ORIGINAL CONTRIBUTION. Sensory Modulation of the Blink Reflex in Patients With Blepharospasm. exhibit an abnormal excitability of the blink reflex
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1 ORIGINAL CONTRIBUTION Sensory Modulation of the Blink Reflex in Patients With Blepharospasm Evelia Gómez-Wong, MD; Maria J. Martí, MD; Eduardo Tolosa, MD; Josep Valls-Solé, MD Objective: To measure the effects of a prepulse stimulus on the blink reflex responses elicited by an electrical stimulation of the supraorbital nerve in patients with blepharospasm with and without an effective sensory trick. Design: Blink reflexes to supraorbital nerve stimulation were preceded in test trials by a prepulse electrical stimulus to the third finger at various leading intervals. Setting: Ambulatory patients were treated regularly with botulinum toxin in the Neurology Department of the Hospital Clinic in Barcelona, Spain. Subjects: Seventeen patients with dystonic blepharospasm and 11 age-matched control subjects. Eight of the patients with dystonic blepharospasm used a sensory trick to alleviate spasms and 9 did not. Main Outcome Measures: We measured amplitude of R1 and area of R2 responses elicited by the supraorbital electrical stimulus and determined the percentage of facilitation or inhibition induced by the prepulse. Results: Prepulse facilitation occurred in the R1 response at intervals of 6 to milliseconds and was normal in all patients. Prepulse inhibition occurred in the R2 response at intervals between 5 and milliseconds and was abnormally reduced in 11 patients (64.7%), including all 9 patients who did not use a sensory trick and 2 of the 8 patients who did use a sensory trick. There was a positive correlation between absence of sensory trick and abnormality of the prepulse effects ( 2 = 23.8; P.1). Conclusions: Prepulse inhibition of the trigeminofacial reflex is abnormal in a percentage of patients with blepharospasm, and this abnormality occurs more frequently in patients who do not use a sensory trick. This sensory derangement may contribute to the maintenance of the dystonic spasms by reducing the amount of physiological gating from peripheral nerve inputs on trigeminofacial reflexes. Arch Neurol. 1998;55: From the Electromyography Unit (Drs Gómez-Wong and Valls-Solé), and the Parkinson and Abnormal Movements Unit (Drs Martí and Tolosa), Neurology Service, Department of Medicine, IDIBAPS (Institut d Investigacions Biomèdiques August Pi i Sunyer); Hospital Clínic, Facultad de Medicina, Universitat de Barcelona, Barcelona, Spain. PATIENTS WITH dystonic blepharospasm exhibit an abnormal excitability of the blink reflex to paired electrical stimulation of the supraorbital nerve. 1-3 Such a dysfunction may result from abnormalities in the control exerted by the basal ganglia on the excitability of the brainstem interneurons of the trigeminofacial circuit. Because of the integrative function of the brainstem on sensory inputs from many nerves, it is conceivable that the abnormal control exerted by the basal ganglia also affects the sensory inputs carried by nerve afferents of the upper limbs. Some patients with dystonia exhibit a trick or geste antogonistique, which they use to transiently alleviate the spasms. 4-8 Although little is known regarding the physiological features of the sensory trick, it is likely that its effects are related to a gating mechanism by which the afferent inputs generated from the trick interfere with abnormally functioning reflex circuits. A gating mechanism is similarly implied in the physiological characteristics of the prepulse effects on the blink reflex. 9,1 Therefore, we hypothesized that patients with dystonic blepharospasm could have an abnormally reduced prepulse inhibition, and that such an abnormality could be associated with an ineffective or inexistent sensory trick. RESULTS CLINICAL ASPECTS The clinical characteristics of all patients examined are summarized in Table 1. All patients exhibited a transient improvement with botulinum toxin injections that had remitted by the time of the study. Of 8 patients who used a sensory trick, 3 rated it as very effective (patients 2, 4, and 6), and 5 rated it as poor (Table 1). This article is also available on our Web site Downloaded From: on 8/31/218
2 SUBJECTS AND METHODS SUBJECTS The study included 17 patients (15 men and 2 women; age range, years). All patients had dystonic blepharospasm, and 5 patients also had signs of dystonia in the lower face (cranialdystonia). Weexcludedpatientswhowerereceivingmedications such as dopamine antagonists or tetrabenazine. No patient was diagnosed as having schizophrenia or manic depressive psychosis, which are conditions known to induce abnormalities in the prepulse effects. 1,11 We also examined 11 healthycontrols(5menand6women; agerange, 29-75years). All subjects gave their informed consent for the study, which was approved by our Institutional Research Committee. Clinically relevant information regarding characteristics of the dystonia and especially the use of a sensory trick was gathered from the patients and their relatives. Although many forms of sensory tricks have been reported, 5,7,8 for the purpose of consistency in the evaluation of our patients, we defined a sensory trick as the selfapplication of a contact stimulus on specific sites in the face that induced a transitory relief of the dystonic spasms not in proportion to the intensity of the stimulus and not explained by the induction of a movement antagonistic to the dystonic posture or movement. 7 All patients were requested to rate their sensory tricks as very effective, poor, or absent. The severity of the dystonic features was assessed using the Scott modified scale. 12 All patients were periodically treated with botulinum toxin injections. The studies described herein were performed between 3 and 4 months after the patients dystonic spasms had resumed following transient relief from one of these treatment sessions. RECORDING AND STIMULATION Orbicularis oculi responses were recorded with a pair of surface recording electrodes placed 3 cm apart at the lower eyelid. Electrical stimulation of the supraorbital nerve was deliveredwithapairofsurfaceelectrodes, withthecathodeplaced at the supraorbital notch and the anode placed over the forehead, at an intensity that gave rise to a stable R2 response in repeated single tests. The electrical stimulus used as a prepulse was delivered with ring electrodes to the digital nerves of the third finger of the right hand at an intensity between 1.5 and 3. times the subject s sensory perception threshold. We made sure in all subjects that the prepulse stimulus was insufficient to elicit a response in the orbicularis oculi. All electromyographic recordings were made with an electromyograph (Neuropack 8, Nihon-Kohden, Tokyo, Japan) with a band pass frequency filter set at 5 to 1 Hz. PROCEDURE The subjects were instructed to lie on an examination bed in a room at moderate temperature. We randomly conducted 3 types of trials involving different stimulus combinations: the supraorbital nerve stimulus alone, the prepulse stimulus alone, and the prepulse stimulus preceding the supraorbital nerve stimulus by a variable interstimulus time interval (ISI). The ISIs used for all subjects were 4, 5, 6, 7, 8, 9, and milliseconds. For a few patients we also used ISIs of 1, 2, 3, 125, 15, 175, 3, and 4 milliseconds. All recordings were made within 5 milliseconds, in which time the prepulse stimulus was presented with a delay of milliseconds from onset of the trace. We also examined the blink reflex excitability recovery curve by applying paired (conditioning and test) stimuli to the supraorbital nerve, separated by ISIs ranging from to milliseconds in steps of milliseconds. At least 2 trials were conducted at each ISI, with a period of rest of at least 1 seconds between each trial. The intensity of the electrical stimulation of the supraorbital nerve was the same as that used in the previous experiment. DATA REDUCTION AND ANALYSIS Statistical analysis was performed separately for control subjects, patients who used a sensory trick (including those who rated the sensory trick as either very effective or poor), and patients who did not use a sensory trick. For all subjects and recordings, we measured the peak amplitude of the R1 and the area (peak amplitude duration) of the R2 response obtained during each trial. For each group of subjects, we normalized the data by assigning the value of % to the amplitude of the R1 and area of the R2 elicited by the supraorbital nerve stimuli in trials without the prepulse (control values), and represented the data obtained in trials with prepulse (test trials) as the percentage of the control values. To determine the statistical significance of the effects induced by the prepulse stimulus at each of the ISIs tested, we compared the mean percentages of R1 facilitation and R2 inhibition with the control values using repeated measures analysis of variance (ANOVA). For control subjects, we determined the 2 ISIs at which the effects induced by the prepulse stimulus were larger for R1 and R2, and used the data gathered from those ISIs for statistical comparison (1-way ANOVA) between control subjects and each group of patients. For analysis of the results for single individuals, we considered that the prepulseinduced facilitation of R1 and inhibition of R2 were normal when the percentage change was within the mean ± 2 SDs of that obtained in the group of control subjects in at least 2 ISIs between 4 and milliseconds. We used the 2 test for nonparametric analysis of the data. Using the blink reflex excitability recovery curve, we determined the percentage of recovery by dividing the area of the R2 response to the test stimulus by that of the R2 response to the conditioning stimulus at all ISIs tested. For analysis of the results for single individuals, we considered that the excitability recovery curve was abnormal when the percentage of recovery was larger than 2% at an ISI of milliseconds or 8% at an ISI of milliseconds. For a statistical comparison between groups of subjects, we determined the shortest ISI at which the percentage of recovery was at least 1%. Statistical comparison was performed with 1-way ANOVA. BLINK REFLEXES AND BLINK REFLEX EXCITABILITY RECOVERY CURVE All control subjects and patients had normal blink reflex responses to electrical stimulation of the supraorbital nerve. The mean (± SD) amplitude of R1 was ± 4.6 µv in control subjects and ± 24.2 µv in patients. The mean (± SD) area of R2 was ± µv/ms in control subjects and ± µv/ms in patients Downloaded From: on 8/31/218
3 Table 1. Clinical Characteristics of the Patients 4 35 Control Subjects A Patient No./ Age, y Type of Dystonia* Severity Duration of Disease, y Localization of Sensory Trick 1/73 BSP 4+ 5 Left eyebrow 2/57 BSP 4+ 4 Lateral border of left eye 3/6 BSP 2+ 6 Left upper eyelid 4/48 BSP 4+ 1 Left upper eyelid 5/57 BSP Right upper eyelid 6/58 BSP Tape on left eyebrow 7/58 CD 2+ 4 Both lower eyelids 8/71 CD 3+ 9 Forehead 9/82 BSP 4+ 1 None 1/76 BSP None 11/6 BSP 3+ 2 None 12/7 BSP 1+ 3 None 13/55 BSP None 14/7 BSP None 15/73 CD 2+ 9 None 16/6 CD 4+ 1 None 17/66 CD 1+ 2 None Patients With ST B *BSP indicates blepharospasm; CD, cranial dystonia (blepharospasm and orofacial dystonia). Values given according to the Scott modified scale. 12 Third Finger Only A B C Patients Without ST C Supraorbital Nerve Only µv 5 ms Figure 1. Examples of the recordings obtained from a control subject (A), a patient with no sensory trick (B), and a patient with a sensory trick (C). Traces are (from top to bottom) a stimulus applied to the third finger only (the stimulus artifact is shown with no response), a stimulus applied to the supraorbital nerve only, R1 and R2 responses, and the same stimulus preceded by the third finger stimulus at the interstimulus time interval marked in milliseconds at the left of each row. In the second to the fifth row, traces have been aligned at the artifact of the supraorbital nerve electrical stimulus (arrow). The blink reflex excitability recovery curve showed an abnormally enhanced recovery of the R2 to the test stimulus in all patients (%) who did not use a sensory trick and in 6 (75%) of the 8 patients who did. PREPULSE EFFECTS The digital nerve electrical stimulus (prepulse stimulus) induced effects on the responses elicited by the electrical stimulation of the supraorbital nerve in all control subjects and in approximately 5% of the patients. Some examples of these effects seen in selected patients are shown in Figure 1. In control subjects, the R1 was facilitated at ISIs between 6 and milliseconds, with Interstimulus Time Interval, ms Figure 2. Amplitude of the R1 response obtained at all the interstimulus time intervals tested in the prepulse experiment, expressed as percentage of the control values in control subjects (A), patients with a sensory trick (ST) (B), and patients without ST (C). Asterisks indicate significance at P.5 relative to baseline values. the peak of the effect at an ISI of 8 milliseconds (Figure 2, A). Facilitation of the R1 was also observed in both patient groups, those with and without a sensory trick, with no significant differences found in the comparison between patients of either group and control subjects (Figure 2, B and C). The R2 was significantly inhibited in control subjects at all ISIs between 5 and milliseconds, with the peak of the effect at an ISI of 9 milliseconds (Figure 3, A). The results for all patients were not uniform. Patients who used a sensory trick showed inhibition of R2 in a percentage that was not different from that observed in control subjects at any of the ISIs tested (Figure 3, B). Conversely, patients who did not use a sensory trick had significantly less inhibition than control subjects or patients who used a sensory trick at all ISIs between 5 and milliseconds (Figure 3, C) Downloaded From: on 8/31/218
4 Control Subjects Patients With ST A B Table 2. Comparison of Clinical and Electrophysiological Variables Between Patients With and Without a Sensory Trick Mean (SD) Variable No Sensory Trick Sensory Trick Age, y 68.2 (8.6) 6.2 (8.1) Severity* 2.67 (1.1) 3.13 (.8) Duration, y 8.9 (6.2) 8. (5.6) Botulinum toxin treatment, y 5.6 (3.6) 4.2 (3.1) Blink reflex recovery 233 (15) 325 (31) R1 amplitude (11.4) 227. (41.8) R2 area 16.7 (49.9) 26.8 (33.2) *Values given according to the Scott modified scale. Expressed as mean interstimulus time interval at onset of R2 recovery ( 1%) in the blink reflex excitability recovery curve. Expressed as mean amplitude percentage of the control values at the interstimulus time interval of 7 milliseconds. Expressed as mean area percentage of the control values at the interstimulus time interval of 9 milliseconds. P.5, using 1-way analysis of variance Patients Without ST Interstimulus Time Interval, ms Figure 3. Area of the R2 response obtained at all the interstimulus time intervals tested with the prepulse experiment, expressed in percentage of the control values, in control subjects (A), patients with sensory trick (ST) (B), and patients without ST (C). The bar at the bottom of C indicates the intervals in which the prepulse was significantly reduced in patients without ST compared with control subjects or patients with ST. Asterisks indicate significance at P.5 relative to baseline values. CORRELATION BETWEEN SENSORY TRICK AND PREPULSE INHIBITION There were no differences in the clinical aspects of patients who did and did not use a sensory trick (Table 2). Among the electrophysiological data, the only significant difference was found in the percentage of prepulse inhibition of the R2 response. Patients who used a sensory trick had normal prepulse inhibition, while those who did not had no inhibition. Using the criteria described in the Methods section to assess whether the prepulse effects were normal in a given individual, we found that all subjects fell within the normal range for both the R1 facilitation and the R2 inhibition. Six patients had normal prepulse inhibition, all of whom exhibited a sensory trick (patients 2, 3, 4, 5, 6, and 8) (Table 1). The 2 remaining patients who used a sensory trick (patients 1 and 7) rated their sensory trick as poor. There was a significant correlation between the presence of a sensory trick, either effective or poor, and normal prepulse inhibition ( 2 = 23.8; P.1). C COMMENT We examined the function of sensory processing mechanisms in patients with dystonic blepharospasm using the test of prepulse inhibition, or modification of the blink reflex. 9,13-17 The main findings of this study are as follows: (1) The prepulse inhibition of the R2 was abnormal in 11 (64.7%) of 17 patients with blepharospasm. (2) There was a significant correlation between abnormally reduced prepulse inhibition and absence of a sensory trick. (3) There was a weak correlation between reduced prepulse inhibition and the enhanced blink reflex excitability recovery curve, although the latter was abnormal in a larger proportion of patients. Our findings suggest that patients with dystonic blepharospasm might have abnormalities in sensorimotor gating mechanisms. It has recently been suggested that the primary cause of dystonia can be an abnormality in the central processing of sensory inputs. 18,19 It may be that the abnormal blink reflex excitability recovery curve found in patients with various forms of dystonia is one expression of the abnormal processing of trigeminal sensory inputs. A widely accepted method for testing central nervous system modulation of sensory inputs is prepulse inhibition We and others have previously shown that the prepulse effects induced in the trigeminofacial reflexes by volleys generated in the peripheral nervous system take place at the trigeminal afferents. 9,16,17 Therefore, the abnormal prepulse inhibition found in this study is consistent with a dysfunction in the sensory pathways. By applying a contact stimulus to a specific site, patients with dystonic blepharospasm are able to transiently reduce the intensity of the spasms and carry on with their tasks with less interference from the unwanted muscular activity. 5-8 In these patients, the afferent volley generated by the sensory trick may modulate the activity in the trigeminofacial circuit. Similar explanations have been given by previous authors reporting examples of the effectiveness of sensory tricks. In pa Downloaded From: on 8/31/218
5 tients with cervical dystonia, Cleeland 2 reports a reduction of the spasms with repeated electrical stimulation of the fingers, and Leis et al 21 report the beneficial effects of vibration applied to selected neck muscles. In patients with forearm dystonia, Kaji et al 19 report the effects of skin contact on vibration-induced abnormal posturing. Our finding of a significant correlation between sensory tricks and normal prepulse inhibition suggests that the beneficial effect of the sensory trick is actually related to the preservation of a functionally active physiological mechanism of prepulse inhibition. Not all patients with dystonia have the benefit of a sensory trick, and some report the loss of an effective sensory trick. This observation, together with the correlation between sensory trick and functional prepulse inhibition, suggests that abnormalities in sensorimotor gating mechanisms are the consequence rather than the cause of the dystonia. The unwanted muscle activity that is characteristic of the dystonic spasms may cause abnormal sensory volleys to reach central nervous system circuits associated with dystonia. Such an oversized input may induce an abnormal overactivity in spinal or brainstem interneurons, producing changes in neuronal metabolism. Continuous overactivity may induce segmental reorganization in neuronal connectivity, which could lead to the stabilization of abnormal reflex circuits and the loss of previous modulatory effects from sensory inputs. Reflex responses such as the blink reflex and the startle reaction are likely protective mechanisms. However, overactivity of the reflex circuits leading to such responses can have a deleterious effect. Habituation and sensory gating constitute probably the most basic strategies used by the central nervous system to limit the number of responses in a certain period. Failure of habituation and abnormality in sensory gating mechanisms can be partly responsible for the enhanced muscular activity seen in some patients with movement disorders. The mechanisms of sensory gating are likely amenable to adaptation and learning, which brings up therapeutic possibilities It might be helpful to recognize patients with dystonia and normal prepulse inhibition, who may be more likely to benefit from treatments devised to reinforce the physiological mechanisms of sensory modulation. Accepted for publication November 25, This work was supported in part by FIS grant 97/65. Reprints: Josep Valls-Solé, MD, Unitat d EMG, Neurology Service, Hospital Clínic, Villarroel 17, Barcelona 836, Spain ( valls@medicina.ub.es). REFERENCES 1. Berardelli A, Rothwell JC, Day BL, Marsden CD. Pathophysiology of blepharospasm and oromandibular dystonia. Brain. 1985;18: Tolosa E, Montserrat L, Bayés A. Blink reflex studies in focal dystonias: enhanced excitability of brainstem interneurons in cranial dystonia and spasmodic torticollis. Mov Disord. 1988;3: Pauletti G, Berardelli A, Cruccu G, Agostino R, Manfredi M. Blink reflex and the masseter inhibitory reflex in patients with dystonia. Mov Disord. 1993;8: Jankovic J, Fahn S. Dystonic disorders. In: Jankovic J, Tolosa E, eds. Parkinson s Disease and Movement Disorders. 2nd ed. Baltimore, Md: Williams & Wilkins; 1993: Weiner WJ, Nora LM. Trick movements in facial dystonia. J Clin Psychiatry. 1984; 45: Deuschl G, Heinen F, Kleedorfer B, Wagner M, Lücking CH, Poewe W. Clinical and polymyographic investigation of spasmodic torticollis. J Neurol. 1992;239: Fahn S, Marsden CD, Calne DB. Classification and investigation of dystonia. In: Marsden CD, Fahn S, eds. Movement Disorders 2. Newton, Mass: Butterworth- Heinemann; 1987: Fahn S. Blepharospasm: a form of focal dystonia. Adv Neurol. 1988;49: Rossi A, Scarpini C. Gating of trigemino-facial reflex from low threshold trigeminal and extratrigeminal cutaneous inputs in humans. J Neurol Neurosurg Psychiatry. 1992;55: Swerdlow NR, Calne SB, Braff DL, Geyer MA. The neural substrates of sensorimotor gating of the startle reflex: a review of recent findings and their implications. J Psychopharmacol. 1992;6: Geyer M, Braff D. Startle habituation and sensorimotor gating in schizophrenia and related animal models. Schizophr Bull. 1987;13: Scott AB, Kennedy RA, Stubbs HA, Musch DC. Treatment of blepharospasm with botulinum toxin. Arch Ophthalmol. 1985;92: Graham FK. The more or less startling effects of weak prestimulation. Psychophysiology. 1975;12: Hoffman HS, Ison JR. Reflex modification in the domain of startle, I: some empirical findings and their implications for how the nervous system processes sensory input. Psychol Rev. 198;87: Ison JR, Hoffman HS. Reflex modification in the domain of startle, II: the anomalous history of a robust and ubiquitous phenomenon. Psychol Bull. 1983;94: Ison JR, Sanes JN, Foss JA. Facilitation and inhibition of the human startle blink reflex by stimulus anticipation. Behav Neurosci. 199;14: Gómez-Wong E, Valls-Solé J. Effects of a prepulse stimulus on the masseteric inhibitory reflex. Neurosci Lett. 1996;28: Hallett M. Is dystonia a sensory disorder? Ann Neurol. 1995;38: Kaji R, Rothwell JC, Katayama M, et al. Tonic vibration reflex and muscle afferent block in writer s cramp. Ann Neurol. 1995;38: Cleeland CS. Behavioral technics in the modification of spasmodic torticollis. Neurology. 1973;23: Leis AA, Dimitrijevic MR, Delapasse JS, Sharkey PC. Modification of cervical dystonia by selective sensory stimulation. J Neurol Sci. 1992;11: Christensen JEJ. New treatment of spasmodic torticollis? Lancet. 1991;338: Downloaded From: on 8/31/218
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