Auditory effects on the electrically elicited blink reflex in patients with Parkinson's disease

Auditory effects on the electrically elicited blink reflex in patients with Parkinson's disease

Electtoencephalography and clinical N~urophysiology."89 (1993) 1118-112 ,~;~1993 Elsevier Scientific Publishers Ireland, Ltd. 0924-9811X/93/$06.I)0 1...

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Electtoencephalography and clinical N~urophysiology."89 (1993) 1118-112 ,~;~1993 Elsevier Scientific Publishers Ireland, Ltd. 0924-9811X/93/$06.I)0

108

EEM 92087

Auditory effects on the electrically elicited blink reflex in patients with Parkinson's disease K. Nakashima, R. Shimoyama, Y. Yokoyama and K. Takahashi Division of Neurology, Institute of Neurological Sciences, Faculty Of Medicine, Tottcni Uniz'ersity, Yonago (Japan)

(Accepted for publication: 30 Decembcr 1992) Summary The effects of sound on the electrically elicited blink reflex were examined in 11 PD patients and 8 control subjects. The blink reflex was conditioned by sound stimulation which did not produce the blink response by itself. Latencies of onset, durations and amplitudes of the R1 and R2 components of the blink reflex produced by single electrical stimulation in PD patients were not different from those in control subjects. In control subjects, sound stimulation produced the facilitation of the R1 component at intervals between 50 and 100 msec. the facilitation of the R2 component at intervals between - 2 0 and 10 msec and the suppression of the R2 component at intervals between 100 and 1000 msec. In PD patients, the facilitation of the R1 and R2 components increased and the suppression of the R2 component decreased. The hyperfunction of the facilitatory interneurones and the hypofunction of the inhibitory interneurones, relating with the blink reflex, might play a role in the abnormal motor control system in the faces of PD patients. These abnormalities might be related to the disturbed function of the reticular formation and the basal ganglia.

Key words: Orbicularis oculi reflex; Sound; Reticular formation; Habituation; Motor control

The nigro-striatal system is disturbed in Parkinson's disease (PD). The reticular formation is projected from the substantia nigra and the striatum (Manetto and Lidsky 1987; Petrovick~ 1988). The disturbance of the function of the reticular system in patients with PD was reported on (Delwaide et al. 1990). The blink reflex is strongly modulated by the reticular system. In the present study, we evaluated the effects of sound on the motor control system of the parkinsonian face, using sound stimulation with the electrically elicited blink reflex. The purpose of this study is to clarify the role of the reticular formation in motor control in PD patients.

Subjects and methods Eleven PD patients (mean age 59.3 years) and 8 control subjects (mean age 56.6 years) were examined. According to Hoehn and Yahr (1967), 2 patients were rated as stage II, 7 as stage III and 2 as stage IV. All patients were receiving medication: levodopa-carbidopa, trihexyphenidyl, amantadine, bromocriptine,

Correspondence to: Dr. K. Nakashima, Division of Neurology, Institute of Neurological Sciences, Faculty of Medicine, Tottori University, 86 Nishimachi, Yonago 683 (Japan). Tel.: 8-859-34-8032; Fax: 8-859-34-8083.

etc. Before the experiments were conducted, the consent of the subjects was obtained after briefing them fully about the aim of the study and the procedures to be performed. Each subject was seated comfortably in a reclining chair. All the electromyography (EMG) recordings were made using bipolar silver/silver chloride surface electrodes. The E M G signals (bandwidth - 3 dB at 50 Hz to 3000 Hz) were amplified and recorded by a Nihon Kohden Neuropack 4. Percutaneous electrical stimuli, with a duration of 0.2 msec and an intensity of 6 times threshold, were delivered to the right supraorbital nerve with intervals of at least 20 sec. The latency, duration and amplitude of the R1 and R2 components produced by single electrical stimulation given to the supraorbital nerve were measured. The amplitude of RI was calculated peak to peak in the raw EMG. The amplitude of R2 was the mean amplitude of the rectified E M G over the time period of the R2 response. The blink reflex was conditioned by sound stimulation, which did not produce the blink response by itself. Subthreshold sound, a sound with 10 msec rise/fall time, 100 msec plateau time, 100 dB intensity and 1 kHz tone burst was used. The conditioning sound after and before the electrical test shock on the supraorbital nerve was given at various time intervals between - 5 0 and 1000 msec. The occurrence of the conditioning sound was randomized. At each time in-

SOUND EFFECTS ON BLINK RELFEX IN PD

terval, 10-20 sets of unconditioned and conditioned blink reflexes were averaged. In order to evaluate which clinical symptoms correlated with the degree of the changes of the electrically elicited blink reflex produced by sound stimulation, the degree of the Hoehn and Yahr (1967) scale, rigidity in the neck (mild and severe), general akinesia (mild, moderate and severe), tremor (no, mild and obvious) and the loss of,postural reflex (mild, moderate and severe) were evaluated and scored. The recovery curves of the R1 and R2 components were also analysed by giving paired stimuli at intervals between 10 and 1000 msec. Ten trials at each interval were given every 20-40 sec and then averaged. In order to determine the real responses produced by the test shock, the values of responses produced by a single shock were subtracted from the values produced by the combined conditioning and test shock at each stimulus interval. Unfortunately, it was not always possible to study the same range of paired intervals in all subjects. In the study of the recovery curves of the blink reflex, 7 control subjects and 7 PD patients were studied at time intervals between 10 and 100 msec; 7 control subjects and 8 PD patients at intervals between 200 and 1000 msec. The peak-to-peak amplitude of the R1 and the mean R2 amplitude of the rectified E M G were measured in the unconditioned and conditioned blink reflex. The size of the R1 and R2 amplitudes is expressed as a percentage of its control size, measured in the absence of any conditioning stimulus. The Wilcoxon rank-sum test was used for statistical analysis of the data from the blink reflex in normal subjects and patients with PD. For comparison in normal subjects, the Wilcoxon signed rank test was used at each time interval between conditioning and test shocks. Two-way analysis of variance was used for statistical analysis of the differences in recovery curves of the blink reflex conditioned by sound or electrical stimulation. One-way analysis of variance was used for the study of the relation between the change of the blink reflex and the clinical symptoms in PD patients.

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intervals between 50 and 100 msec (mean + S.E.; 50 msec: 188.13 + 30.18%, Wilcoxon signed rank test P < 0.05; and 100 msec: 179.28 + 29.24%, P < 0.01), the facilitation of the R2 component of the blink reflex at intervals between - 2 0 and 10 msec ( - 20 msec: 183.66 + 21.29%, P < 0.05; 0 msec: 182.15 + 24.41%, P < 0.01; and 10 msec: 183.66 + 21.29%, P < 0.05) and the suppression of the R2 component at intervals between 100 and 1000 msec (100 msec: 50.49 + 9.75%, P < 0.05; 200 msec: 53.45 + 8.85%, P < 0.01; 500 msec: 53.06 + 6.16%, P < 0.05; and 1000 msec: 67.13 + 5.49%, P < 0.01).

(3) The effects of sound on the blink reflex in patients with PD In PD patients, the facilitation of the R1 component at time intervals between 10 and 200 msec increased (Fig. 3: 2-way analysis of variance between 10 and 200 msec: F (1, 8 5 ) = 5.52, P < 0.05). The facilitation of the R2 component between - 2 0 and 20 msec increased (Fig. 4: 2-way analysis of variance between - 2 0 and 20 msec: F (1, 68)=4.12, P < 0.05) and the suppression of the R2 comoonent between 100 and ms 5C 4C

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(1) Blink reflex produced by single electrical stimulation Latencies of onset, durations and amplitudes of the R1 and R2 components of the blink reflex in PD patients were not different from those in control subjects (Figs. 1 and 2).

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Fig. 5. Recovery cycles for the R2 component of the blink reflex in normal subjects and PD patients. Mean data plotted _+ I S.E. Open circle, normal subjects; closed circle, PD patients.

with severe rigidity 92.85 _+ 12.73%; 1-way analysis of variance: F (2, 16) = 4.48, P < 0.05). 1000 msec (2-way analysis of variance between 100 and 1000 msec: F (1, 68) = 9.66, P < 0.01) decreased. Only rigidity in the neck significantly correlated with the degree of the suppression of the R2 component at the time interval of 500 msec between sound and electric stimulation (normal subjects 53.12 + 8.79%; PD patients with mild rigidity 67.75 + 5.55%; PD patients

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In normal subjects, the R1 component was facilitated at time intervals of 10-50 msec (10 msec: 254.1 + 69.4%, Wilcoxon signed rank test P < 0.05; 20 msec: 296.7 _+ 57.3%, P < 0.05; and 50 msec: 522.1 _+ 182.4%, P < 0.05). The fluctuation of the facilitation was strong. The statistically significant difference of the R1 component between normal subjects and PD patients was not observed (2-way analysis of variance between 10 and 100 msec: F (1, 48) = 1.68, P > 0.05). In normal subjects, the R2 component was suppressed at time intervals of 20, 50, 100, 200, 500 and 1000 msec (20 msec: 65.47 _+ 18.01%, Wilcoxon signed rank test P < 0.05; 50 msec: 41.00 + 18.01%, P < 0.05; 100 msec: 29.54 _+ 12.37%, P < 0.05; 200 msec: 17.31 ± 3.69%, P < 0.05; 500 msec: 23.11 _+ 3.49%, P < 0.05; and 1000 msec: 45.04 + 7.64%, P < 0.05). However, the facilitation of the R2 component was not observed. In PD patients, the suppression of the R2 component was significantly lower than in normal subjects (Fig. 5: 2-way analysis of variance between 200 and 1000 msec: F (1, 39) = 4.15, P < 0.05).

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Fig. 4. Effects of sound on the R2 component of the blink reflex. Mean data plotted + 1 S.E. Open circle, normal subjects; closed circle, PD patients.

In the projection from the trigeminal nerve to the facial nerve nucleus, there are 2 main interneuronal pathways: R1 and R2. In the present study, all of the latencies, durations and amplitudes of R1 and R2

SOUND EFFECTS ON BLINK RELFEX IN PD components of the electrically elicited blink reflex in patients with PD were the same as those in normal subjects. Therefore, the reflex pathway of the R1 and R2 components itself, mediating the blink reflex, may be normal in PD patients. The blink reflex may be elicited not only by electrical stimulation but also by glabellar tap (Gandhavadi 1982; Sunohara et al. 1985), air-puff to the cornea (Hiraoka and Shimamura 1978), sound (Fox 1978; Tackman and Ettlin 1982; Yamada et al. 1984; Brown et al. 1991) and photic stimulation (Tackman and Ettlin 1982; Tanaka et al. 1984). A variety of stimulation, including auditory stimulation, modulates the blink reflex (Plant and Hammond 1989). In the recovery curve of the blink reflex produced by paired electrical stimulation, the facilitation of the R1 component (Penders and Delwaide 1973; Kohara 1988) and the suppression of the R2 component (Kimura 1973; Berardelli et al. 1985; Nakashima et al. 1990a) have been reported. In the present study, preceding electrical stimulation did not produce the early facilitation of the R2 component, although sound stimulation produced it. It is not yet obvious whether the early facilitation of the R2 component is produced by preceding electrical stimulation (Hiraoka and Shimamura 1978) or not (Kohara 1988). Some kinds of preceding stimulation may produce the early facilitation of the R2 component. The facilitatory and inhibitory interneurones may be projected from the auditory nerve. It is still unclear whether electrical and auditory effects on the electrically elicited blink reflex share the same interneurones. The R2 component passes through the medullar reticular formation (Kimura 1982). The midbrain reticular formation contributes to the blink reflex produced by sound stimulation (Yamada et al. 1984). The projection from the sound stimulation which facilitates or inhibits the blink reflex may be related to the reticular formation in the brain-stem. The facilitation of the R1 component and the facilitation and the suppression of the R2 component were elicited by sound through the reticular formation. In PD patients, the early recovery of the R2 component produced by paired electrical stimulation has been reported on (Penders and Delwaide 1971; Kimura 1973; Esteban and Gim6nez-Rold~n 1975). However, the recovery curve of the R1 component may be normal (Kimura 1973). The R1 component of the test response was difficult to measure at time intervals less than 60 msec because of its overlap with the R2 component of the conditioning response (Kimura 1973). It was easy to detect the early change produced by sound stimulation in the electrically elicited R1 component, because of the lack of the direct response produced by the conditioning sound stimulation. The interneurones contributing to the facilitation of the R1 and R2 components and to the suppression of the R2 component

111 may be related to the reticular formation and may be projected from the basal ganglia. In PD patients, the disturbed function of the reticular formation and of the basal ganglia may produce the hyperfunction of the excitatory interneurone and the hypofunction of the inhibitory interneurone and then the enhanced R1 and R2 components and the suppressed R2 component may be seen. In the present study, the reduction in the suppression related to the degree of rigidity. However, the number of the PD patients studied was rather small. Therefore, further study will be necessary in order to clarify the relation between clinical symptoms in PD patients and the change produced by sound stimulation in electrically elicited blink reflex. The facilitatory effects of sound stimulation on the blink reflex exist in PD patients: hyperfunction of the facilitatory interneurone and hypofunction of the inhibitory interneurone. Besides the facilitatory effects on the blink reflex, other abnormal facilitatory changes of the motor control system may exist in PD patients. The decreased exteroceptive suppression of the jawclosing muscles (Nakashima et al. 1990b), the decreased cutaneous suppression in the hand muscle (Nakashima and Takahashi 1992) and leg muscle (Delwaide et al. 1974), the abnormal cutaneous facilitation in the leg muscle (Delwaide et al. 1974) and the decreased Ib inhibition (Delwaide et al. 1991) have been observed in PD patients. The motor control through these interneuronal systems is disturbed in PD patients, due to the abnormal function of the projection from the basal ganglia a n d / o r the reticular formation to these interneurones. Not only less suppression of the R2 component, but also the increased facilitation of the R1 and R2 components, might play a role in the abnormal motor control system in the faces of PD patients. We conclude that there may be abnormal function of the facilitatory and inhibitory interneurones, due to the abnormal function of the basal ganglia in PD patients. These interneurones may be related to the reticular system in the brain-stem. This work was supported in part by funds from the Research Committee of CNS Degenerative Disease, the Ministry of Health and Welfare of Japan and presented in part at the 2nd International Congress of MovementDisorders in Munich on June 25th, 1992.We are indebted to Miss R. Maeda and Miss S. Ito for their assistance.

References

Berardelli, A., Rothwell, J.C., Day, B.L. and Marsden, C.D. Pathophysiologyof blepharospasm and oromandibular dystonia. Brain, 1985, 108: 593-608. Brown, P., Rothwell, J.C., Thompson, P.D., Britton, T.C., Day, B.L. and Marsden, C.D. New observations on the normal auditory startle reflex in man. Brain, 1991, 114: 1891-1902.

112 Delwaide, P.J., Schwab, R.S. and Young, R.R. Polysynaptic spinal reflexes in Parkinson's disease. Neurology, 1974, 24: 820-827. Delwaide, P.J., Pepin, J.L. and Maertens de Noordhout, A. Startle reaction in parkinsonism. New evidence implying the reticular formation in pathophysiology of motor troubles. Movem. Dis., 1990, 5 (Suppl.): 23. Delwaide, P.J., Pepin, J.L. and Maertens de Noordhout, A. Shortlatency autogenic inhibition in patients with parkinsonian rigidity. Ann. Neurol., 1991, 30: 83-89. Esteban, A. and Gim6nez-Rold~n, S. Blink reflex in Huntington's chorea and Parkinson's disease. Acta Neurol. Scan&, 1975, 52: 145-157. Fox, J.E. Excitatory and inhibitory components of the eyeblink responses to startle evoking stimuli, studied in the human subject. Electroenceph. clin. Neurophysiol., 1978, 44: 490-501. Gandhavadi, B. Glabellar reflex habituation in mentally retarded adults. J. Ment. Defic. Res., 1982, 26: 271-278. Hiraoka, M. and Shimamura, M. Electro-physiological approach to the blink reflex in human. Electroenceph. Electromyogr. (Tokyo), 1978, 6: 117-126. Hoehn, M.M. and Yahr, M.D. Parkinsonism: onset, progression, and mortality. Neurology, 1967, 17: 427-442. Kimura, J. Disorder of interneurons in parkinsonism. The orbicularis oculi reflex to paired stimuli. Brain, 1973, 96: 87-96. Kimura, J. Conduction abnormalities of the facial and trigeminal nerves in polyneuropathy. Muscle Nerve, 1982, 5: S139-S144. Kohara, N. The effect of somatosensory stimulation on the orbicularis oculi reflex. Clin. Electroenceph. (Osaka), 1988, 30: 389-393. Manetto, C. and Lidsky, T.1. Influences of the basal ganglia on the medullary reticular formation. Neurosci. Lett., 1987, 75: 278-282. Nakashima, K. and Takahashi, K. Silent periods in the abductor pollicis brevis muscle in patients with Parkinson's disease. Electromyogr. Clin. Neurophysiol., 1992, 32: 215-219. Nakashima, K., Rothwell, J.C., Thompson, P.D., Day, B.L, Be-

K. NAKASHIMA ET AL. rardelli, A., Agostino, R., Artieda, J., Papas, S.M., Obeso, J.A. and Marsden, C.D. The blink reflex in patients with idiopathic torsion dystonia. Arch. Neurol., 1990a, 47: 413-416. Nakashima, K., Takahashi, K., Azumi, T. and lshida, G. Exteroceptire suppression of the masseter and temporalis muscles produced by electrical stimulation of the mental nerve in patients with Parkinson's disease. Acta Neurol. Scand., 1990b, 81: 407-410. Penders, C.A. and Delwaide, P.J. Blink reflex studies in patients with parkinsonism before and during therapy. J. Neurol. Neurosurg. Psychiat., 1971, 34: 674-678. Penders, C.A. and Detwaide, P.J. Physiologic approach to the human blink reflex. In: J.E. Desmedt (Ed.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 3. Karger, Basel, 1973: 649-657. Petroviclc~, P. Double-labelled nigral compacta and reticulata cells from injections in the reticular formation and in the striatum. An experimental study using retrograde double labelling with HRP and iron-dextran in the rat. J. Hirnforsch., 1988, 29: 243.-253. Plant, Y. and Hammond, G.R. Temporal integration of acoustic and cutaneous stimuli shown in the blink reflex. Percept. Psychophys., 1989, 45: 258-264. Sunohara. N., Tomi, H., Satoyoshi, E. and Tachibana, S. Glabella tap sign. Is it due to a lack of R2-habituation? J. Neurol. Sci., 1985, 70: 257-267. Tackman, W. and Ettlin. T. Blink reflexes elicited by electrical. acoustic and visual stimuli. I1. Their relation to visual-evoked potentials and auditory brain stem evoked potentials in the diagnosis of multiple sclerosis. Eur. Neurol., 1982, 21: 264-269. Tanaka, M., Mizuki, Y., Isozaki, H. and Inanaga, K. Consciousness level and the averaged photopalpebral reflex in normal humans. Clin. Electroenceph. (Osaka), 1984, 26: 250-256. Yamada, A., Yasuhara, A. and Yasuhara, M. Blink reflex elicited by auditory stimulatkm. Clin. Electroenceph. (Osaka), 1984, 26: 244-249.