Neurophysiol Clin (1992) 22, 321-326 © Elsevier, Paris

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Perineal m o t o r potentials to magnetic stimulation, pudendal e v o k e d potentials and perineal reflex in w o m e n A Ghezzi 1, L Callea l, M Zaffaroni~, A Zibettil, R Montanini 2 1Centro Studi Sclerosi Multipla, Universita' di Milano, Ospedale di Gallarate; 2Divisione Neurologica, Ospedale di Gallarate, via Pastori 4, 21013 Gallarate, Italy

(Received 7 October 1991; accepted 27 March 1992)

Summary - Motor potentials to transcranial and lumbar magnetic stimulation were recorded from the perineum in 14 healthy women. The response to transcranial stimulation presented an onset at 20.2 _+1.3 ms and a negative peak at 25.1 + 1.9 ms. Lumbar responses presented an onset at 5.1 +0.8 ms, and the motor central conduction time measured 14.4_+ 1.5 ms. Perineal reflex, cortical and lumbar pudendal evoked potentials were recorded after electrical stimulation of the labia minora. These tests are of possible clinical use in the evaluation of sphincter disturbances as they investigate the afferent and efferent pathways concerning pudendal nerve function. motor potential / magnetic stim.ulation / pudendal nerve / evoked potential

R~sum~ - l~tude neurophysioiogique du p6rin~e chez la femme. Nous avons enregistrd sur le p~rin~e les potentiels ~voqu~s moteurs g~n~rds par stimulation magn~tique corticale ou lombaire chez 14 femmes bien portantes. Par stimulation crfinienne on observe un d~but de r~ponse ~ 20,2 + 1,3 ms et une onde n~gative ~ 25,1 -+1,9 ms. Par stimulation lombaire, d~but de r~ponse gt 5,1 +_0,8 ms; tandis que le temps de conduction motrice centrale dtait de 14, 4 +_1, 5 ms. La latence du rdflexe p~rin6al, ainsi que les potentie& dvoqu~s corticaux et lombaires ont 6t~ enregistr6s aprbs stimulation ~leetrique des petites lbvres. Ces tests ont des applications cliniques possibles clans I'dtude des troubles sphinet~riens et clans l'examen des voies effdrentes et aff~rentes ~ destin~e p~rin~ale. potentiel moteur / stimulation magn~tique / nerf honteux / potentiel ~voqu~

Introduction

The diagnosis of bladder, bowel and sexual disturbances has made new and interesting advances since pudendal evoked potentials (PEPs) (Haldeman

e t al, 1982) a n d

p e r i n e a l r e f l e x e s ( P R s ) ( S i r o k y e t al, 1 9 7 9 ; P e d e r s e n e t al, 1 9 8 2 ; P e d e r s e n ,

1985;

V o d u s e k e t al, 1983 ; V a r n a e t al, 1986) h a v e b e c o m e r e c o r d a b l e . I n r e c e n t y e a r s t h e r e c o r d i n g o f m o t o r p o t e n t i a l s ( M P s ) f r o m p e l v i c f l o o r m u s c l e s t o t r a n s c r a n i a l elec-

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tric or m a g n e t i c s t i m u l a t i o n has p e r m i t t e d m e a s u r e m e n t o f the m o t o r c o n d u c t i o n t i m e f r o m cortex to t a r g e t muscles ( M e r t o n et al, 1982; O p s o m e r et al, 1989; DressIer et al, 1990; E r t e k i n et al, 1990; G h e z z i et al, 1991). R e s p o n s e s have been stand a r d i z e d in male subjects a n d seem to be useful in p a t h o l o g i c a l c o n d i t i o n s (Kiff a n d Swash, 1984; M a t h e r s et al, 1990). A t p r e s e n t no d a t a a r e a v a i l a b l e o n pelvic f l o o r M P s in female subjects a n d o n l y a few p a p e r s h a v e d e s c r i b e d the characteristics o f P E P s a n d P R s in w o m e n ( H a l d e m a n et al, 1982; V o d u s e k , 1990). F o r this r e a s o n we have r e c o r d e d these responses in a series o f f e m a l e subjects to verify the a p p l i c a b i l i t y o f these tests a n d to assess their n o r m a t i v e d a t a .

Subjects and methods Fourteen consenting healthy women took part in the study. The mean age was 38.9 years (range 21-63 years), the mean height was 162.9 cm (range 158-169 cm). The subjects were free from neurological, urinary and bowel disorders. MPs were recorded with a protocol similar to that used for male subjects (Ghezzi et al, 1991). Briefly, magnetic stimulation was delivered by a Novametrix Magstim 200 device positioning the coil tangentially at the vertex, or slightly anterior to it, to obtain cortical motor potentials (C-MPs) and over the L1 spinous process to obtain lumbar motor potentials (L-MPs). Intensity was 10% over the motor threshold, generally 90-100°70, the maximum output of the device for C-MPs and 7 0 - 8 0 % , the maximum output for L-MPs. A slight contraction of pelvic floor muscles was requested to obtain larger C-MPs; L-MPs were recorded in relaxed muscles. Responses were recorded by a surface Ag/AgC1 electrode on the perineum, anterior to the anus, referenced to S1. At least eight single responses were recorded and superimposed. PEPs were recorded from the scalp by Cz (2 cm behind Cz) and Fz electrodes and from the lumbar spine by L 1 - L 5 electrodes, with bandpass of 1-2000 Hz. At least 500 electrical stimuli were delivered at a frequency of 4 Hz by clip electrodes attached to the labia minora. The intensity was slightly increased over the sensitivity threshold and just beneath the pain threshold, generally 2 . 5 - 3 times over the threshold. Two or more traces were obtained and superimposed. The PR was recorded by the same surface electrodes used for MP recording, stimulating as for PEP recording. The term 'PR' was preferred to the term 'bulbocavernosus reflex' (BCR) used in men, the recording electrode being applied on the perineum. For other technical details concerning the recording of PEP and PR, see Ghezzi et al (1991).

Results M o t o r potentials M P s to t r a n s c r a n i a l m a g n e t i c s t i m u l a t i o n c o u l d be r e c o r d e d in all subjects o f o u r series: a high s t i m u l a t i o n intensity, up to 90-100°70, the m a x i m u m o u t p u t o f the device, a n d a slight c o n t r a c t i o n o f pelvic f l o o r muscles were necessary to o b t a i n consistent responses. S o m e e x a m p l e s o f C - M P s are r e p o r t e d in figure 1. T h e onset o f

Perineal motor potentials in women

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Fig 1. Examples of motor potentials from perineum following transcranial magnetic stimulation in four female subjects. O = onset, P = peak.

the response presented a latency of 20.2_ 1.3 ms (range 17.7-21.7), followed by a negative peak at 25.1 + 1.9 ms (range 22.5-28.6). The amplitude from the onset to the negative peak was 221 + 154 ffV (range 110-520). L-MPs were obtained with a lower intensity, the maximum output usually being 7 0 - 8 0 % ; onset could be easily detected in all cases in spite of the stimulus artifact : its latency measured 5.1 _+0.8 ms (range 4-5.8). The central motor conduction time (CCT = C - M P s - L - M P s ) measured 14.4+ 1.5 ms (range 13.0-16.5).

Pudendal evoked potentials Cortical PEPs presented the W configuration shown in figure 2 (upper traces), similar to male PEPs and to somatosensory evoked potential of lower limbs. The onset was labelled No and measured 30.9 +_2.4 ms (range 27.7-36), followed by a positive peak (P1) at 38.7_+3.0 ms (range 35.2-44.7). The No-P1 amplitude measured 0.6 _+0.5 ffV (range 0.2-2.3). Responses could not by picked up by lumbar electrodes because of their low amplitude.

Perineal reflex The PR was characterized by a large negative peak, as shown in figure 2 (lower traces). Onset and peak latencies were respectively 47.3 +4.2 ms (range 46.7-52.4) and 60.9_+ 4.0 ms (range 58.6-66.2); the amplitude was 25.4 _+ 14.8 ffV (range 5.2-46). The latency and amplitude of C-MPs, PEPs and PR are summarized in table I.

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Fig 2. (A) Pudendal evoked potentials (three traces are superimposed, No and P1 waves are indicated); (B) perineal reflexes (three traces are superimposed) of a single subject. O = onset, P = peak. Calibration: 10 ms, 0.2/zV for pudendal evoked potentials, 16 #V for perineal reflexes.

Discussion

MPs to transcranial and lumbar magnetic stimulation could be recorded in all subjects of our series, making it possible to measure the m o t o r conduction time f r o m cortex and spinal roots respectively to perineum. The m o t o r C C T was obtained by difference, and measured 14.4 +_ 1.5 ms. As in male subjects, high intensity stimuli were necessary to record well defined C-MPs, probably because m o t o r neurons are localized deep in the interhemispheric fissure (Opsomer et al, 1989). The M P characteristics of females were comparable with those of males : the latency of the C-MPs and of the C C T was slightly lower in females than in males (respectively 20.2_+ 1.3

Table 1. Normative data of the tests. Mean

SD

Cortical MP

Onset latency 20.2 Peak latency 25.1 Amplitude 221.0

Mean

SD

PEP

1.3 1.9 154.0

Latency in ms, amplitude in t~V.

No latency P1 latency Amplitude

Mean

SD

PR

30.9 38.7 0.6

2.4 3'.0 0.5

Onset latency Peak latency Amplitude

47.3 60..9 25.4

4.2 4.0 14.8

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and 14.4 + 1.5 ms instead of 22.9 + 1.8 and 17.0 + 2.5 ms (Ghezzi et al, 1991)) probably because of the reduced body height (162.9 instead of 169.2 cm). PEPs were recorded via the scalp in all subjects whereas lumbar responses could not be recognized because of their small amplitude. The latency of cortical PEPs was similar to that reported by Haldeman et al (1982) and by Vodusek (1990). Their configuration was similar to that in males but the latency was slightly lower, probably because of the smaller body height, as seen above. The amplitude was also lower, depending on several causes : the different application of stimulating electrodes, the different intensity used, the different innervation of g e ~ a l s (Hatdeman et al, 1982). In our female subjects the PR latency was considerably higher than the latency of the BCR recorded in males with a similar technique ( 4 7 . 3 + 4 . 2 instead of 34.5 _+3.3 ms). It could be due to the fact that in females the surface electrode records the m o t o r activity of the external anal sphincter beyond the bulbocavernosus muscle. Afferent fibers of the pudendo-anal reflex are A delta type, whereas those involved in the bulbocavernosus reflex are A beta type (Vodusek, 1983). However, it has been demonstrated that the two reflexes have quite similar latencies (Varma et al, 1986). Another explanation could be the different and lower stimulation intensity; however, the same intensity was used to record PEPs and their latency was not more prolonged in women than in men. Using a needle concentric electrode in the bulbocavernosus or in the external sphincter muscles, four successive components can be recorded after stimulation o f different sites such as glans penis, clitoris, the mucosa of the rectum, urethra, bladder, and skin of the legs (Pedersen et al, 1982; Swash, 1982; Vodusek et al, 1983; Pedersen, 1985; Varna et al, 1986). An early c o m p o n e n t appears at 5 - 8 ms and is ascribed to the antidromic volley in the efferent nerve travelling to a point of branching then travelling anterogradely in the collateral division of the pudendal nerve. A second component at about 13-18 ms could be a spinal reflex. A third component is then recorded at 3 0 - 4 5 ms and represents a polysynaptic reflex as well as the fourth component of about 55 ms. It could be argued that the reflex response we recorded in our series represents the fourth c o m p o n e n t of the reflex, the third being masked in females for unknown reasons : in the present study we did not think it proper to use a needle electrode in our healthy volunteers. Apart f r o m these considerations, the P R latency, if recorded by a surface electrode, can merely give an indirect and unreliable measure o f the afferent and efferant branches of pudendal nerve being a polysynaptic reflex, as well as the BCR. Unfortunately l,umbar P E P s could not be recorded in women because of their small amplitude: so the evaluation of the afferent pathway following pudendal nerve stimulation is only based on cortical responses. Conversely, the motor pathways from cortex to pelvic floor muscles can be well evaluated in the two following components : f r o m ~oTt,ex to muscles a n d f r o m spinal roots (Ugawa et al, 1989) to muscles. Promising data also seem to derive from the recording of MPs in the external anal muscle and in the external urethral sphincter in m a n (Thiry and Deltenre, 1989; Ertekin et al, 1990).

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Conclusion In c o n c l u s i o n , o u r s t u d y d e m o n s t r a t e s t h a t C - M P s , L - M P s a n d P E P s a r e well tolera t e d a n d c a n be r e l i a b l y r e c o r d e d in female subjects. I f o u r results are c o n f i r m e d , these tests will be o f potential clinical usefulness in neurological diseases a n d in p a t h o logical c o n d i t i o n s involving sexual a n d sphincter d i s t u r b a n c e s .

References Dressier D, Schonle PW, Neubauer H (1990) Central motor conduction time to bulbocavernosus muscle : evaluation by magnetic brain stimulation and testing of bulbocavernosus reflex. J Neurol 237, 239-240 Ertekin C, Hansen MV, Larsson LE, Sjodahl R (1990) Examination of the descending pathway to the external anal sphincter and pelvic floor muscles by transcranial cortical stimulation. Electroencephalogr Clin Neurophysio175, 500-5 l0 Ghezzi A, Callea L, Zaffaroni M, Montanini R, Tessera G (1991) Motor potentials of bulbocavernosus muscle after transcranial and lumbar magnetic stimulation : comparative study with bulbocavernosus reflex and pudendal evoked potentials. J Neurol Neurosurg Psychiatry 54, 524-526 Haldeman S, Bradley WE, Bhatia NN, Mazeuder N, Johnson BK (1982) Pudendal evoked responses. Arch Neuro139, 280-283 Kiff ES, Swash M (1984) Normal proximal and delayed distal conduction in the pudendal nerves of patients with idiopathic (neurogenic) faecal incontinence. J Neurol Neurosurg Psychiatry 47, 820-823 Mathers SE, Ingram DA, Swash M (1990) Electrophysiology of motor pathways for sphincter control in multiple sclerosis. J Neurol Neurosurg Psychiatry 53,955-960 Merton PA, Morton HB, Hill DK, Marsden CO (1982) Scope of a technique for electrical stimulation of human brain, spinal cord and muscle. Lancet ii, 597-600 Opsomer R J, Caramia MD, Zarola F, Pesce

F, Rossini PM (1989) Neurophysiological evaluation of central-peripheral sensory and motor pudendal fibres. Electroencephalogr Clin Neurophysio174, 260-270 Pedersen E, Klemar B, Schroder H D A A T~rring J (1982) Anal sphincter responses after perianal electrical stimulation. J Neurol Neurosurg Psychiatry 45,770-773 Pedersen E (1985) The anal reflex. In: Coloproctology and the Pelvic Floor Pathophysiology and Management (Henry MM, Swash M, eds) Butterworths, London, 104-111 Siroky MB, Sax DS, Krane RJ (1979) Sacral signal tracing: the electrophysiology of the bulbocavernosus reflex. J Uro1122, 661-664 Swash M (1982) Early and late components in the human anal reflex. J Neurol Neurosurg Psychiatry 45, 767-769 Thiry A J, Deltenre PF (1989) Neurophysiological assessment of the central motor pathway to the external uretheral sphincter in man. Br J Urol 63, 515-519 Ugawa.Y, Rothwell JC, Day BL, Thompson PD, Marsden CD (1989) Magnetic stimulation over the spinal enlargments. J Neurol Neurosurg Psychiatry 52, 1025-1032 Varma JS, Smith AN, McInnes A (1986) Electrophysiological observations on the human pudendo-anal reflex. J Neurol Neurosurg Psychiatry 49, 1411-1416 Vodusek DB, Janko M, Lokar J (1983) Direct and reflex responses in perineal muscles on electrical stimulation. J Neurol Neurosurg Psychiatry 46, 67-71 Vodusek DB (1990) Pudendal SEP and bulbocavernosus reflex in women, glectroencephalogr Clin Neurophysio177, 134-136