced blink and glabellar reflexes. This can be considered as an easy and useful method for their differentiation in the electrophysiological study of certain oculopalpebral motor disorders. Blinking consists of a series of reflex activities, the most outstanding ones being an early m. lev. palp, basal activity inhibition, followed by the activation of the orbicularis oculi muscle and a brief increase in m. rect. sup. activity (reflex Bell phenomenon). This coordinated reflex organization could be perfectly related to that known in other human nociceptive reflexes.
Esteban/Salincro
158
Material and Method 17 patients have been studied, all of whom pre sented some disorder in their oculopalpebral move ments: 2 patients with peripheral idiopathic facial palsy and 2 with myotonic dystrophy who showed a weakness or paralysis of the musculus orbicularis oculi (m. orb. oc.); 6 patients with amyotrophic lateral sclerosis and 1 with pseudobulbar palsy in which there was an alteration of Bell’s phenomenon; 3 with pro gressive supranuclear palsy, 1 with postencephalitic parkinsonism, and 2 with mesencephalic lesions, of tumoral and vascular etiology, respectively, who showed conjugate vertical gaze disorders associated in some cases with eyelid motility impairment, such as spasmodic m. orb. oc. contraction (blepharospasm) or prolonged m. lev. palp, inhibition (blcpharocholisis). In each case, the following tests were performed: (a) eye movement in pursuit of a moving target in the vertical plane; (b) forced eyelid occlusion; (c) sponta neous blinking; (d) blink reflex elicited by a supra orbital electrical stimulus, and (e) blink reflex caused by a glabellar tap. The recordings have been obtained by means of coaxial needle electrodes. In m. orb. oc., the electrode was inserted into the external portion of the lower eyelid; for m. lev. palp, and m. rect. sup., the needle was inserted through the skin in the middle portion of the upper eyelid and directed towards the roof of the orbit, resting on the superior part of the equator of the eyeball. The position of the electrode in each one of these muscles was controlled by observing their maximum electric activity on the oscilloscope; the
cable of the electrode was then secured in that position. All the recordings were carried out with the subject in supine position. Electrical percutaneous shocks of quadrangular-wave stimuli of 0.5 msec dura tion and varying intensity were given on the internal supraorbital area. For the mechanical stimulus, finger tapping on the glabella was used. Signals were ampli fied by means of a two-channel clinical Mcdelec EMG MS-5 recorder.
Results
Pursuit o f a Moving Target in the Vertical Plane During the primary gaze position, both m. lev. palp, and m. rect. sup. show a very intense activity, which progressively increases in ampli tude and intensity when a slow upward pursuit movement is carried out and diminishes gently and progressively with the opposite movement (fig. 1). A total absence of activity is very difficult to obtain, even with extreme infravergence, especially in m. rect. sup. In this muscle, brief phasic bursts have been observed, general ly appearing during the initial and final mo ments of the movement, which probably corre spond to microsaccades of steady fixation. These impulses do not appear in m. lev. palp.; in this muscle, a brief and abrupt interruption of its basal activity has been observed only incidentally (see spontaneous blinking). No activity has been recorded in m. orb. oc. during these manoeuvres. Forced Eyelid Occlusion When the patient is asked to perform a forced sustained contraction of m. orb. oc. (fig. 2), m. rect. sup. shows a sudden intensifi cation of its activity, which begins soon after the closing of the eyelids and continues until after their opening, and which corresponds to the clinically upward displacement of the eye-
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The aim of this study is to demonstrate that in every case, the electrically or mechanically elicited blink reflex behaves in opposite and systematically different ways in m. lev. palp, and m. rect. sup.; it can, therefore, be consid ered in every instance as an easy, clear-cut, differentiation method. This behavior can ex plain some details in the physiological mecha nism of spontaneous blinking and Bell’s phe nomenon and why they must both be consid ered as essential parts of a general coordinated reflex of ocular protection.
Ocular Retlcx Activity in Blinking
159
m.rect sup.
m. orb oc._____________ __________
m.rect. sup.
m lev palp.
V#
^=0
m orb. oc
m rect. sup.
-
- 500 msec
mm-
1 mV m. lev palp.
m orb.-oc.
• m. orb. oc.
m. rect. sup
m. lev. palp.
m. orb o c ____________________ ____________________
m. orb. oc.
- 500 msec
m.lev. palp -------500 msec m. rect. sup. . — . >, ■>
m. orb.oc.
Fig. 1. EMC recordings from m. rect. sup. (a) and m. lev. palp, (b) during movements on vertical gaze. Basal activity on primary position gaze progressively increases during slow upward movement and decreases
with the downward gaze. M. rect. sup. shows brief superimposed discharges in initial (bottom trace) and final phases of movement. In m. orb. oc., no activity is seen in any position of the gaze.
balls during this manoeuvre (Bell’s phenome non). Conversely, an abrupt interruption of the activity of m. lev. palp, is observed, with a slight delay regarding the beginning of the activity of m. orb. oc. which is usually total at first, but with potentials which gradually begin to group, until recovery of the basal activity. This occurs suddenly and, contrary to what happens in m. rect. sup., it usually precedes slightly the ceasing of activity of m. orb. oc. In spite of Bjork and Kugelberg's(\953b) opinion we have neither found evidence of a dimin
ishing of the density prior to the closing of the eyelid nor of intensified postinhibition activity. Spontaneous Blinking The modifications which occur in the basal activity during spontaneous blinking are inverse in m. lev. palp, and m. rect. sup. (fig. 3). In m. lev. palp., there is an inhibition which begins and ends abruptly and which, as in the case of voluntary eyelid occlusion, is only complete in its first part. Its duration varies between 70 and 100 msec. During this inhibition period, a dis-
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m orb, oc
160
Esteban/Salincro
m. re c t sup
mm
m orb. oc
m reef sup
m orb
m. orb. oc
300 m sec m. lev. palp. «
m
é ^ ----------- —
~-‘— r— ■«-
m orb. oc. .......................................................... M M
' -------------------------- i - W
* . ........
m. lev. palp.
*TnryT>!rp^ a . « » n i » l i » n < iin t» '» i« iim n . . . iw )()|ii> n n iiillllin t » i » .b ■
Fig. 2. Sustained voluntary occlusion of the eyes. In m. rect. sup., increase in activity is observed corresponding to Bell’s clinical phenomenon (a); in m.
lev. palp., inhibition of basal activity is obtained (b). These same manoeuvres are repeated several times (c, d). See text.
charge can be registered in m. orb. oc., of equal duration only when m. orb. oc. detection is performed in the pars palpebralis of the muscle. The potential is smaller, or even absent, when the recording is made in the pars orbitaria. It is also absent in the cases studied with peripheral idiopathic facial palsy. In m. rect. sup., each spontaneous blinking action induces a phasic overactivation.
The alternate recording of m. lev. palp, and m. rect. sup. simultaneously with m. orb. oc. during this electrically induced blink reflex has produced the following results: the R 1 and R2 m. orb. oc. reflex discharges are correlated with m. lev. palp, basal activity inhibition (fig. 4). A remarkable fact, however, is that this m. lev. palp, inhibition has systematically preceded the appearance of m. orb. oc. potentials. When the intensity of the electrical stimulus was progres sively increased, it was observed that the lowest strength produced a decrease in m. lev. palp, activity, coinciding precisely with the future Rl and R2 orbicular responses, not yet present. The inhibition gradually becomes complete as the potentials of m. orb. oc. become more apparent. The eyelid activity which exists be tween the two reflex inhibitions is evident at
Electrically Induced Blink Reflex The electrical stimulation of the supraorbital nerve induces a reflex contraction of m. orb. oc. This reflex has two components: an early, ipsilateral potential, known as R l, and a later, bilateral response, known as R2 (Kugelberg, 1952; Rushworth, 1962).
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m. orb. oc.
Ocular Reflex Activity in Blinking
first, and then disappears, producing a zone of continuous inhibition which goes from the be ginning of the R1 potential to beyond the end of the R2 (fig. 5). As for m. rect. sup., no trace of inhibition of its activity with the orbicular potentials has been observed in any of the cases. Neither have we been able to demonstrate any reflex over activation effect (fig. 4). The basal activity of this muscle has remained unmodified, even when we have tried to bring about its facilita tion by means of voluntary eyelid occlusion. The possibility that a reflex response might be concealed by the intense electrical activity of the muscle in primary position is a problem we have tried to avoid by infravergence;but in this case we have not either observed any increases
1mV
m. orb.
Fig. 4. Electrically induced blink reflex. M. orb. oc responses coincide with an inhibition of m. lev. palp, activity (a); there is no modification in m. rect. sup. activity (b). Several superimposed traces.
which could be related to reflex orbicular potentials. Glabellar Reflex With a mechanical stimulus in the region of the glabella, orbicular responses are produced similar to the R1 and R2 potentials of the
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Fig. 3. EMG recording of spontaneous blinking. Simultaneous recording of m. lev. palp, and m. orb. oc. (a), and m. rect. sup. and m. orb. oc. (b). Duration of burst in m. orb. oc. is of same duration as m. lev. palp, inhibition when recording is from its pars palpcbralis (a; left), is smaller in the pars orbitaria (a; middle) or, even, is absent as in facial palsy (a; right). In m. rect. sup. each blinking movement causes a brief increase in activity (arrows).
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Vv
vf«r^'S
2
»
v '; .
4
V ~ v */V/' • y
5 m/*
7 m>4
9 mA
Fig. 5. Two examples of blink reflex in m. lev. palp. Weakstrength stimuli give rise to inhibi tion pauses in m. lev. palp, activi ty prior to the appearance of m. orb. oc. potentials. This inhibition progressively increases in relation to the rise in intensity of electri cal shocks and the consecutive output of m. orb. oc. reflex responses. M. lev. palp, in upper traces; m. orb. oc. in lower traces. Discussion
M. lev. palp, acts as an antagonist mucle for m. orb. oc. M. rect. sup., on the other hand, acts synergistically with this muscle. However, both m. lev. palp, and m. rect. sup. must not be considered as antagonists in all situations; their behavior is synergistic during vertical rotation movements of the eyeball, in which case the electric recordings are practically impossible to differentiate.
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electrically induced blink reflex (Rushworth, 1962). In m. lev. palp., a systematic phasic inhibition is produced coinciding with the or bicular potentials which it usually outlasts. In m. rect. sup., contrary to what occurs with the electrical stimulus, we have been able to ob serve an increase of activity in direct relation with the m. orb. oc. discharge. The duration, as in the case of the inhibition of m. lev. palp., is also greater than that of the m. orb. oc. poten tial (fig. 6).
Fig. 6. Glabellar tapping causes an m. orb. oc. discharge related to an inhibition of m. lev. palp, ac tivity (a) and an overactivation of the m. rcct. sup. (b).
All the tests which have been used in this study and in which m. orb. oc. took part have shown differential values in the EMG detection of these two muscles. However, in some partic ular situations, in the oculopalpebral pathology we have studied, especially those which includ ed alteration of the eyelid activity in excess (blepharospasm) or defect (ptosis and blepharocholisis), the only method that has proved to be definitely trustworthy has been the blink re flex, whether induced electrically or mecanically. In our opinion it must be stressed as an easy, useful method in ocular electrophysiological studies. During spontaneous blinking, there is an abrupt interruption in m. lev. palp, activity. Its duration is apparently independent of the dura tion of the normally associated discharge of m. orb. oc. Both phenomena, however, coincide very precisely when the m. orb. oc. potential has been recorded in the pars palpebralis of the
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muscle. This portion is made up of fibers of histochemical type 2 (phasic), and is the part that normally acts as a complement of the inhibition of m. lev. palp, during spontaneous blinking, giving it a greater efficiency (Moldaver, 1973). However, it has been well known since Sherrington (1898) that complete periph eral facial palsy does not prevent the paralyzed eyelid from falling a few milimeters during blinking. In this lesion, we have found that a normal inhibitory pause in m. lev. palp, does exist, in spite of the absence of any type of orbicular activity. Furthermore, as we have been able to dem onstrate, an inhibitory reflex effect in m. lev. palp, systematically precedes the reflex activa tion of m. orb. oc. During low-strength stimuli, inhibitory pauses can be obtained which coin cide with the latent periods of the reflex orbic ular potentials, not yet present; with higher intensities, when the orbicular potentials have appeared, the total inhibition of m. lev. palp, extends from the beginning of the R1 response to beyond the ending of R2. In agreement with
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participation of both sides of the brain (Bender, 1960; Pasik et al„ 1969). Blinking must be considered in its ultimate purpose as an ocular defense mechanism. Its organization is perfectly comparable to that demonstrated in other human nociceptive re flexes such as those of tire abdominal and erector spinae {Kugelberg and Hagbarth, 1958), and plantar and withdrawal reflexes in the lower limb {Kugelberg et al, 1960; Hagbarth, 1960). Just as in these, a coordinated response for protection is made by means of a segmental reflex mechanism following the principle of reciprocal innervation {Creed et al, 1972). The central control of this activity could probably be organized in certain brainstem zones as would suggest the results of Szentagothai's (1950) experimental studies, in which the stimulation of Cajal’s interstitial and Darkschewitsch’s nuclei produces coordinated activi ties in the different extrinsic ocular muscles. References Bender, M.B.: Comments on the physiology and pathology of eye movements in the vertical plane. J. nerv. ment. Dis. 130: 456-466 (1960). Bender, M.B.: Disorders of eye movements; in Vinken and Bruyn, Handbook of clinical neurology, vol. 1, pp. 574-630 (North-Holland, Amsterdam 1969). Bjork, A.: Electromyographic study of conditions involving limited mobility of the eye, chiefly due to neurogenic pareses. Br. J. Ophthal. 38: 528-544 (1954a). Bjork, A.: Electromyographic studies on the coordina tion of antagonistic muscles in cases of abducens and facial palsy. Br. J. Ophthal. 38: 605-615 (1954b). Bjork, A. and Kugelberg, E.: Motor unit activity in the human extraocular muscles. Electroenceph. clin. Neurophysiol. 5: 271-278 (1953a). Bjork, A. and Kugelberg, E.: The electrical activity of the muscles of the eye and eyelids in various position and during movement. Electroenceph. clin. Neurophysiol. 5: 595-602 (1953b).
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Bjork's (1954b) suggestion, we believe that the reflex contraction of m. orb. oc. is fastest and with the least resistance during blinking because of the early inhibitory reflex in m. lev. palp., which has a lower threshold of induction. During sustained voluntary closing of the eyes, the resulting modifications in m. lev. palp, and m. rect. sup. activities show different fea tures. M. lev. palp, basal activity is suddenly blocked; by means of an irregular addition of potentials, blocking is progressively reduced to the point where it returns abruptly, shortly before the ceasing of m. orb. oc. activity. On the contrary, m. rect. sup. shows an increase in its activity which appears soon after the begin ning of m. orb. oc. activity and disappears shortly after its completion. These facts, first described by Bjork (1954b) represent the EMG counterpart of the clinically well-known synkinetic upward ocular deviation associated with forced closing of the eyes (Bell’s phenomenon). But this same m. rect. sup. overactivation has also been obtained during spontaneous blinking {Bjork, 1954a) and glabellar tapping, although we have never been able to find it during electrically induced blink reflex. This reflex Bell phenomenon could confirm Bell's observa tion in his classic description ( Wilkins and Brody, 1969), later corroborated by Bender (1960, 1969), of a brief, upward movement of the eyeballs in spontaneous blinking. Its sys tematic absence in the electrical blink reflex does not have an easy explanation; it is possible that the unilateral stimulus used was not appro priate or sufficient to induce this vertical ocular movement. Bell’s clinical phenomenon cannot be obtained with the voluntary occlusion of just one eye, not even by impeding fixation of the gaze in a dark chamber, and it is also well known that conjugate ocular motility in the vertical plane, both of voluntary and reflex types (vestibular caloric tests), requires the
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Moldaver, J.: Some comments on blink reflexes', in Desmedt, New developments in electromyography and clinical neurophysiology, vol. 3, pp. 658-659 (Kargcr, Basel 1973). Pasik, P.; Pasik, T., and Bender, M.B.: The pretectal syndrome in monkeys. I. Disturbances of gaze and body posture. Brain 92: 521—534 (1969). Rushworth, G.: Observations on blink reflexes. J. Neurol. Neurosurg. Psychiat. 25: 93-109 (1962). Sherrington, C.S.: On the reciprocal innervation of antagonistic muscles. Proc. R. Soc. 64: 179-181 (1898). Szentagothai, J.: Recherches experimentales sur les voies oculogyres. Sem. Hop. Paris 63: 2989-2995 (1950). Wilkins, R.H. and Brody, LA.: Neurological classics. XXVI. Bell’s palsy and Bell’s phenomenon. Archs Neurol., Chicago 21: 661-699 (1969). Received: June 9,1978 Accepted: June 30, 1978 Dr. A. Esteban, Laboratory of Clinical Neurophysiology, Ciudad Sanitaria Provincial, c/o Dr. Esquerdo, 46, Madrid 30 (Spain)
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Creed, R.S.; Denny-Brown, D.; Eccles, J.C.; Liddell, E.G.T., and Sherrington, C.S.: Reflex activity of the spinal cord (Oxford University Press, London 1972). Esteban, A. and Gimenez-Roldan, S.: Intermittent blepharocholisis; a study of its mechanism in a certain striatal disorder. Excerpta Med. Int. Congr. Ser., No. 296, p. 130 (1973). Esteban, A.; De Andres, C., and Gimenez-Roldan, S.: Abnormalities of Bell’s phenomenon in amyotro phic lateral sclerosis. A clinical and electrophysiological evaluation. J. Neurol. Neurosurg. Psychiat. 41: 690 698 (1978). Hagbarth, K.E.: Spinal withdrawal reflex in the human lower limbs. J. Neurol. Neurosurg. Psychiat. 23: 222 -227 (1960). Kugelberg, E.: Facial reflexes. Brain 75: 385 - 396 (1952). Kugelberg, E. and Hagbarth, K.E.: Spinal mechanism of the abdominal and erector spinae skin reflexes. Brain 81: 290-304 (1958). Kugelberg, E.; Eklund, K., and Grimby, L.: An elec tromyographic study of the nociceptive reflexes of the lower limb. Mechanism of the plantar re sponses. Brain 83: 394-410 (1960).
