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Recruitment of single motor units in the human blink reflex
Neuroscience Letters, 34 (1982) 301-305
301
Elsevier Scientific Publishers Ireland L:d.
RECRUITMENT OF SINGLE MOTOR UNITS IN THE HUMAN BLINK REFLEX
g. DENGLER* F. RECHL and A. STRUPPLER
Department o f Neurology, Technical University Miinchen, MOhlstrasse 28, D-8000 Mtinchen 80 (F. R. G./ (Received November 15th, 1982; Accepted N~vember I'P~, 1982)
Key wc+rds: single motor units - human blink reflex
The recruitment of single motor units (MU) in the early (RI) and late (R2) components of the electrically evoked human blink reflex (BR) was studied using bipolar needle electrodes with a limited take-off area. It could be shown that the same MUs c-_,ndischarge in R! and R2 of a BR as well aN during voluntary eyelid contraction. At repetitive stimulation (1 Hz), facilitation of MU discharges in R I and habituation in R2 became apparent. The visible reflex eyelid contraction may mainly be due to rel~titive MU diu:harges in R2. The dischargc:s of the same MUs in RI, however, contribute to it and shorten the latency betw~n stimwus and reflex response.
The electrically evoked blink reflex (BR) is a double component trigemino-facia~ brainstem reflex [5, 7, 9]. The early component (RI, latency 8-12 ms) is conducted through an oligosynaptic pontine reflex arc and appears unilaterally in the or bicularis oculi muscle on the stimulated side [4]. There is considerable evidence that R I is not a monosynaptic stretch reflex, as thought by the early authors [5, 7, 10], but rather an exteroceptiv¢ ~.ui.,~zJ~ous reflex [9, Ill. Its biological role, however, is still undefined. The second bilateral componen~t (R2, latency 25-40 ms) passes along polysynaptic medullary path,+ays and resembles the corneal reflex in several respects [6]. It is agreed to be a protective reflex for the eye. Little is known about the discharge pattern of single motor units (SMU, MU) in the BR. Gordon [3] has studied SMUs during various eyelid movements and found repetitive discharges i;~ spontaneous blinking and in the corneal reflex. Trontelj and Trontelj [ l l ] measured the jitter of RI using single-fibre EMG techniiques. The purpose of the present investigation was to study the recruitment of SMUs in the components of the BR. The question to b-. answered was whether the same MU's discharge in R1 and R2 z-nd in voluntary eyelid contraction. Ten normal volupteers aged from 22 to 53 years (mean 28.3 years) ~vere investigate1. The BR were elicited by electrical stimulation of the supraorbital nerve * To whom correspondence should be setAt. 0306.3940/82/0(gg)-0(K~0/$ 02.75 g,,) 1982 Elsevier Scientific Publishers Ireland Ltd.
302
using surface electrodes [2]. The stimulus ivtensity was increased stepwis¢ until the interference of SMU potentials made their identification impossible (0.5-10 mA; 0.1 ms). "[he reflex responses; were recorded etectromyographically from tile orbicularisoculi muscle of the lower eydid on the stimulated(Ic~t)side,Fme, bipolar needle electrodes with a limited tr,tke-off area were used. The needles were inserted into the preseptal part of the muscle, that is between the p.-~ritarsal and ~pitarsal part. 3MUs were identified and labelled by their characteristic action potential configuration (amplitude, duration, number of peaks). The BR activity was in most cases simultaneously recorded by means of surface electrodes [2]. Thesignals were amplified Coandpass 80-3200 Hz), displayed on a storage oscilloscope and stored on a magnetic tape. For further evaluation, they wers fed to a digital store, displayed on an oscilloscope (1024 data points) and plotted out. Several MUs, mostly 5-10, could be labelled and followed through consecutive
~ 8LINKREFLEX
!
B
lo, my
t I0.2 mV
C
10 msec 0.1mV
['ig. !. A ~nd B, blink reflex of a normal subject simultaneously recorded with a bipolar needle electrode CA) anu surface electrodes (El). C: blink reflex of another normal subject recorded with a bipolar needle ~.lectrode The arrow indicates the stimulus onset.
3~)3
BR trials in each subject. Two or lhree needle positions were investigated. A tolal c4" 78 MUs could be studied. All MUs show,~i discharges in RI and R2 of consccufive BR trials, frequently even within RI and R2 of the same BR (57 MU). Fig. I illustrates a B R recorded simultaneously with a bipolar neeale (A) and suriace electrodes 013). An MU with a characteristic potential configuration discharges in RI as well as in R2, overlapping with another MU ~n the beginrLing 3f R2. Generally, the firing threshold was lower for R2 than for P,.l. Mostly 1-3 MUs had been recruited in R2 until a:furthe: increase of the stimulu.,., i.~:ltensity evoked the first discharges in RI. Sanes et al. [8] recently elso reported a low~.i• threshold of P,2 under various experimental conditions. Repetitive discharges of SMUs were common in R2 and occurred rarely in R I. Fig. !C shows a BR with an MU firing twice in R, and 3 times in R2. The discharge frequencies, as calculated from single interpotentiaJ intervals, ranged between 100 and 150 Hz in R2 and reached peak values of about 2:~0 Hz in R1. This is in g~od agreement with the observations of Gordon [3], who fou,'d [,eak firing frequencies of about 180 Hz in spontaneous eye blinks. The high frequeeLcy discharges oi" SMUs in 1'.2 should be associated with a fus~.d tetarms and will mainly account for the visible reflex contraction. On the other hand, the discharges of MUg in R1 can be
BLINKREFLEX:HABITUATION
( 1/secl
A
B
II
'°°"° I ° " v
C
D
Fig. 2. A - D : 4 consecutive blink reflexes of a 1 Hz stimulus series recorded with a bipc, lar needle electrode. The arrow indicates the stimulu~ onset. 1, 2 and 3 label distinct motor units.
304
regarded as the first in a series continued by repetitive firing of the same M U s i n R2, in particular, because the inu~-rval between Rt and R2is usually.no longer than 25-30 ms. Thus, whatever the biok~gical role of RI may be it clearly contributes to the reflex eyelid contraction on the stimulated side and shortens the interval between stimulu~ and reflex response. The frequency dependence of $0MU discharges in RI and R2 was tested in all suUjects by several series of 8-10 repetitive stimuli applied at a rate of I Hz. Fig. 2 shows 4 cou~ecutive BR trials of a I Hz series. The~fourth ~gttmulus (D)is no longer followed by MU discharges in IL2 as a sign of thewell known hab/tuation [7, 10], R 1, however, which is not yet evoked by the first stimulus due to subthreshold i~tensity (A), shows facilitation with comecuti,/e stimuli, as known from surface .dectrode records [ 1]. ,'~his facilitation, however, does not appear to be associated with recruitnJent of new MUs but rather with ~, ,endency of the MU discharges to .~nift from R2 to RI. ii'hus, the MUs ~1' and '2', ,'till f'Lring in R2 in Fig. 2A, occur ia Fig. 2D only in R I. These findings could be con-oborated in the records of 7 furthe:r subje~s. SLIGHT
CONTRACTION
A
i
Jl
/
B
10 msec
Io'lmV
i
Fig. 3, A and B: discharges of an MU during slight voluntary eyelid contraction in a normal subject. C: the same MU discharge; in RI and R2 of a blink reflex. The arrow indicates she stimulus .reset.
30~
Gordon [3] has already observed that some MUs of the orbicularis oculi muscle can be recruited voluntarily as well as in the corneal reflex and in .~pontaneous blinking. This t~ding can be extended to both RI and R2 of the BR. Eight subjects showed a total of 41 MUs which discharged in E2 or in both R1 and R2 of BR trials as well as during sustained voluntary contraction. Fig. 3A, B shows an MU firing rather regularly during slight voluntary eyelid contraction. The same ME also discharges in RI a n d R 2 of a BR shown in Fig. 3C. Thus, the preseptal pact of the orbictflaris oculi muscle contains MUs participating in voluntary as well as in refl6x eyelid contraction. At present, it cannot be said whether this finding can be extended to the other parts of the muscle. The result~ of this study unequivocally demonstrate that the same MUs can be recruited in RI and R2 of the BR and in voluntary eyelid contraction. The fun~:ti,~ of the MU discharges in RI, that is their biological role, could be to shorten the latency of the reflex contraction evoked by stronger stimuli. This view is supported by the observations that RI has a higher threshold than R2 and appears only on the side of the stimulus. This work was supported by Deutsche Forschungsgemeinschaft (De 227/2). We th~xtk Miss G. Troesch for techrfical assistance. 1 Boelhower, A.J.W. and Brunia, C., Effects of stimulus frequency on the blink reflex during rest and r.ask, Electroenceph. clin. N,:u,-ophysiol., 47 (1979) ,'11-716. 2 Dengler, R., Kossev, A., Gippner, Ch. and StruppleJr, A., Quantitative analysis ~,,"blink rcfl,:xes in patients with hemiplegic disorders, Electrocnceph. din. New ophysiol., 53 (1982) 393-400. 3 Gordon, G., Observations upon the movements ~f the eyelids, Brit. J. Ophthalmol., 35 (1951) ~93-351. 4 Kmmra, J., A~terations of orbicularis oculi reflex by pontine lesions Study in multiple scierosis, Arch. Neurol., 22 (1970) 156-161. 5 Kugelberg, E., Facial reflexes, Brain, 75 (1952) 385-396. 6 0 n g e r l ~ - r de Visser, B.W. and MofEe, D., Effects of brainstem and thalamic lesions on the corneal reflex, an electrophysiological and anatomical study, Brain, 102 (1979) 595-608. 7 Rushworth, G., Observations on blink retirees, J. Neurol. Neurosurg. Psychiat., 25 (1962) 93-108. 8 Sanes, J.N., Foss, J.A. and Ison, J.R., Conditions that affect the thresholds of the compon~.,~ts ~'f" the eyeblink reflex in humans, J. Neurol. Neurosurg. Psychiat., 45 (1982) 543-549. 9 Shahani, Bh., The human blink reflex, J. ~leurol. Neurosurg. Psychiat., 33 (1970) 7e2-800. 10 Struppler, A. und Dobbelstein, H., Elektromyogral~hische Untersuchung des GlabellarefieJes bei verschiedenen neurologischen St6rungen, l~ervenartz, 34 (1963) 347-352. 11 Trontelj, M. and Trontelj, J.V., First coff~ponent of human blink reflexes studied on single facial motoneurons, Brain Res., 53 (1973) 214--217.
301
Elsevier Scientific Publishers Ireland L:d.
RECRUITMENT OF SINGLE MOTOR UNITS IN THE HUMAN BLINK REFLEX
g. DENGLER* F. RECHL and A. STRUPPLER
Department o f Neurology, Technical University Miinchen, MOhlstrasse 28, D-8000 Mtinchen 80 (F. R. G./ (Received November 15th, 1982; Accepted N~vember I'P~, 1982)
Key wc+rds: single motor units - human blink reflex
The recruitment of single motor units (MU) in the early (RI) and late (R2) components of the electrically evoked human blink reflex (BR) was studied using bipolar needle electrodes with a limited take-off area. It could be shown that the same MUs c-_,ndischarge in R! and R2 of a BR as well aN during voluntary eyelid contraction. At repetitive stimulation (1 Hz), facilitation of MU discharges in R I and habituation in R2 became apparent. The visible reflex eyelid contraction may mainly be due to rel~titive MU diu:harges in R2. The dischargc:s of the same MUs in RI, however, contribute to it and shorten the latency betw~n stimwus and reflex response.
The electrically evoked blink reflex (BR) is a double component trigemino-facia~ brainstem reflex [5, 7, 9]. The early component (RI, latency 8-12 ms) is conducted through an oligosynaptic pontine reflex arc and appears unilaterally in the or bicularis oculi muscle on the stimulated side [4]. There is considerable evidence that R I is not a monosynaptic stretch reflex, as thought by the early authors [5, 7, 10], but rather an exteroceptiv¢ ~.ui.,~zJ~ous reflex [9, Ill. Its biological role, however, is still undefined. The second bilateral componen~t (R2, latency 25-40 ms) passes along polysynaptic medullary path,+ays and resembles the corneal reflex in several respects [6]. It is agreed to be a protective reflex for the eye. Little is known about the discharge pattern of single motor units (SMU, MU) in the BR. Gordon [3] has studied SMUs during various eyelid movements and found repetitive discharges i;~ spontaneous blinking and in the corneal reflex. Trontelj and Trontelj [ l l ] measured the jitter of RI using single-fibre EMG techniiques. The purpose of the present investigation was to study the recruitment of SMUs in the components of the BR. The question to b-. answered was whether the same MU's discharge in R1 and R2 z-nd in voluntary eyelid contraction. Ten normal volupteers aged from 22 to 53 years (mean 28.3 years) ~vere investigate1. The BR were elicited by electrical stimulation of the supraorbital nerve * To whom correspondence should be setAt. 0306.3940/82/0(gg)-0(K~0/$ 02.75 g,,) 1982 Elsevier Scientific Publishers Ireland Ltd.
302
using surface electrodes [2]. The stimulus ivtensity was increased stepwis¢ until the interference of SMU potentials made their identification impossible (0.5-10 mA; 0.1 ms). "[he reflex responses; were recorded etectromyographically from tile orbicularisoculi muscle of the lower eydid on the stimulated(Ic~t)side,Fme, bipolar needle electrodes with a limited tr,tke-off area were used. The needles were inserted into the preseptal part of the muscle, that is between the p.-~ritarsal and ~pitarsal part. 3MUs were identified and labelled by their characteristic action potential configuration (amplitude, duration, number of peaks). The BR activity was in most cases simultaneously recorded by means of surface electrodes [2]. Thesignals were amplified Coandpass 80-3200 Hz), displayed on a storage oscilloscope and stored on a magnetic tape. For further evaluation, they wers fed to a digital store, displayed on an oscilloscope (1024 data points) and plotted out. Several MUs, mostly 5-10, could be labelled and followed through consecutive
~ 8LINKREFLEX
!
B
lo, my
t I0.2 mV
C
10 msec 0.1mV
['ig. !. A ~nd B, blink reflex of a normal subject simultaneously recorded with a bipolar needle electrode CA) anu surface electrodes (El). C: blink reflex of another normal subject recorded with a bipolar needle ~.lectrode The arrow indicates the stimulus onset.
3~)3
BR trials in each subject. Two or lhree needle positions were investigated. A tolal c4" 78 MUs could be studied. All MUs show,~i discharges in RI and R2 of consccufive BR trials, frequently even within RI and R2 of the same BR (57 MU). Fig. I illustrates a B R recorded simultaneously with a bipolar neeale (A) and suriace electrodes 013). An MU with a characteristic potential configuration discharges in RI as well as in R2, overlapping with another MU ~n the beginrLing 3f R2. Generally, the firing threshold was lower for R2 than for P,.l. Mostly 1-3 MUs had been recruited in R2 until a:furthe: increase of the stimulu.,., i.~:ltensity evoked the first discharges in RI. Sanes et al. [8] recently elso reported a low~.i• threshold of P,2 under various experimental conditions. Repetitive discharges of SMUs were common in R2 and occurred rarely in R I. Fig. !C shows a BR with an MU firing twice in R, and 3 times in R2. The discharge frequencies, as calculated from single interpotentiaJ intervals, ranged between 100 and 150 Hz in R2 and reached peak values of about 2:~0 Hz in R1. This is in g~od agreement with the observations of Gordon [3], who fou,'d [,eak firing frequencies of about 180 Hz in spontaneous eye blinks. The high frequeeLcy discharges oi" SMUs in 1'.2 should be associated with a fus~.d tetarms and will mainly account for the visible reflex contraction. On the other hand, the discharges of MUg in R1 can be
BLINKREFLEX:HABITUATION
( 1/secl
A
B
II
'°°"° I ° " v
C
D
Fig. 2. A - D : 4 consecutive blink reflexes of a 1 Hz stimulus series recorded with a bipc, lar needle electrode. The arrow indicates the stimulu~ onset. 1, 2 and 3 label distinct motor units.
304
regarded as the first in a series continued by repetitive firing of the same M U s i n R2, in particular, because the inu~-rval between Rt and R2is usually.no longer than 25-30 ms. Thus, whatever the biok~gical role of RI may be it clearly contributes to the reflex eyelid contraction on the stimulated side and shortens the interval between stimulu~ and reflex response. The frequency dependence of $0MU discharges in RI and R2 was tested in all suUjects by several series of 8-10 repetitive stimuli applied at a rate of I Hz. Fig. 2 shows 4 cou~ecutive BR trials of a I Hz series. The~fourth ~gttmulus (D)is no longer followed by MU discharges in IL2 as a sign of thewell known hab/tuation [7, 10], R 1, however, which is not yet evoked by the first stimulus due to subthreshold i~tensity (A), shows facilitation with comecuti,/e stimuli, as known from surface .dectrode records [ 1]. ,'~his facilitation, however, does not appear to be associated with recruitnJent of new MUs but rather with ~, ,endency of the MU discharges to .~nift from R2 to RI. ii'hus, the MUs ~1' and '2', ,'till f'Lring in R2 in Fig. 2A, occur ia Fig. 2D only in R I. These findings could be con-oborated in the records of 7 furthe:r subje~s. SLIGHT
CONTRACTION
A
i
Jl
/
B
10 msec
Io'lmV
i
Fig. 3, A and B: discharges of an MU during slight voluntary eyelid contraction in a normal subject. C: the same MU discharge; in RI and R2 of a blink reflex. The arrow indicates she stimulus .reset.
30~
Gordon [3] has already observed that some MUs of the orbicularis oculi muscle can be recruited voluntarily as well as in the corneal reflex and in .~pontaneous blinking. This t~ding can be extended to both RI and R2 of the BR. Eight subjects showed a total of 41 MUs which discharged in E2 or in both R1 and R2 of BR trials as well as during sustained voluntary contraction. Fig. 3A, B shows an MU firing rather regularly during slight voluntary eyelid contraction. The same ME also discharges in RI a n d R 2 of a BR shown in Fig. 3C. Thus, the preseptal pact of the orbictflaris oculi muscle contains MUs participating in voluntary as well as in refl6x eyelid contraction. At present, it cannot be said whether this finding can be extended to the other parts of the muscle. The result~ of this study unequivocally demonstrate that the same MUs can be recruited in RI and R2 of the BR and in voluntary eyelid contraction. The fun~:ti,~ of the MU discharges in RI, that is their biological role, could be to shorten the latency of the reflex contraction evoked by stronger stimuli. This view is supported by the observations that RI has a higher threshold than R2 and appears only on the side of the stimulus. This work was supported by Deutsche Forschungsgemeinschaft (De 227/2). We th~xtk Miss G. Troesch for techrfical assistance. 1 Boelhower, A.J.W. and Brunia, C., Effects of stimulus frequency on the blink reflex during rest and r.ask, Electroenceph. clin. N,:u,-ophysiol., 47 (1979) ,'11-716. 2 Dengler, R., Kossev, A., Gippner, Ch. and StruppleJr, A., Quantitative analysis ~,,"blink rcfl,:xes in patients with hemiplegic disorders, Electrocnceph. din. New ophysiol., 53 (1982) 393-400. 3 Gordon, G., Observations upon the movements ~f the eyelids, Brit. J. Ophthalmol., 35 (1951) ~93-351. 4 Kmmra, J., A~terations of orbicularis oculi reflex by pontine lesions Study in multiple scierosis, Arch. Neurol., 22 (1970) 156-161. 5 Kugelberg, E., Facial reflexes, Brain, 75 (1952) 385-396. 6 0 n g e r l ~ - r de Visser, B.W. and MofEe, D., Effects of brainstem and thalamic lesions on the corneal reflex, an electrophysiological and anatomical study, Brain, 102 (1979) 595-608. 7 Rushworth, G., Observations on blink retirees, J. Neurol. Neurosurg. Psychiat., 25 (1962) 93-108. 8 Sanes, J.N., Foss, J.A. and Ison, J.R., Conditions that affect the thresholds of the compon~.,~ts ~'f" the eyeblink reflex in humans, J. Neurol. Neurosurg. Psychiat., 45 (1982) 543-549. 9 Shahani, Bh., The human blink reflex, J. ~leurol. Neurosurg. Psychiat., 33 (1970) 7e2-800. 10 Struppler, A. und Dobbelstein, H., Elektromyogral~hische Untersuchung des GlabellarefieJes bei verschiedenen neurologischen St6rungen, l~ervenartz, 34 (1963) 347-352. 11 Trontelj, M. and Trontelj, J.V., First coff~ponent of human blink reflexes studied on single facial motoneurons, Brain Res., 53 (1973) 214--217.