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Effects of a prepulse stimulus on the masseteric inhibitory reflex in humans
N[UIIltiC[ ELSEVIER
NeuroscienceLetters208(1996)183-186
UTIIH8
Effects of a prepulse stimulus on the masseteric inhibitory reflex in humans E. G6mez-Wong, J. Vails-Sol6* Unitat d'EMG, Servei de Neurologia, Hospital Clinic, ~llarroel, 170, Barcelona, 08036, Spain Received 21 February 1996; revised version received 20 March 1996; accepted 22 March 1996
Abstract
We investigated the effects of a weak cutaneous stimulus applied to the digital nerves (prepulse) on the masseter inhibitory reflex (MIR) to electrical stimulation of the mental nerve in nine healthy volunteers. The prepulse stimulus, which had no direct effect on the masseter muscle EMG ac.tivity, induced a significant decrement in the area of the second phase of the MIR at interstimulus intervals between 50 and 100 ms. '/'he percentage reduction induced on the inhibitory phase of the MIR was not different from that induced by the same prepulse on the late excitatory phase (R2) of the orbicularis oculi muscle to supraorbital nerve electrical stimulation during voluntary contraction. The effects observed during contraction were significantly less marked than those observed in the blink reflex at rest. We conclude that prepulse inhibition occurs in various brainstem reflexes, is similarly active on excitatory and inhibitory responses, and is reduced during voluntary activation.
Keywords: Prepulse inhibition; Brainstem reflexes; Masseteric inhibitory reflex; Blink reflex; Sensorimotor gating; Startle
Prepulse inhibition is known as the inhibitory effect induced on a response to a strong stimulus by a preceding stimulus of subthreshold intensity [5,6,8]. To assess the effects of prepulse in the domain of the startle, the reaction of the whole body is measured in rats and other species [4,9], while the response of the orbicularis oculi reflex is measured in humans [4,6,8]. Prepulse inhibition is considered a protective mechanism for avoidance of the disrupting effects of a startling stimulus. We have hypothesized that prepulse not only inhibits the startle reaction but is effective also on responses of brainstem reflexes not considered a part of the startle reaction. In this study we have investigated the prepulse effects on the masseteric inhibitory reflex (MIR). The study was carried out in nine healthy volunteers, five men and four women, aged 19-45 years, who gave their informed consent for the study. Recording EMG electrodes were attached to the skin overlying the belly of the masseter muscle, with reference to the earlobe. Electrical stimuli for elicitation of the MIR were delivered through cutaneous electrodes attached over the mental nerve at the lateral aspect of the chin. Stimulus intensity was set at 5--6 times the sensory perception threshold, * Corresponding author. Tel.: +34 3 2275413; fax: +34 3 2275454.
which was sufficient for eliciting a stable suppression of the ongoing EMG activity during voluntary contraction in all subjects. Electrical prepulse stimuli were applied to the digital nerves of the 3rd finger with ring electrodes. Stimulus intensity was set at 1-1.5 times the subject's sensory perception threshold, and we made sure that no effect was induced by such stimulus on the EMG activity of the masseter muscle. For comparison, we also examined the effects induced by the same digital nerve electrical stimulus on the blink reflex responses (BR) obtained by electrical stimulation of the supraorbital nerve at rest and during a sustained voluntary contraction of the orbicularis oculi. The EMG activity was recorded with an electromyograph Neuropack 8 (Nihon-Khoden) with a band pass frequency filter set at 50-10 000 Hz. The prepulse stimulus was applied at 100 ms from onset of the sweep and the mental nerve stimulus was presented with an interstimulus interval (ISI) of 0, 10, 20, 30, 40, 50, 60, 70, 80, 90, 100, 200, or 300. The EMG activity was full-wave rectified and ten successive epochs of 500 ms were averaged time-locked to the electrical stimulus. Rate of electrical stimulation was 0.1 Hz. For every ISI, we obtained first the responses to electrical stimulation of the mental nerve alone, and then those to the same stimulus preceded by
0304-3940/96/$12.00 © 1996 Elsevier Science Ireland Ltd. All rights reserved PII: S 0 3 0 4 - 3 9 4 0 ( 9 6 ) 1 2 5 7 4 - 8
184
E. G6mez- Wong, J. Valls-Sol~ / Neuroscience Letters 208 (1996) 183-186
A
C
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40
. --J
100
._AL__. ~"
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ms, Digital
S
S
S
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[so 5 0 ms
200
200'
2oo]
-e 150
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.
.
.
.
I0 30 50 70 90 200
,
,
,
,
,
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,
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I0 30 50 70 90 200
Interstimulus interval (ms)
###
0
,
,
,
,
i ii ,
,
i
,
,
,
-r
10 30 50 70 90 200
###
Fig. 1. The blink reflex to supraorbital nerve stimulation, with the orbicularis oculi at rest (A) and during a sustained voluntary contraction (B), and the MIR to mental nerve stimulation (C). Traces are the result of averaging ten rectified responses to the electrical stimulus of the corresponding nerve (arrow), when applied alone (control) and when preceded by a digital nerve electrical stimulus at the 1SI marked at the left side of each trace. Scattergrams show the mean and one SD of the area of the responses obtained at all ISis examined, expressed as a percentage of control values. *ISis in which the mean area of the response is significantly smaller (P < 0.01) than that of the responses obtained in control trials. #ISis in which the mean area of the R2 response obtained in test trials is significantly different (P < 0.05) during contraction with respect to rest.
the digital nerve electrical stimulus. We followed the same procedure for the BR to supraorbital nerve electrical stimulation at rest and during contraction of the orbicularis oculi. The area of the responses was measured by multiplying amplitude by duration. In the inhibitory and excitatory responses obtained during contraction, the amplitude was measured as the depth or the height, respectively, of the peak of the response taken from arbitrary lines drawn at 80% and 120% of the mean level of background EMG activity in the 100 ms preceding the first electrical stimulus. Normalization of the data was accomplished by assigning the value of 100% to the area of the MIR elicited by the mental nerve stimulus alone, or to the area of the BR elicited by supraorbital nerve stimulus alone, and expressing the area of the response obtained when the same stimulus was preceded by the digital nerve stimulus as a percentage.
At every ISI, we compared the area of the response to combined digital nerve and mental nerve stimuli with that of the response to mental nerve stimulus alone, and those to digital nerve and supraorbital nerve stimuli with that of the responses to supraorbital nerve stimulus alone. We also compared for every ISI the effects induced on the MIR with those induced on the BR, as well as the effects observed in the BR at rest with those observed during contraction. All statistical comparisons were performed by repeated analysis of variance (ANOVA). The MIR to mental nerve stimuli alone had two distinct phases in all subjects (MIR1 and MIR2). Latency of MIR1 was 17.1 ms (SD= 2.1) and area was 2141 a.u. ( S D = 2 1 3 a.u). Latency of MIR2 was 51.8ms (SD= 5.8 ms), and area was 3310 a.u. (SD = 346 a.u.). The prepulse stimulus caused no effect on MIR1, but induced a reduction of the area of the MIR2 which decreased to 3040% of the control values at ISis between 60 and 100 ms
E. Gdmez-Wong, J. Valls-Sol~/ Neuroscience Letters 208 (1996) 183-186
(Fig. 1). The BR at rest had two responses. The mean latency of R1 was 10.8 ms (SD = 1.1 ms), and the mean amplitude was 530/~V (SD = 106/~V). The mean latency of R2 was 37.6 ms (SD = 5.4 ms), and the mean area was 5640 a.u. (SD = 650 a.u.). The preceding digital nerve stimulus caused facilitation of R1 at ISis between 50 and 70 ms, and inhibition of R2 at ISis between 50 and 200 ms. During contraction of the orbicularis oculi, supraorbital nerve stimulation induced two excitatory phases at a latency corresponding with that of the R1 and R2 responses elicited at rest. The preceding digital nerve had no effect on the excitatory phase corresponding to R1, but reduced significantly the phase corresponding to R2 at ISis of 50-100 ms. The percentage reduction induced by the prepulse on the inhibitory MIR2 was not different from that induced on the excitatory R2 during contraction of the orbicularis oculi at any ISI (P values between 0.13 and 0.68). However, the effects of the prepulse on MIR2 and on R2 during contraction were significantly smaller than those induced on R2 at rest at the ISis of 7 0 m s ( P = 0.04), 8 0 m s ( P = 0.01), and 90 ms (P = 0.02). The most relevant findings of the present study are that there is a common effect of a weak prepulse stimulus on various brainstem reflexes, that the effects are similar on excitatory and inhibitory responses, and that they are reduced during voluntary activation with respect to rest. There is not much research done in humans regarding the collision of activity in different neural circuits. This is in contrast with the fact that the central nervous system is normally exposed to the simultaneous arrival of many sensory inputs of different modalities with any human activity. Sensorimotor inhibition or 'gating' is probably one of the most basic strategies used by the central nervous system for select:ion of useful information from the constant environmental bombardment of inputs [6,8]. Prepulse inhibition may be the neurophysiological expression of a gating mechanism on processing of reflex responses [17]. Studies done in animals suggest that prepulse inhibition is a feature of the brainstem [10,15,17]. The exact location of the effect, however, is unknown. Animal experiments suggested lhat prepulse inhibition is mediated by a complex neural circuitry involving several structures such as the frontal cortex, the nucleus accumbens, the palidum, the pontine nuclei, and the superior colliculus, but neither the exact structure nor the neurotransmitter in charge of the prepulse effect have been identified so far [9,17]. From our study it appears that a weak prepulse has a multi-level effect, inducing inhibition on several brainstem reflex responses. It is possible that prepulse inhibition uses a brainstem circuit processing sensory inputs from many modalities. Rimpel et al. [13] hypothesized the existence of a common polysensory system integrating the activity from visual, acoustic and trigeminal inputs before reaching the facial nerve. Afferent inputs
185
from nerves of the limbs can be added to such a common brainstem polysensory system since the finding of their modulatory influences on trigemino-facial reflexes [2,14, 18]. The present study shows that trigemino-trigeminal inhibitory reflexes should be included as one of the targets expressing brainstem sensorimotor gating phenomena. Similar findings have been reported by other authors using thermic [3] and electrical stimuli producing tactile or painful sensations [16]. The observation in our work of the occurrence of the same effect on trigemino-trigeminal (MIR2) and trigemino-facial (BR) reflexes indicates that prepulse effects occur at the trigeminal nerve afferents themselves, before synapsing with facial or trigeminal motoneurons. This is in keeping with reports from experiments performed in animals [1]. The prepulse effects induced in the blink reflex were markedly reduced during voluntary contraction with respect to rest. Facilitation of R1 disappeared and inhibition of R2 diminished significantly. Activity in the corticonuclear tract may conceal both the excitatory and the inhibitory effects of a prepulse by modifying the excitability of the brainstem interneurons mediating such effects. Once the presence of voluntary contraction was taken into account, the effects of a digital prepulse were the same for the excitatory responses of the BR and the inhibitory responses of the MIR. This indicates that the prepulse effects are exerted on excitatory and inhibitory interneurons of the brainstem with no specificity. R1 was facilitated at rest, a finding that has been observed many times before and has been interpreted as the result of an enhanced preparatory state while processing sensory information [8]. The differential effects between R1 and R2, and those between MIR1 and MIR2, could be related to the different amount of interneurons in the chain of early and late responses, or to the fact that these responses follow a different circuit in the brainstem [11, 12]. Brainstem excitatory and inhibitory reflexes are routinely used in the neurophysiological assessment of patients with neurological diseases [7]. Studying the prepulse effects of peripheral nerve afferents on the blink reflex and on the masseteric inhibitory reflex offers new possibilities for the assessment of brainstem reflex functions in humans. [1] Baldissera, E, Broggi, G. and Mancia, M., Depolarization of trigeminal afferents induced by stimulation of brainstem and peripheral nerves, Exp. Brain Res., 4 (1967) 1-17. [2] Boulu, Ph., Willer, J.V. and Cambier, J., Analyse electrophysiologique du reflexe de clignement chez l'homme: interactions des affrrences sensitives segmentaires et intersegmentaires, des affrrences auditives et visuelles, Rev. Neurol., 137 (1981) 523533. [3] Cadden, S.W. and Newton, J.E, The effects of inhibitory controls triggered by heterotopic noxious stimuli on a jaw reflex evoked by perioral stimuli in man, Arch. Oral Biol., 39 (1994) 473--480. [4] Geyer, M.A., Swerdlow, N.R., Mansbach, R.S. and Braff, D.L., Startle response models of sensorimotor gating and habituation deficits in schizophrenia, Brain Res. Bull., 25 (1990) 485-498.
186
E. G6mez- Wong, J. Valls-Solg / Neuroscience Letters 208 (1996) 183-186
[5] Graham, EK., The more or less startling effects of weak prestimulation, Psychophysiology, 12 (1975) 238-248. [6] Hoffman, H.S. and Ison, J.R., Reflex modification in the domain of startle, 1: some empirical findings and their implications for how the nervous system processes sensory input, Psychol. Rev., 87 (1980) 175-189. [7] Hopf, H.C., Topodiagnostic value of brain stem reflexes, Muscle Nerve, 17 (1994) 475--484. [8] Ison, J.R, Sanes, J.N., Foss, J.A. and Pinckney, L.A., Facilitation and inhibition of the human startle blink reflex by stimulus anticipation, Behav. Neurosci., 104 (1990) 418-429. [9] Koch, M. and Friauf, E., Glycine receptors in the caudal pontine reticular formation: are they important for the inhibition of the acoustic startle response? Brain Res., 671 (1995) 63-72. [10] Koch, M., Kungel, M. and Herbert, H., Cholinergic neurons in the pedunculopontine tegmental nucleus are involved in the mediation of prepulse inhibition of the acoustic startle response in the rat, Brain Res., 97 (1993) 71-82. [11] Ongerboer de Visser, B.W. and Goor, C., Cutaneus silent periods in masseter muscles: electrophysiological and anatomical data, J. Neurol. Neurosurg. Psychiatry, 39 (1976) 674-679. [12] Ongerboer de Visser, B.W. and Kuypers, G.J.M., Late blink reflex changes in lateral medullary lesions: an electrophysiological and
[13]
[14]
[15]
[16]
[17]
[18]
neuro-anatomical study of Wallenberg's syndrome, Brain, 101 (1978) 285-294. Rimpel, J., Geyer, D. and Hopf, H.C,, Changes in the blink responses to combined trigeminal, acoustic and visual repetitive stimulation, studied in the human subject, Electroencephalogr. Clin. Neurophysiol., 54 (1982) 552-560. Rossi, A. and Scarpini, C., Gating of trigemino-facial reflex from low-threshold trigeminal and extratrigeminal cutaneus in humans, J. Neurol. Neurosurg. Psychiatry, 55 (1992) 774-780. Saitoh, K., Tilson, H.A., Shaw, S. and Dyer, R.S., Possible role of the brainstem in the mediation of prepulse inhibition in the rat, Neurosci. Lett., 75 (1987) 216-222. Shoenen, J., Wang, W. and Gerard, P., Modulation of temporalis muscle exteroceptive suppression by limb stimuli in normal man, Brain Res., 657 (1994) 214-220. Swerdlow, N.R., Caine, S.B., Braff, D.L. and Geyer, M.A., Neural substrates of sensori-motor gating of the startle reflex: a review of recent findings and their implications, J. Psychopharmacol., 6 (1991) 176-190. Vails-SolE, J., Cammarota, A., Alvarez, R. and Hallett, M., Orbicularis oculi responses to stimulation of nerve afferents from upper and lower limbs in normal humans, Brain Res., 650 (1994) 313-316.
NeuroscienceLetters208(1996)183-186
UTIIH8
Effects of a prepulse stimulus on the masseteric inhibitory reflex in humans E. G6mez-Wong, J. Vails-Sol6* Unitat d'EMG, Servei de Neurologia, Hospital Clinic, ~llarroel, 170, Barcelona, 08036, Spain Received 21 February 1996; revised version received 20 March 1996; accepted 22 March 1996
Abstract
We investigated the effects of a weak cutaneous stimulus applied to the digital nerves (prepulse) on the masseter inhibitory reflex (MIR) to electrical stimulation of the mental nerve in nine healthy volunteers. The prepulse stimulus, which had no direct effect on the masseter muscle EMG ac.tivity, induced a significant decrement in the area of the second phase of the MIR at interstimulus intervals between 50 and 100 ms. '/'he percentage reduction induced on the inhibitory phase of the MIR was not different from that induced by the same prepulse on the late excitatory phase (R2) of the orbicularis oculi muscle to supraorbital nerve electrical stimulation during voluntary contraction. The effects observed during contraction were significantly less marked than those observed in the blink reflex at rest. We conclude that prepulse inhibition occurs in various brainstem reflexes, is similarly active on excitatory and inhibitory responses, and is reduced during voluntary activation.
Keywords: Prepulse inhibition; Brainstem reflexes; Masseteric inhibitory reflex; Blink reflex; Sensorimotor gating; Startle
Prepulse inhibition is known as the inhibitory effect induced on a response to a strong stimulus by a preceding stimulus of subthreshold intensity [5,6,8]. To assess the effects of prepulse in the domain of the startle, the reaction of the whole body is measured in rats and other species [4,9], while the response of the orbicularis oculi reflex is measured in humans [4,6,8]. Prepulse inhibition is considered a protective mechanism for avoidance of the disrupting effects of a startling stimulus. We have hypothesized that prepulse not only inhibits the startle reaction but is effective also on responses of brainstem reflexes not considered a part of the startle reaction. In this study we have investigated the prepulse effects on the masseteric inhibitory reflex (MIR). The study was carried out in nine healthy volunteers, five men and four women, aged 19-45 years, who gave their informed consent for the study. Recording EMG electrodes were attached to the skin overlying the belly of the masseter muscle, with reference to the earlobe. Electrical stimuli for elicitation of the MIR were delivered through cutaneous electrodes attached over the mental nerve at the lateral aspect of the chin. Stimulus intensity was set at 5--6 times the sensory perception threshold, * Corresponding author. Tel.: +34 3 2275413; fax: +34 3 2275454.
which was sufficient for eliciting a stable suppression of the ongoing EMG activity during voluntary contraction in all subjects. Electrical prepulse stimuli were applied to the digital nerves of the 3rd finger with ring electrodes. Stimulus intensity was set at 1-1.5 times the subject's sensory perception threshold, and we made sure that no effect was induced by such stimulus on the EMG activity of the masseter muscle. For comparison, we also examined the effects induced by the same digital nerve electrical stimulus on the blink reflex responses (BR) obtained by electrical stimulation of the supraorbital nerve at rest and during a sustained voluntary contraction of the orbicularis oculi. The EMG activity was recorded with an electromyograph Neuropack 8 (Nihon-Khoden) with a band pass frequency filter set at 50-10 000 Hz. The prepulse stimulus was applied at 100 ms from onset of the sweep and the mental nerve stimulus was presented with an interstimulus interval (ISI) of 0, 10, 20, 30, 40, 50, 60, 70, 80, 90, 100, 200, or 300. The EMG activity was full-wave rectified and ten successive epochs of 500 ms were averaged time-locked to the electrical stimulus. Rate of electrical stimulation was 0.1 Hz. For every ISI, we obtained first the responses to electrical stimulation of the mental nerve alone, and then those to the same stimulus preceded by
0304-3940/96/$12.00 © 1996 Elsevier Science Ireland Ltd. All rights reserved PII: S 0 3 0 4 - 3 9 4 0 ( 9 6 ) 1 2 5 7 4 - 8
184
E. G6mez- Wong, J. Valls-Sol~ / Neuroscience Letters 208 (1996) 183-186
A
C
contro,
:V.
40
. --J
100
._AL__. ~"
~ ' ~ ' ~ - " -
ms, Digital
S
S
S
nerve stimulus
[so 5 0 ms
200
200'
2oo]
-e 150
1SO'
150~
. ,
lOOi so:
50' .........................
.
.
.
.
I0 30 50 70 90 200
,
,
,
,
,
,
,
,
i
i
"r
I0 30 50 70 90 200
Interstimulus interval (ms)
###
0
,
,
,
,
i ii ,
,
i
,
,
,
-r
10 30 50 70 90 200
###
Fig. 1. The blink reflex to supraorbital nerve stimulation, with the orbicularis oculi at rest (A) and during a sustained voluntary contraction (B), and the MIR to mental nerve stimulation (C). Traces are the result of averaging ten rectified responses to the electrical stimulus of the corresponding nerve (arrow), when applied alone (control) and when preceded by a digital nerve electrical stimulus at the 1SI marked at the left side of each trace. Scattergrams show the mean and one SD of the area of the responses obtained at all ISis examined, expressed as a percentage of control values. *ISis in which the mean area of the response is significantly smaller (P < 0.01) than that of the responses obtained in control trials. #ISis in which the mean area of the R2 response obtained in test trials is significantly different (P < 0.05) during contraction with respect to rest.
the digital nerve electrical stimulus. We followed the same procedure for the BR to supraorbital nerve electrical stimulation at rest and during contraction of the orbicularis oculi. The area of the responses was measured by multiplying amplitude by duration. In the inhibitory and excitatory responses obtained during contraction, the amplitude was measured as the depth or the height, respectively, of the peak of the response taken from arbitrary lines drawn at 80% and 120% of the mean level of background EMG activity in the 100 ms preceding the first electrical stimulus. Normalization of the data was accomplished by assigning the value of 100% to the area of the MIR elicited by the mental nerve stimulus alone, or to the area of the BR elicited by supraorbital nerve stimulus alone, and expressing the area of the response obtained when the same stimulus was preceded by the digital nerve stimulus as a percentage.
At every ISI, we compared the area of the response to combined digital nerve and mental nerve stimuli with that of the response to mental nerve stimulus alone, and those to digital nerve and supraorbital nerve stimuli with that of the responses to supraorbital nerve stimulus alone. We also compared for every ISI the effects induced on the MIR with those induced on the BR, as well as the effects observed in the BR at rest with those observed during contraction. All statistical comparisons were performed by repeated analysis of variance (ANOVA). The MIR to mental nerve stimuli alone had two distinct phases in all subjects (MIR1 and MIR2). Latency of MIR1 was 17.1 ms (SD= 2.1) and area was 2141 a.u. ( S D = 2 1 3 a.u). Latency of MIR2 was 51.8ms (SD= 5.8 ms), and area was 3310 a.u. (SD = 346 a.u.). The prepulse stimulus caused no effect on MIR1, but induced a reduction of the area of the MIR2 which decreased to 3040% of the control values at ISis between 60 and 100 ms
E. Gdmez-Wong, J. Valls-Sol~/ Neuroscience Letters 208 (1996) 183-186
(Fig. 1). The BR at rest had two responses. The mean latency of R1 was 10.8 ms (SD = 1.1 ms), and the mean amplitude was 530/~V (SD = 106/~V). The mean latency of R2 was 37.6 ms (SD = 5.4 ms), and the mean area was 5640 a.u. (SD = 650 a.u.). The preceding digital nerve stimulus caused facilitation of R1 at ISis between 50 and 70 ms, and inhibition of R2 at ISis between 50 and 200 ms. During contraction of the orbicularis oculi, supraorbital nerve stimulation induced two excitatory phases at a latency corresponding with that of the R1 and R2 responses elicited at rest. The preceding digital nerve had no effect on the excitatory phase corresponding to R1, but reduced significantly the phase corresponding to R2 at ISis of 50-100 ms. The percentage reduction induced by the prepulse on the inhibitory MIR2 was not different from that induced on the excitatory R2 during contraction of the orbicularis oculi at any ISI (P values between 0.13 and 0.68). However, the effects of the prepulse on MIR2 and on R2 during contraction were significantly smaller than those induced on R2 at rest at the ISis of 7 0 m s ( P = 0.04), 8 0 m s ( P = 0.01), and 90 ms (P = 0.02). The most relevant findings of the present study are that there is a common effect of a weak prepulse stimulus on various brainstem reflexes, that the effects are similar on excitatory and inhibitory responses, and that they are reduced during voluntary activation with respect to rest. There is not much research done in humans regarding the collision of activity in different neural circuits. This is in contrast with the fact that the central nervous system is normally exposed to the simultaneous arrival of many sensory inputs of different modalities with any human activity. Sensorimotor inhibition or 'gating' is probably one of the most basic strategies used by the central nervous system for select:ion of useful information from the constant environmental bombardment of inputs [6,8]. Prepulse inhibition may be the neurophysiological expression of a gating mechanism on processing of reflex responses [17]. Studies done in animals suggest that prepulse inhibition is a feature of the brainstem [10,15,17]. The exact location of the effect, however, is unknown. Animal experiments suggested lhat prepulse inhibition is mediated by a complex neural circuitry involving several structures such as the frontal cortex, the nucleus accumbens, the palidum, the pontine nuclei, and the superior colliculus, but neither the exact structure nor the neurotransmitter in charge of the prepulse effect have been identified so far [9,17]. From our study it appears that a weak prepulse has a multi-level effect, inducing inhibition on several brainstem reflex responses. It is possible that prepulse inhibition uses a brainstem circuit processing sensory inputs from many modalities. Rimpel et al. [13] hypothesized the existence of a common polysensory system integrating the activity from visual, acoustic and trigeminal inputs before reaching the facial nerve. Afferent inputs
185
from nerves of the limbs can be added to such a common brainstem polysensory system since the finding of their modulatory influences on trigemino-facial reflexes [2,14, 18]. The present study shows that trigemino-trigeminal inhibitory reflexes should be included as one of the targets expressing brainstem sensorimotor gating phenomena. Similar findings have been reported by other authors using thermic [3] and electrical stimuli producing tactile or painful sensations [16]. The observation in our work of the occurrence of the same effect on trigemino-trigeminal (MIR2) and trigemino-facial (BR) reflexes indicates that prepulse effects occur at the trigeminal nerve afferents themselves, before synapsing with facial or trigeminal motoneurons. This is in keeping with reports from experiments performed in animals [1]. The prepulse effects induced in the blink reflex were markedly reduced during voluntary contraction with respect to rest. Facilitation of R1 disappeared and inhibition of R2 diminished significantly. Activity in the corticonuclear tract may conceal both the excitatory and the inhibitory effects of a prepulse by modifying the excitability of the brainstem interneurons mediating such effects. Once the presence of voluntary contraction was taken into account, the effects of a digital prepulse were the same for the excitatory responses of the BR and the inhibitory responses of the MIR. This indicates that the prepulse effects are exerted on excitatory and inhibitory interneurons of the brainstem with no specificity. R1 was facilitated at rest, a finding that has been observed many times before and has been interpreted as the result of an enhanced preparatory state while processing sensory information [8]. The differential effects between R1 and R2, and those between MIR1 and MIR2, could be related to the different amount of interneurons in the chain of early and late responses, or to the fact that these responses follow a different circuit in the brainstem [11, 12]. Brainstem excitatory and inhibitory reflexes are routinely used in the neurophysiological assessment of patients with neurological diseases [7]. Studying the prepulse effects of peripheral nerve afferents on the blink reflex and on the masseteric inhibitory reflex offers new possibilities for the assessment of brainstem reflex functions in humans. [1] Baldissera, E, Broggi, G. and Mancia, M., Depolarization of trigeminal afferents induced by stimulation of brainstem and peripheral nerves, Exp. Brain Res., 4 (1967) 1-17. [2] Boulu, Ph., Willer, J.V. and Cambier, J., Analyse electrophysiologique du reflexe de clignement chez l'homme: interactions des affrrences sensitives segmentaires et intersegmentaires, des affrrences auditives et visuelles, Rev. Neurol., 137 (1981) 523533. [3] Cadden, S.W. and Newton, J.E, The effects of inhibitory controls triggered by heterotopic noxious stimuli on a jaw reflex evoked by perioral stimuli in man, Arch. Oral Biol., 39 (1994) 473--480. [4] Geyer, M.A., Swerdlow, N.R., Mansbach, R.S. and Braff, D.L., Startle response models of sensorimotor gating and habituation deficits in schizophrenia, Brain Res. Bull., 25 (1990) 485-498.
186
E. G6mez- Wong, J. Valls-Solg / Neuroscience Letters 208 (1996) 183-186
[5] Graham, EK., The more or less startling effects of weak prestimulation, Psychophysiology, 12 (1975) 238-248. [6] Hoffman, H.S. and Ison, J.R., Reflex modification in the domain of startle, 1: some empirical findings and their implications for how the nervous system processes sensory input, Psychol. Rev., 87 (1980) 175-189. [7] Hopf, H.C., Topodiagnostic value of brain stem reflexes, Muscle Nerve, 17 (1994) 475--484. [8] Ison, J.R, Sanes, J.N., Foss, J.A. and Pinckney, L.A., Facilitation and inhibition of the human startle blink reflex by stimulus anticipation, Behav. Neurosci., 104 (1990) 418-429. [9] Koch, M. and Friauf, E., Glycine receptors in the caudal pontine reticular formation: are they important for the inhibition of the acoustic startle response? Brain Res., 671 (1995) 63-72. [10] Koch, M., Kungel, M. and Herbert, H., Cholinergic neurons in the pedunculopontine tegmental nucleus are involved in the mediation of prepulse inhibition of the acoustic startle response in the rat, Brain Res., 97 (1993) 71-82. [11] Ongerboer de Visser, B.W. and Goor, C., Cutaneus silent periods in masseter muscles: electrophysiological and anatomical data, J. Neurol. Neurosurg. Psychiatry, 39 (1976) 674-679. [12] Ongerboer de Visser, B.W. and Kuypers, G.J.M., Late blink reflex changes in lateral medullary lesions: an electrophysiological and
[13]
[14]
[15]
[16]
[17]
[18]
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