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. 2001 Mar 1;531(Pt 2):559–571. doi: 10.1111/j.1469-7793.2001.0559i.x

Excitability of the human trigeminal motoneuronal pool and interactions with other brainstem reflex pathways

G Cruccu *, A Truini *, A Priori *
PMCID: PMC2278464  PMID: 11230527

Abstract

  1. We studied the properties of motoneurones and Ia-motoneuronal connections in the human trigeminal system, and their functional interactions with other brainstem reflex pathways mediated by non-muscular (Aβ) afferents. With surface EMG recordings we tested the recovery cycles of the heteronymous H-reflex in the temporalis muscle and the homonymous silent period in the masseter muscle both elicited by stimulation of the masseteric nerve at the infratemporal fossa in nine healthy subjects. In four subjects single motor-unit responses were recorded from the temporalis muscle. In six subjects we also tested the effect of the stimulus to the mental nerve on the temporalis H-reflex and, conversely, the effect of Ia input (stimulus to the masseteric nerve) on the R1 component of the blink reflex in the orbicularis oculi muscle.

  2. The recovery cycle of the H-reflex showed a suppression peaking at the 5-20 ms interval; conversely the time course of the masseteric silent period was facilitated at comparable intervals. The inhibition of the test H-reflex was inversely related to the level of background voluntary contraction. Single motor units were unable to fire consistently in response to the test stimulus at intervals shorter than 50 ms.

  3. Mental nerve stimulation strongly depressed the H-reflex. The time course of this inhibition coincided with the EMG inhibition elicited by mental nerve stimulation during voluntary contraction. The trigeminal Ia input facilitated the R1 component of the blink reflex when the supraorbital test stimulation preceded the masseteric conditioning stimulation by 2 ms.

  4. We conclude that the time course of the recovery cycle of the heteronymous H-reflex in the temporalis muscle reflects the after-hyperpolarization potential (AHP) of trigeminal motoneurones, and that the Ia trigeminal input is integrated with other brainstem reflexes.

Weak electrical stimuli delivered to the motor nerve supplying the masseter muscle (masseteric nerve) during voluntary contraction of jaw-closing muscles elicit, in humans, an H-reflex in the masseter (Godaux & Desmedt, 1975a; Cruccu et al. 1989) and temporalis muscles (Macaluso & De Laat, 1995). The activation of heteronymous Ia projections arising from the masseter muscle and directed to temporalis motoneurones elicits the pure reflex excitation of temporalis motoneurones with no antidromic influences on their excitability. Stimulation of the masseteric nerve also evokes an antidromic volley along motor axons thus invading the homonymous masseteric motoneurones (Cruccu et al. 1989) and thereby leading to a transient suppression of the voluntary ongoing EMG activity in the masseter muscle, namely the silent period (Merton, 1951).

Trigeminal motoneurones have been studied less extensively than spinal motoneurones. They also differ from them in several ways: for example, they receive strong inhibitory inputs from mechanoreceptors through Aβ and possibly from Aδ afferents (Nakamura, 1980; Miles & Turker, 1987; Cruccu & Ongerboer de Visser, 1999), and have neither reciprocal nor recurrent inhibition (Lorente De Nò, 1933; Nakamura, 1980).

Several physiological mechanisms influence spinal motoneuronal excitability in vivo and the net contribution of each individual mechanism is often difficult to estimate (for references, see Rothwell, 1994). For example, the excitability of the H-reflex and the duration of the silent period in a limb muscle both reflect the actions of various mechanisms affecting motoneuronal excitability. Primary changes in the membrane potential (i.e. the after-hyperpolarization potential (AHP)) are only one among the complex array of physiological phenomena that modulate the H-reflex and motoneuronal excitability in limb muscles.

A useful approach to understanding the role of these complex excitatory and inhibitory mechanisms is to study a motoneuronal pool that has a comparatively simple segmental organization. The trigeminal motoneuronal pool therefore seemed an ideal system for investigating the intrinsic mechanisms controlling motoneuronal excitability. In this paper we studied the properties of Ia-motoneuronal connections and motoneurones in the human trigeminal system by assessing the recovery cycles of the heteronymous H-reflex in the temporalis muscle and homonymous silent period in the masseter muscle, both elicited by paired stimulation of the masseteric nerve. We also studied the functional interactions of Ia-motoneuronal trigeminal connections with other brainstem reflex pathways mediated by non-muscular (Aβ) afferents. We did so by testing the excitability of the trigeminal motoneuronal pool at various times after the cutaneous stimulus, using the heteronymous H-reflex as a test stimulus, and the conditioning effect of masseteric Ia input on the short-latency (R1) component of the blink reflex.

Preliminary results have been reported in abstract form (Priori et al. 1998b).

METHODS

Subjects

Twelve healthy volunteers (7 women, 5 men, mean age 29 years, range 23-48 years) participated in six different experiments. Subjects gave their informed written consent and the experimental protocol conformed to the Declaration of Helsinki and was approved by the local ethical committee. None of the subjects had neurological or dental diseases. During experiments, subjects were seated in a comfortable chair and instructed to gaze forward and, when asked, to contract the jaw-closing muscles of both sides in intercuspal occlusion and under audio-visual feedback of the electromyographic (EMG) activity. Subjects were instructed to maintain a fixed level of EMG activity. To avoid fatigue they were allowed to rest after each trial. A consistent level of contraction was achieved for each trial (see below). Maximal clenching was measured at the beginning and at the end of each experimental session. In single motor unit recordings, to avoid changes in the position of the needle electrode subjects (exerting a lower level of contraction) were not allowed to rest (see below).

EMG recording and signal processing

The surface EMG signal was usually recorded from the right masseter and the right temporalis muscle, with pairs of surface non-polarizable Ag-AgCl disk electrodes (outer diameter 9.0 mm). For the masseter muscle the active electrode was placed over the muscle belly and the reference electrode about 2 cm below the angle of the jaw; for the temporalis muscle the active electrode was placed over the anterior part of the muscle and the reference electrode about 3 cm anteriorly over the forehead (Cruccu & Ongerboer de Visser, 1999). The electrode impedance was optimized at the beginning of each experiment and was checked throughout the session. During most experiments subjects exerted a voluntary contraction of 75 % of the maximum EMG level in the temporalis muscle; for single-unit experiments they exerted a 35-45 % voluntary contraction.

Signals were amplified, filtered (10 Hz-2 kHz), digitized (Cambridge 1401, sampling rate 5 kHz; Cambridge Electronic Design Ltd, UK), and processed on a PC by a dedicated software program for the analysis of biological signals (SIGAVG, Cambridge Electronic Design Ltd). Off-line averaging was used for quantitative analyses. The peak-to-peak amplitude and the onset latency of the M-wave in the masseter muscle and the H-reflex in the temporalis muscle were measured off-line. The duration of the EMG silent period after the M-wave in the masseter muscle was measured from the end of the positive phase of the M-wave to the end of the absolute electrical silence. In paired stimulation experiments the amplitude of the test H-reflex and the duration of the test silent period were expressed as a percentage of the respective unconditioned control response.

In four subjects we recorded possible long-latency responses in the temporalis muscle, at rest and during voluntary contraction. The stimulus intensity was adjusted so as to evoke a clear and relatively stable H-reflex during contraction; EMG signals were rectified and averaged over 100 trials.

In four subjects the response from single motor units of the temporalis muscle was studied by concentric needle recordings (Strumentazione Elettronica Industriale, Cittadella, Italy). To reduce the signal arising from other adjacent motor units, single motor unit spikes were captured and analysed with a special off-line digital signal band-passing (low cut 500 Hz). This method and careful positioning of the needle electrode ensured stable recording conditions of spikes from one or occasionally two motor units. Spikes were discriminated off-line and the firing probability in response to S2 was calculated and normalized to the firing probability in response to S1 of the same unit (see below). During this experiment, to avoid electrode displacements, reduce muscle fatigue, and avoid activating too many motor units, we asked subjects to contract the target muscle at 35-45 % of maximum.

Nerve stimulation

In the main experiment the right masseteric nerve was electrically stimulated in the infratemporal fossa (Fig. 1) with a technique similar to that described by Macaluso & De Laat (1995). Cathodal square pulses (0.1 ms) generated by a constant current nerve stimulator (Digitimer Stimulator DS7; Digitimer Ltd, Welwyn Garden City, UK) were delivered through a Teflon-coated monopolar needle electrode (TECA 902-DMG25, 53534) with an uninsulated tip (diameter 0.36 mm; area 0.28 mm2) inserted to 1.5 cm through the skin below the zygomatic arc and anterior to the temporo-mandibular joint into the infratemporal fossa (Fig. 1). The anode was a surface non-polarizable Ag-AgCl disk electrode (outer diameter 9.0 mm) placed over the ipsilateral earlobe. Electrical stimulation of the masseteric nerve never produced pain and the subjects perceived only the muscle twitch. The proper position of the stimulating electrodes was monitored throughout the experimental session by checking on-line the size of the M-wave in the masseter muscle. The threshold current intensities for the M-wave and for the H-reflex were measured.

Figure 1. The heteronymous H-reflex in the temporalis muscle and the M-wave with its ensuing silent period in the masseter muscle elicited by electrical stimulation of the masseteric nerve in the infratemporal fossa.

Figure 1

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Left, anatomic schematic representation of the human infratemporal fossa in coronal section, showing the temporalis muscle and deep temporal nerves (T), the masseter muscle and masseteric nerve (M), and the site of stimulation with a monopolar needle electrode (Stim). Right, H-reflex (H), M-wave (M) and silent period (SP) in a representative subject during maximum voluntary contraction; traces are raw signals (superimposition of 8 trials). Upper traces, bipolar surface EMG recording from the right temporalis muscle; horizontal calibration, 20 ms; vertical calibration, 0.5 mV. Lower traces, bipolar surface recording from the right masseter muscle; horizontal calibration, 20 ms; vertical calibration, 2 mV. The H-reflex in the temporalis muscle has a latency of 4.5 ms and the M-wave in the masseter muscle has a latency of 1.5 ms. In the temporalis muscle the stimulus elicits no silent period whereas in the masseter muscle it elicits a silent period lasting about 30 ms.

Recovery cycles

Throughout the text the recovery cycle is defined as the time course of the changes in the size of a given test response when it is preceded at variable time intervals by a conditioning response. The recovery cycle of the H-reflex was studied in nine subjects by delivering pairs of equal stimuli to the masseteric nerve: the first or conditioning stimulus (S1) elicited the unconditioned response, and the second or test stimulus (S2) elicited the test response. The stimulator output was monitored on an oscilloscope to ensure that S1 and S2 were identical. The interstimulus interval between S1 and S2 or the conditioning-test interval ranged from 5 to 200 ms. The stimulus intensity was kept at a level eliciting a reflex of 75 % of the maximum reflex size (2-3 mA). At short intervals (< 15 ms) when the conditioning and test responses overlapped, a control reflex was randomly acquired in separate trials with one stimulus alone. At longer conditioning-test intervals the amplitude of unconditioned and test responses were measured in the same sweep. From eight to 16 trials were acquired and averaged for each conditioning-test interval: 50 % were unconditioned control trials (S1) and 50 % were conditioned test trials (S1 + S2). The amplitude of the (conditioned) test H-reflex was expressed as a percentage of the (unconditioned) control response. In single unit recordings the firing probability in response to S2 was calculated and normalized to the firing probability in response to S1 of the same unit.

With a similar procedure we studied the recovery cycle of the homonymous silent period elicited in the masseter muscle by antidromic volley along motor axons. The stimulus intensity was kept at a level eliciting a maximum-amplitude M-wave (2-4 mA). Control responses were acquired in separate trials randomly alternated with conditioned trials. The duration of the (conditioned) test silent period was expressed as a percentage of the duration of the (unconditioned) control silent period.

Conditioning of the heteronymous H-reflex by trigeminal cutaneous input

In this and in subsequent experiments the conditioning and the test stimuli were delivered to two distinct and spatially separated sets of afferents.

In six subjects we studied the conditioning effect of mentalis nerve stimulation on the ipsilateral temporalis H-reflex. Electrical stimuli (0.2 ms) were delivered through a pair of surface non-polarizable Ag-AgCl disk electrodes (diameter 0.9 mm): the cathode over the mental foramen, and the anode 2 cm laterally. The stimulus intensity was adjusted to elicit clearly distinguishable early and late exteroceptive suppressions without causing pain (18-34 mA) (Cruccu & Ongerboer de Visser, 1999). A test H-reflex was evoked in the temporalis muscle by masseteric nerve stimuli delivered at various conditioning-test intervals after the mentalis stimulus (from 0 to 100 ms). Each conditioning-test trial was alternated with a control trial using unconditioned masseteric stimulation alone. From eight to 16 trials were repeated for each conditioning-test interval: 50 % were unconditioned control trials and 50 % were conditioned test trials. The amplitude of the test H-reflex was expressed as a percentage of the control. In all subjects we also separately recorded the rectified and averaged (8-16 trials) EMG suppression after mental nerve stimulation.

Conditioning of the blink reflex by Ia trigeminal input

In six subjects we studied the conditioning effect of masseteric nerve stimulation on the R1 blink reflex. The intensity of the masseteric stimuli (2-3 mA) was similar to that used in recovery cycle experiments; it elicited the H-reflex during contraction, and the subject perceived only the muscle twitch. The subject kept all muscles (including the temporalis) fully relaxed. Signals were recorded from the ipsilateral orbicularis oculi muscle through surface electrodes. Electrical stimuli (0.2 ms) were delivered to the supraorbital nerve through a pair of surface non-polarizable Ag-AgCl disk electrodes (diameter 0.9 mm): the cathode was placed over the supraorbital groove, and the anode 2 cm more cranially. The stimulus intensity (12-20 mA), about twice the sensory threshold, consistently elicited a stable R1 blink reflex. Subjects described the stimuli as non-painful. Control trials with supraorbital stimulation alone were randomly alternated with test trials with conditioning masseteric stimulation. Test stimuli to the supraorbital nerve were delivered at various conditioning-test intervals: 4 and 2 ms before the masseteric stimulation, simultaneously, and 2, 4, 10 and 15 ms after masseteric stimulation. From eight to 16 trials were repeated for each conditioning-test interval: 50 % were unconditioned control trials and 50 % were conditioned test trials. The amplitude of the (conditioned) test R1 blink reflex was expressed as a percentage of the amplitude of the (unconditioned) control R1.

Statistical analysis

Data in the text are means ± 1 s.e.m. Because data had a Gaussian distribution (as assessed by the Kolmogorov-Smirnov test) and the variances were homogeneous, they were analysed with parametric methods. We used either a Student's two-sample or a paired t test. In one experiment, detailed in the text, we also used repeated measures ANOVA. We also used non-parametric methods to evaluate whole time courses of recovery cycles with Kruskal-Wallis analysis and the correlation between different variables with the Spearman R correlation coefficient. The level of significance was set at P < 0.05 (two-tailed). For statistical analysis and graphs we used the Prism 3.0 software package (GraphPad, Sorrento Valley, CA, USA).

RESULTS

General characteristics of the EMG responses evoked by masseteric nerve stimulation

None of the 12 subjects had an H-reflex in the temporalis muscle at rest. But they all had a readily distinguishable response during voluntary contraction (Fig. 1). In contrast, none of the six subjects tested for this purpose had long-latency responses.

The temporalis H-reflex and the masseter M-wave had a similar threshold intensity (1.5 ± 0.3 mA and 1.2 ± 0.2 mA, P > 0.2). Supramaximal stimuli elicited a temporalis H-reflex with a latency of 5.0 ± 0.2 ms and an amplitude of 2.1 ± 0.4 mV, and a masseter M-wave with a latency of 1.5 ± 0.1 ms and an amplitude of 8.4 ± 1.0 mV.

The silent period following the M-wave in the masseter muscle had a duration of 40.0 ± 5.0 ms. Masseter nerve stimulation selectively elicited a silent period in the homonymous muscle but in the ipsilateral temporalis and contralateral jaw-closing muscles it did not. In surface recordings the H-reflex in the temporalis muscle had no ensuing silent period (Fig. 1).

Recovery cycle of the heteronymous temporalis H-reflex

During the experiments with paired stimulation (the stimulus intensity was kept submaximal) the H-reflex had an amplitude of 1.65 ± 0.3 mV (Fig. 2). The test H-reflex was markedly smaller (up to 50 % of the control) at short conditioning-test intervals (between 5 and 20 ms, P < 0.01), then progressively recovered, approaching control values at the 100 ms interval. The changes in the whole time course were statistically significant (Kruskal-Wallis, P < 0.001).

Figure 2. Recovery cycle of the heteronymous H-reflex in the temporalis muscle.

Figure 2

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Upper panel, raw signals (averages of 8 trials) of the recovery cycle with paired electrical stimuli in a representative subject; 1: control H-reflex; 2-9: paired stimuli at conditioning-test intervals of 5 ms (2), 10 ms (3), 20 ms (4), 30 ms (5), 40 ms (6), 50 ms (7), 100 ms (8) and 150 ms (9); vertical calibration, 1 mV; horizontal calibration, 10 ms for traces 1-7, 25 ms for traces 8-9. Lower left graph, average time course of the recovery cycle of the H-reflex in all the subjects. Y-axis, size of the conditioned test reflex expressed as a percentage of the peak-to-peak amplitude of the unconditioned control H-reflex; X-axis, conditioning-test interval (ms) on a logarithmic scale; symbols and error bars, mean ± 1 s.e.m.; *P < 0.05; **P < 0.01 (paired t test; n = 9 for each interval). Kruskal-Wallis analysis of the whole curve is highly significant (P < 0.001). Note that at conditioning-test intervals between 5 and 20 ms the test H-reflex is smaller, then progressively increases until it regains the control amplitude at about 100 ms. Lower right graph, recovery cycle of the H-reflex in single motor unit (SMU) recordings. Y-axis, probability (%) that the same SMU is excited twice first by the conditioning then by the test stimulus (the Y-axis probability is normalized to the probability of a single motor unit firing after a single stimulus across the recording session); X-axis, conditioning-test intervals (ms); symbols and error bars, mean ± 1 s.e.m.*P < 0.01; **P < 0.0001 (paired t test; n = 6 for the 10 and 25 ms intervals; n = 7 for the 50, 75 and 100 ms intervals). Note that single motor units are unable to fire consistently in response to the test stimulus at intervals shorter than 50 ms.

In single unit recordings, a single electrical shock to the masseteric nerve rarely elicited a stable response: of 23 motor units assessed in the temporalis muscle, only seven consistently responded and did so at a latency of 5-9 ms. When both stimuli were delivered at intervals shorter than 50 ms none of the seven units tested over 100 trials consistently fired twice in response to the two stimuli (Fig. 2, lower right graph).

Examined in six subjects, the recovery of the test H-reflex with surface recordings at the 10 ms conditioning-test interval was proportional to the level of background EMG activity (Fig. 3): the test response was significantly larger at high than at low levels of EMG activity (P < 0.02). The size of the conditioned test response was linearly correlated with the background level of voluntary contraction (Spearman R, P < 0.01).

Figure 3. Effect of voluntary contraction on the inhibition of the test H-reflex.

Figure 3

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Left graph, filled circles and error bars show mean ± 1 s.e.m. of the amplitude of the control H-reflex (right Y-axis); filled squares and error bars show mean ± 1 s.e.m. of the test H-reflex (expressed as a percentage of the amplitude of the control H-reflex), at the 10 ms conditioning-test interval (left Y-axis). The subjects were asked to exert a 50 % maximum contraction (‘condition 50′) and 100 % maximum contraction (‘condition 100′) (X-axis). In condition 50 the background EMG level, as measured in the contralateral temporalis muscle, was 45 ± 5.3 % of the maximum EMG level. In condition 100, to obtain a control H-reflex with the same size as in condition 50, the stimulus intensity was slightly lowered. The amplitude of the test H-reflex was significantly higher in condition 100 than in condition 50 (paired t test, P = 0.0159; n = 6). Right graph, linear regression (continuous line) ± 95 % confidence interval (dashed curves) of the correlation between the test H-reflex (Y-axis) and the background EMG level, normalized between subjects (X-axis, 100 %= average maximum absolute EMG level). Each subject is represented by two squares (low and high levels of contraction). The correlation was highly significant (Spearman R, P = 0.0087; n = 12). Note that the inhibition of the test H-reflex linearly decreases with increasing level of voluntary background contraction.

Recovery cycle of the homonymous masseteric silent period

At all intervals tested the M-waves elicited by the test shock remained unchanged. The shape of the recovery curve of the silent period in the masseter muscle was inverted compared with that of the H-reflex in the temporalis muscles, but the time courses were similar (Fig. 4). The test silent period was markedly longer (up to 140 % of the control) at short conditioning-test intervals (between 5 and 20 ms, P < 0.01), then progressively returned to control values at the 80-100 ms intervals. The changes in the whole time course were statistically significant (Kruskal-Wallis, P < 0.001).

Figure 4. Recovery cycle of the silent period in the masseter muscle.

Figure 4

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Upper panel, recovery cycle of the silent period to paired stimuli in the masseter muscle (superimpositions of 8 trials) in a representative subject: control silent period (1), paired stimuli at conditioning-test intervals of 10 ms (2), 20 ms (3), 50 ms (4), 100 ms (5) and 150 ms (6); vertical calibration, 2 mV; horizontal calibration, 10 ms for traces 2-4, 20 ms for traces 1, 5 and 6. Note the M-wave before each silent period. Lower panel, diagram of the average time course of the recovery cycle of the silent period in the masseter muscle in all subjects; Y-axis, size of the conditioned test silent period expressed as a percentage of the duration of the unconditioned control value; X-axis, conditioning-test interval (ms) logarithmic scale; squares and error bars, means ± 1 s.e.m.*P < 0.05; **P < 0.01 (paired t test; n = 9 for each interval). Kruskal-Wallis analysis of the whole curve is highly significant (P < 0.001). Note that the silent period in the masseter muscle is strongly facilitated at conditioning-test intervals between 5 and 20 ms.

Conditioning of the heteronymous temporalis H-reflex by cutaneous input

The test H-reflex recorded in the temporalis muscle after mental nerve stimulation was strongly depressed (Fig. 5). At conditioning-test intervals from 10 to 20 ms it was abolished; at the 30 ms interval it recovered to 60 % of the control value and from 50 to 70 ms again underwent strong suppression (up to 25 % of the control). The test H-reflex returned to control values by the 100 ms interval.

Figure 5. Effect of cutaneous trigeminal input on the heteronymous temporalis H-reflex.

Figure 5

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Upper panel, conditioning of the test H-reflex (A) and voluntary EMG (B) in the temporalis muscle after mental nerve stimulation in a representative subject; the test H-reflexes are averages of 8 trials at conditioning-test intervals of 0 ms (1), 10 ms (2), 30 ms (3), 50 ms (4), 70 ms (5) and 90 ms (6); the voluntary EMG signal is full-wave rectified and averaged (8 trials); A: horizontal calibration, 10 ms; vertical calibration, 1 mV; B: horizontal calibration, 20 ms; vertical calibration, 0.2 mV. Lower graph, average time course of the test H-reflex (continuous line) and the voluntary EMG level (dashed line) after conditioning stimulation of the mental nerve, in all subjects; Y-axis, size of the test response, expressed as percentage of either the amplitude of the control H-reflex or the average prestimulus background EMG level; X-axis, conditioning-test intervals (ms) for the H-reflex (first (left) values) and time + 5 ms after the conditioning stimulus for the EMG (second (right) values); the EMG is shifted 5 ms later than the test stimulus to allow for the H-reflex latency; error bars are ± 1 s.e.m. Note that the time courses of the EMG and the H-reflex coincide. Inset, linear regression and correlation between the same two variables that are plotted on the Y-axis of the main graph, at all intervals; here the size of test H-reflex (% of the unconditioned control reflex) is plotted on the Y-axis and the EMG level (% of the average prestimulus background EMG) on the X-axis. Each symbol represents one subject at a given conditioning-test interval; the test H-reflex at a given interval was compared with the EMG level at that interval + 5 ms (see above). The correlation between the two variables was highly significant (Spearman R, P < 0.0001).

Cutaneous conditioning had the same effect on the voluntary EMG and on the H-reflex, thus yielding two almost equal curves (Fig. 5). The amplitude (%) of the test H-reflex co-varied with that of the voluntary EMG (Spearman R, P < 0.0001). Repeated measures ANOVA showed no significant differences between the test H-reflex and the voluntary EMG activity at any interval tested (P > 0.20), thus excluding even small extra-effects.

Conditioning of the blink reflex by Ia trigeminal input

The latency of the test R1 was 11.5 ± 0.7 ms, and the amplitude was 0.2 ± 0.05 mV. When the supraorbital test stimulus preceded the masseteric conditioning stimulus by 2 ms, the test R1 response reached a 20 % facilitation (P < 0.01; paired t test) then progressively decreased (Fig. 6).

Figure 6. Effect of trigeminal Ia input on the R1 component of the blink reflex.

Figure 6

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Upper panel, control R1 (traces 1 and 3) and test R1 after conditioning stimulation of the masseteric nerve at conditioning-test intervals of -2 ms (2) and 10 ms (4) in a representative subject; each trace is the average of 8 trials; surface recordings from the orbicularis oculi muscle; horizontal calibration, 5 ms; vertical calibration, 0.2 mV; the large deflection that precedes R1 in traces 2 and 4 is the volume-conducted masseter M-wave detected by the orbicularis oculi electrodes. Note that the test R1 in trace 2 is slightly facilitated with respect to its control in trace 1, whereas the responses in traces 3 and 4 are almost identical. Lower panel, graph of the time course of the R1 changes after masseteric nerve conditioning stimulation, in all subjects; Y-axis, peak-to-peak amplitude of the test R1 expressed as a percentage of the control R1; X-axis, conditioning-test interval (ms) separating the masseteric nerve stimulation from supraorbital nerve stimulation; the minus sign means that the conditioning masseteric stimulation follows the test supraorbital stimulation; symbols and error bars, means ± 1 s.e.m. Note the significant facilitation when the conditioning stimulation (to the masseteric nerve) is given 2 ms after the test stimulation (to the supraorbital nerve) (paired t test, *P < 0.01; n = 6).

DISCUSSION

In this study we investigated the properties of the Ia-motoneuronal connections and motoneurones in the human trigeminal system. The recovery cycle of the temporalis H-reflex showed a suppression peaking at the 5-20 ms interval, whereas at comparable intervals the time course of the masseteric silent period showed a lengthening. In the experiments investigating the interaction between masseteric Ia input and other brainstem reflexes, the conditioning trigeminal cutaneous input strongly inhibited the heteronymous H-reflex. In turn, the conditioning masseteric Ia input facilitated transmission through the pathway for the cutaneous R1 blink reflex.

The masseteric nerve is a muscle nerve containing motor axons and group I, III and IV muscle afferents, but no cutaneous afferents (Martin & Panneton, 1986; Nishimori et al. 1986). Ia afferents from muscle spindles could not be detected because they have their cell body in the mesencephalic nucleus (Darian-Smith, 1973; Nakamura, 1980), and in jaw-closing muscles Golgi tendon organs are very few, their functional action being vicariously accomplished by the periodontal mechanoreceptors (Lund et al. 1978; De Laat, 1987).

For delivering masseteric stimuli we essentially used the technique described by Macaluso & De Laat (1995) and obtained almost identical H-responses in the temporalis muscle. The slight differences in threshold and latency presumably depend on the shorter duration of our stimulus: to minimize the possibility that our stimulus excited small fibres we used a stimulus duration of 0.1 ms instead of 1 ms (Macaluso & De Laat, 1995; Macaluso et al. 1998; Svensson et al. 1998). Besides the heteronymous H-reflex, masseteric nerve stimulation elicited an M-wave in the masseter muscle followed by a silent period lasting 30-40 ms, similar to that seen after low-intensity electrical stimuli in intraoperative recordings (Cruccu & Bowsher, 1986).

The recovery cycles of EMG responses in jaw-closing muscles

Overall, the recovery cycle experiments showed that for some 100 ms after a conditioning stimulation the temporalis H-reflex (i.e. the heteronymous Ia- motoneurone connection) is inhibited, whereas the masseter silent period (i.e. the homonymous antidromic motoneuronal inhibition) is facilitated.

These findings raise two questions: whether the time courses of the two recovery cycles have a single underlying mechanism or two distinct, independent mechanisms, and of what type. The excitability profile of both phenomena strongly indicates as the underlying mechanism the AHP in jaw-closing motoneurones. All other possible mechanisms seem improbable. The fact that trigeminal motoneurones have no recurrent axon collaterals excludes Renshaw inhibition (Lorente De Nò, 1933; Nakamura, 1980). Presynaptic inhibition of group Ia afferents probably plays no role for several reasons. First, whereas available data indicate that presynaptic inhibition of group I afferents and their PAD (primary afferent depolarization) in the trigeminal system are elicited either by the lingual nerve (Goldberg, 1972) or by cutaneous trigeminal fibres (Goldberg & Nakamura, 1977), in our recovery cycle experiments we avoided stimulating these afferents (see below). In human jaw-closing muscles presynaptic inhibition has no effect on the gain of the stretch reflex (Lobbezoo et al. 1993). We also conducted our H-reflex experiments during voluntary contraction, a condition that reduces or abolishes presynaptic inhibition (Priori et al. 1995, 1998a). In addition, whereas muscle vibration reduces the H-reflex size by presynaptic inhibition in limb muscles, vibration enhances the H-reflex in the jaw-closing muscles (Godaux & Desmedt, 1975a). Hence, though presynaptic inhibition of Ia afferents might operate a tonic inhibitory control at rest, under our experimental condition during voluntary contraction it presumably does not. Neither do our recovery cycles reflect cutaneous input. Stimulation of the mental nerve, exciting pure cutaneous afferents, elicits strong EMG inhibition in the jaw-closing muscles, the so-called exteroceptive suppression or masseter inhibitory reflex (Godaux & Desmedt, 1975b). By selectively stimulating a muscle nerve we explicitly avoided exciting cutaneous afferents. Furthermore, the stimulus intensity was too low and the stimulus duration too short to excite group III fibres. Indeed, the subjects perceived only the proprioceptive sensation of muscle twitch. If our stimuli had excited non-muscular afferents they would presumably have elicited widespread inhibition, but they did not: masseteric nerve stimulation elicited no silent period after the H-reflex in the temporalis muscle, no second silent period (40-90 ms) after the M-wave in the masseter muscle (Cruccu & Bowsher, 1986), and more important, no contralateral silent periods. Insofar as periodontal receptors provide an inhibitory input to trigeminal motoneurones (Bonte et al. 1993; Turker et al. 1994), the masseter muscle twitch might determine a mechanical stimulation of periodontal receptors. Experiments in humans indicate, however, that periodontal loading has no effect on the gain of the stretch reflex in the jaw-closing muscles (Lobbezoo et al. 1993). In addition, after the masseter M-wave we observed the silent period only in the ipsilateral masseter muscle, whereas periodontal receptor input would have caused a bilateral inhibition in both the masseter and temporal muscles (De Laat, 1987; Bonte et al. 1993). Ib input is unlikely to influence the excitability of the heteronymous H-reflex during a sustained muscle contraction (as in our experiments) because the Ib inhibitory postsynaptic potentials in motoneurones decline so that the gain of force feed-back is reduced (Zytnicki et al. 1990). In addition, because masticatory muscles contain remarkably few Golgi organs, the functions of Golgi organs are accomplished by the periodontal mechanoreceptors (Lund et al. 1978; De Laat, 1987). The collision mechanism thought partly responsible for the silent period elicited in a limb mixed nerve probably contributes little at trigeminal level. The probability that an orthodromic and an antidromic volley collide is directly related, at a given motoneuronal firing frequency, to the distance between the origin of the antidromic volley and the cell. If the distance is short, the antidromic volley is more likely to reach without collision the cell body during the time interval between two adjacent spikes travelling along motor axons. Hence, given the short distance between the site of stimulation in the infratemporal fossa and the motoneuronal somata in the brainstem, orthodromic and antidromic impulses collide scarcely or not at all. Spindle unloading presumably plays no substantial role because the existence of heteronymous Ia-motoneurone connections implies that unloading effects after a masseter muscle twitch coexisted also in the temporalis muscle. Yet they clearly did not because the H-reflex in the temporalis muscle had no ensuing silent period. Using similar reasoning we can equally exclude presynaptic inhibition and Ib inhibition: indeed these mechanisms are organized for co-modulation of synergist pools of motoneurones (for references, see Rothwell, 1994). Hence, we conclude that the common mechanism responsible for the two time courses we observed is the average AHP, the only process that could selectively inhibit the homonymous motoneurones.

When nerve cells are studied using intracellular electrodes, a long-lasting refractoriness follows each action potential, mostly accounted for by the AHP. In cat spinal motoneurones the action potential is followed by an AHP lasting 40-200 ms (Coombs et al. 1955; Gustafsson, 1974), attributable in trigeminal motoneurones to a calcium-activated increase in potassium membrane conductance (Kobayashi et al. 1997). Rather than being a fixed feature of the motoneuronal membrane, AHP can be affected by various factors that can also alter the firing properties of the cell. The modulation of the AHP by synaptic inputs on the cell is in line with the influence of the level of voluntary contraction on the inhibition of the test H-reflex in our recovery cycle experiments. Interestingly, in our paired stimulation experiments the two masseter muscle silent periods summated: the summation was more evident at intervals below 30 ms. This finding could fit with the known algebraic summation of two AHPs reported in studies using intracellular recordings in animals (Ito & Oshima, 1962; Calvin & Schwindt, 1972). Unfortunately all current methods for estimating postsynaptic potentials with single stimuli (through surface EMG or single motor unit recordings) in human motoneurones have limitations (for a review, see Miles, 1997). Our experiments testing the silent period in jaw-closing muscles cannot estimate the basal trajectory of the membrane potential after a single stimulus: a single silent period in the jaw-closing muscles is a flat isoelectric line. As such, it provides evidence of the existence and duration of underlying inhibition, but gives no estimate of the behaviour of the average motoneuronal membrane potential at each interval. On the other hand, H-reflex experiments describing the excitability profile of the Ia-motoneurone connection probably reflect the profile of the average AHP in heteronymous motoneurones after a single excitatory input and, hence, the basal trajectory of the membrane potential. Therefore, assuming that the masseter and temporalis motoneurones have similar AHPs, the experiments testing the recovery cycles of the H-reflex and the masseter silent period might best be interpreted together. A preliminary consideration is that although the two time courses had almost identical temporal profile (albeit with opposite directions) they essentially reflect the same excitability changes. Under these premises, summating the percentage gain of the time course of the recovery cycle of the silent period, at each interval, to the level of the membrane potential shown by experiments with the H-reflex recovery cycle, yields a curve equal to that produced by the simple algebraic summation of the H-reflex recovery curve itself (Fig. 7). Insofar as AHPs undergo algebraic summation (Gustaffson, 1974) and the sum of the time course of the masseteric silent period with the H-reflex recovery curve gives a curve identical to the curve of algebraic sum of the H-reflex, this again supports the hypothesis that both recovery curves reflect the same phenomenon, namely the average AHP of trigeminal motoneurones. This conclusion fits in well with recordings from rat trigeminal motoneurones: Inoue et al. (1999) report control AHPs in trigeminal jaw-closing motoneurones with a shape and duration similar to the time courses of the recovery cycles we found in humans.

Figure 7. Estimated summation of two AHPs in trigeminal motoneurones.

Figure 7

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Left Y-axis, size of the test responses (silent period and H-reflex) expressed as a percentage of the control responses. Right Y-axis, theoretical percentage changes in the membrane potential. X-axis, conditioning-test intervals (ms) plotted on a logarithmic scale. Curve 1 (▪), time course of the recovery cycle of the silent period (the same curve as that in Fig. 4); curve 2 (♦), time course of the recovery cycle of the H-reflex (the same curve as that in Fig. 2, lower left); curve 3 (•), algebraic summation of two time courses estimated at each point from values on curve 2; curve 4 (○ and thick lines), theoretical summation of curves 1 and 2: because curve 1 reflects the facilitation of an inhibitory response (and curve 2 the inhibition of an excitatory response) we reversed its percentage gain and negatively summated it to curve 2. Note that curves 3 and 4 are almost identical, thus suggesting that the AHP accounts for the time courses of the H-reflex and of the masseteric silent period (see Discussion).

In line with other studies (Macaluso & De Laat, 1995; Macaluso et al. 1998), after delivering single electrical stimuli to the masseteric nerve we obtained no long-latency responses in the temporalis muscle. This finding contrasts with the long-latency excitatory response seen in the masseter after muscle stretch (Miles et al. 1995). The discrepancy has at least two possible explanations. First, in triggering trigeminal motoneurones, a single electrical shock to the nerve is probably much less effective than the volley of action potentials arising from spindle stretch, as it is in general also for other motoneuronal pools. Second, heterotopic stimulation may be less effective in eliciting long-latency responses even in synergist muscles. Synergistic muscles located in the same limb segment respond differently to muscle stretch (Rothwell, 1994): for example the flexor digitorum profundus muscle has a definite long-latency response (Day et al. 1991) whereas the flexor carpi radialis does not (Rothwell et al. 1991).

Recordings from single motor units showed that the firing probability recovered at conditioning-test intervals of about 75-100 ms, consistent with the findings of Miles et al. (1995).

Though the test responses recovered at similar conditioning- test intervals for surface and single-unit recordings, surface test responses showed a relative inhibition, whereas single units underwent an absolute inhibition for about 50 ms after conditioning. The difference could depend on the different level of contraction used in surface and single-unit recordings. At the higher contraction level used in surface recordings, the increased synaptic input to motoneurones decreases the depth of the average AHP, thus making a larger fraction of motoneurones responsive to the second stimulus. Indeed, the size of the test H-reflex response was proportional to the level of background voluntary contraction (Fig. 3).

Finally, paired masseteric stimuli at selected conditioning- test intervals, elicited a facilitation of the test silent period. This finding contrasts with the observation that paired mixed-nerve stimuli (ulnar nerve) at comparable intervals leave the hand-muscle silent period unchanged (Bertasi et al. 2000). Presumably, in the mixed-nerve experiment the late inhibition induced by cutaneous afferents hindered the shorter-lasting AHP-induced effects, or the difference lies in the peculiar physiological properties of trigeminal motoneurones.

Interactions with other brainstem reflexes mediated by Aβ afferents

Whereas reflex interactions between Aβ and Aδ cutaneous afferents have been studied in the human trigeminal system (Berardelli et al. 1985; Cruccu & Romaniello, 1998), scanty data are available on the interactions between muscle and non-muscle afferents. Existing knowledge on Ia trigeminal interactions shows only that stimulation of the perioral cutaneous nerves inhibits the jaw-jerk evoked by chin taps (a response mediated by Ia afferents) (Godaux & Desmedt, 1975b).

The experiments we report here extend the existing knowledge, first by showing that the cutaneous trigeminal input strongly inhibits the H-reflex. Electrical or mechanical stimulation of the perioral region during ongoing voluntary contraction of jaw-closing muscles evokes two silent periods (or exteroceptive suppressions): the first mediated by an oligosynaptic pontine circuit and the second by a polysynaptic bulbopontine circuit (Godaux & Desmedt, 1975b; Miles & Turker, 1987; Cruccu & Ongerboer de Visser, 1999). In cats, both circuits are thought to exert postsynaptic inhibition on trigeminal motoneurones (Kidokoro et al. 1968; Nakamura, 1980). The inhibitory action of the cutaneous input on trigeminal motoneurones intervenes in the reflex control of mastication and jaw movements during speech. We found no difference between the inhibitory effect of mental nerve stimulation on voluntary contraction or on the H-reflex (Fig. 5). Most important, we found no extra-effects suggesting the existence of presynaptic inhibitory mechanisms. In their experiments, Godaux & Desmedt (1975b) found that the jaw jerk underwent intense inhibition. But, being unable to trigger the jaw jerk with a hand-held hammer, they certainly could not measure either small extra-effects or the precise timing of this inhibition. Our findings indicate that whatever the excitatory input (i.e. corticobulbar or Ia input), the cutaneous input inhibits the trigeminal motoneurones similarly.

Second, a novel finding is the facilitatory effect exerted by the Ia masseteric input on the R1 response of the blink reflex. Clinical-electrophysiological correlations and experiments in cats indicate that R1 is mediated through an oligosynaptic circuit in the pons (Kimura et al. 1970).

Masseteric nerve stimulation induced the maximum R1 facilitation when we delivered the conditioning stimulus 2 ms after the test stimulus. Given the mean R1 latency of 11.5 ms in our subjects and the reported estimated conduction time of 5 ms from the facial motoneurone to the muscle (Möller & Jannetta, 1985; Schriefer et al. 1988), conduction from the supraorbital foramen to the facial motonerones should take 6.5 ms, including passage through interneurones and synaptic times (Cruccu & Bowsher, 1986). The mean H-reflex latency in our subjects was 5 ms; the estimated time taken to travel along the efferent arc (from the trigeminal motoneurones to the temporal muscle) is 2.8 ms (Cruccu, 1986). This leaves 2.2 ms for afferent conduction (including synaptic times). According to these calculations the Ia input reaches the trigeminal motoneurones 4.3 ms before the supraorbital input reaches the facial motoneurones. Hence, the afferent volley elicited by a masseteric stimulus delivered 2 ms after the supraorbital stimulus would reach the brainstem motoneurones approximately 2-3 ms earlier than the supraorbital volley. Although this extra-delay does not exclude a direct monosynaptic connection between trigeminal Ia afferents and facial motoneurones, it favours interneuronal connections.

Support for interneuronal connections comes from evidence that masseteric Ia afferents project onto interneurones of the trigeminal subnucleus oralis (Matesz, 1981) which, in turn, projects onto the facial motor nucleus (Pinganaud et al. 1999). Thus anatomical data would fit with an oligosynaptic connection. Whatever the mechanism, our observation generally indicates that in the human brainstem the excitatory effects of Ia- trigeminal input spread to involve other motor nuclei. This spreading is of interest because muscles innervated by facial nerve have no muscle spindles and hence no Ia afferents (Poppele, 1993).

Functional and clinical significance

Apart from their usefulness in basic neurophysiological research, the recovery cycles reported in this study provide a simple method for indirectly estimating the average AHP in human jaw-closing motoneurones. AHP reflects several features of the somatic and dendritic motoneuronal membrane. Indirect estimation of the AHP in jaw-closing motoneurones could be useful in testing drug actions. Serotonin, for example, exerts a powerful modulation of medium AHP duration in rat motoneurones (Talley et al. 1997). Testing recovery cycles would also provide pathophysiological information in diseases (such as for example amyotrophic lateral sclerosis) that primarily affect motoneurones.

The interaction of masseteric Ia input with other reflex pathways in the brainstem suggests that multiple pathways involving various cranial motoneuronal pools and different afferents integrate within the brainstem, thus accounting for the behavioural complexity of craniofacial movements. The heteronymous facilitation of Ia input on facial motoneurones deserves further study in patients with movement disorders that concomitantly involve the masticatory and facial muscles.

Acknowledgments

We wish to thank Dr Laura Bertolasi for her scientific contribution. This study was partly supported by the MURST (Ministero dell'Universitá e Ricerca Scientifica e Tecnologica, Roma).

References

  1. Berardelli A, Cruccu G, Manfredi M, Rothwell JC, Day BL, Marsden CD. The corneal reflex and the R2 component of the blink reflex. Neurology. 1985;35:797–801. doi: 10.1212/wnl.35.6.797. [DOI] [PubMed] [Google Scholar]
  2. Bertasi V, Bertolasi L, Frasson E, Priori A. The excitability of human cortical inhibitory circuits responsible for the muscle silent period after transcranial brain stimulation. Experimental Brain Research. 2000;132:384–389. doi: 10.1007/s002210000352. [DOI] [PubMed] [Google Scholar]
  3. Bonte B, Linden RW, Scott BJ, van Steenberghe D. Role of periodontal mechanoreceptors in evoking reflexes in the jaw-closing muscles of the cat. Journal of Physiology. 1993;465:581–594. doi: 10.1113/jphysiol.1993.sp019694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Calvin WH, Schwindt PC. Steps in production of motoneuron spikes during rhythmic firing. Journal of Neurophysiology. 1972;35:297–310. doi: 10.1152/jn.1972.35.3.297. [DOI] [PubMed] [Google Scholar]
  5. Coombs JS, Eccles JC, Fatt P. The electrical properties of the motoneuronal membrane. Journal of Physiology. 1955;130:291–325. doi: 10.1113/jphysiol.1955.sp005411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cruccu G. Intracranial stimulation of the trigeminal nerve in man. I. Direct motor responses. Journal of Neurology, Neurosurgery and Psychiatry. 1986;49:411–418. doi: 10.1136/jnnp.49.4.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cruccu G, Berardelli A, Inghilleri M, Manfredi M. Functional organization of the trigeminal motor system in man. A neurophysiological study. Brain. 1989;112:1333–1350. doi: 10.1093/brain/112.5.1333. [DOI] [PubMed] [Google Scholar]
  8. Cruccu G, Bowsher D. Intracranial stimulation of the trigeminal nerve in man. II. Reflex responses. Journal of Neurology, Neurosurgery and Psychiatry. 1986;49:419–427. doi: 10.1136/jnnp.49.4.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cruccu G, Ongerboer de Visser BW. The jaw reflexes. The International Federation of Clinical Neurophysiology. Electroencephalography and Clinical Neurophysiology Supplement. 1999;52:243–247. [PubMed] [Google Scholar]
  10. Cruccu G, Romaniello A. Jaw-opening reflex after CO2 laser stimulation of the perioral region in man. Experimental Brain Research. 1998;118:564–568. doi: 10.1007/s002210050312. [DOI] [PubMed] [Google Scholar]
  11. Darian-Smith I. The trigeminal system. In: Iggo A, editor. Handbook of Sensory Physiology. Vol. 2. Berlin: Springer; 1973. pp. 271–315. [Google Scholar]
  12. Day BL, Riescher H, Struppler A, Rothwell JC, Marsden CD. Changes in response to magnetic and electric stimulation of the motor cortex following muscle stretch in man. Journal of Physiology. 1991;433:41–58. doi: 10.1113/jphysiol.1991.sp018413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. De Laat A. Reflexes elicitable in jaw muscles and their role during jaw function and dysfunction: a review of the literature. Part I: Receptors associated with the masticatory system. Cranio. 1987;5:139–151. doi: 10.1080/08869634.1987.11678184. [DOI] [PubMed] [Google Scholar]
  14. Godaux E, Desmedt JE. Human masseter muscle: H and tendon reflexes. Archives of Neurology. 1975a;32:229–234. doi: 10.1001/archneur.1975.00490460045005. [DOI] [PubMed] [Google Scholar]
  15. Godaux E, Desmedt JE. Exteroceptive suppression and motor control of the masseter and temporalis muscles in normal man. Brain Research. 1975b;85:447–458. doi: 10.1016/0006-8993(75)90819-7. [DOI] [PubMed] [Google Scholar]
  16. Goldberg LJ. Excitatory and inhibitory effects of lingual nerve stimulation on reflexes controlling the activity of masseteric motoneurones. Brain Reserach. 1972;39:95–108. doi: 10.1016/0006-8993(72)90787-1. [DOI] [PubMed] [Google Scholar]
  17. Goldberg LJ, Nakamura Y. Production of primary afferent depolarization in group Ia fibers from the masseter muscle by stimulation of trigeminal cutaneous afferents. Brain Research. 1977;134:561–567. doi: 10.1016/0006-8993(77)90831-9. [DOI] [PubMed] [Google Scholar]
  18. Gustafsson B. Afterhyperpolarization and the control of repetitive firing in spinal motoneurones of the cat. Acta Physiologica Scandinavica Supplement. 1974;416:5–47. [PubMed] [Google Scholar]
  19. Kidokoro Y, Kubota K, Shuto S, Sumino R. Reflex organization of cat masticatory muscles. Journal of Neurophysiology. 1968;31:695–708. doi: 10.1152/jn.1968.31.5.695. [DOI] [PubMed] [Google Scholar]
  20. Kimura J, Rodnitzky RL, Van Allen WM. Electrodiagnostic study of the trigeminal nerve. Orbicularis oculi reflex and masseter reflex in trigeminal neuralgia, paratrigeminal syndrome and other lesions of the trigeminal nerve. Neurology. 1970;20:574–583. doi: 10.1212/wnl.20.6.574. [DOI] [PubMed] [Google Scholar]
  21. Kobayashi M, Inoue T, Matsuo R, Masuda Y, Hidaka O, Kang Y, Morimoto T. Role of calcium conductances on spike afterpotentials in rat trigeminal motoneurones. Journal of Neurophysiology. 1997;77:3273–3283. doi: 10.1152/jn.1997.77.6.3273. [DOI] [PubMed] [Google Scholar]
  22. Inoue T, Itoh S, Kobayashi M, Kang Y, Matsuo R, Wakisaka S, Morimoto T. Serotonergic modulation of the hyperpolarizing spike afterpotential in rat jaw-closing motoneurones by PKA and PKC. Journal of Neurophysiology. 1999;82:626–637. doi: 10.1152/jn.1999.82.2.626. [DOI] [PubMed] [Google Scholar]
  23. Ito M, Oshima T. Temporal summation of hyperpolarization following a motoneuronal spike. Nature. 1962;195:910–911. [Google Scholar]
  24. Lobbezoo F, van der Glas HW, Buchner R, van der Bilt A, Bosman F. Jaw-jerk reflex activity in relation to various clenching tasks in man. Experimental Brain Research. 1993;93:139–147. doi: 10.1007/BF00227788. [DOI] [PubMed] [Google Scholar]
  25. Lorente De NÒ R. Vestibulo-ocular reflex arc. Archives of Neurology and Psychiatry. 1933;30:245–291. [Google Scholar]
  26. Lund JP, Richmond FJ, Touloumis C, Patry Y, Lamarre Y. The distribution of Golgi tendon organs and muscle spindles in masseter and temporalis muscles of the cat. Neuroscience. 1978;3:259–270. doi: 10.1016/0306-4522(78)90107-0. [DOI] [PubMed] [Google Scholar]
  27. Macaluso G, De Laat A. H-reflexes in masseter and temporalis muscle in man. Experimental Brain Research. 1995;107:315–320. doi: 10.1007/BF00230051. [DOI] [PubMed] [Google Scholar]
  28. Macaluso GM, Pavesi G, De Laat A. Heteronymous H-reflex in temporal muscle motor units. Journal of Dental Research. 1998;77:1960–1964. doi: 10.1177/00220345980770120201. [DOI] [PubMed] [Google Scholar]
  29. Martin JW, Panneton WM. Organization of sensory neurones to muscles of mastication in the cat. Neuroscience Letters. 1986;70:336–341. doi: 10.1016/0304-3940(86)90575-6. [DOI] [PubMed] [Google Scholar]
  30. Matesz C. Peripheral and central distribution of fibres of the mesencephalic trigeminal root in the rat. Neuroscience Letters. 1981;27:13–17. doi: 10.1016/0304-3940(81)90198-1. [DOI] [PubMed] [Google Scholar]
  31. Merton PA. The silent period in a muscle of the human hand. Journal of Physiology. 1951;114:183–198. doi: 10.1113/jphysiol.1951.sp004610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Miles TS. Estimating post-synaptic potentials in tonically discharging human motoneurones. Journal of Neuroscience Methods. 1997;74:167–174. doi: 10.1016/s0165-0270(97)02247-4. [DOI] [PubMed] [Google Scholar]
  33. Miles TS, Poliakov AV, Nordstrom MA. Responses of human masseter motor units to stretch. Journal of Physiology. 1995;483:251–264. doi: 10.1113/jphysiol.1995.sp020582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Miles TS, Turker KS. Decomposition of the human electromyogramme in an inhibitory reflex. Experimental Brain Research. 1987;65:337–342. doi: 10.1007/BF00236306. [DOI] [PubMed] [Google Scholar]
  35. Møller AR, Jannetta PJ. Hemifacial spasm: results of electrophysiologic recording during microvascular decompression operations. Neurology. 1985;35:969–974. doi: 10.1212/wnl.35.7.969. [DOI] [PubMed] [Google Scholar]
  36. Nakamura Y. Brainstem neuronal mechanisms controlling the trigeminal motoneuron activity. In: Desmesdt JE, editor. Spinal and Supraspinal Mechanisms of Voluntary Motor Control and Locomotion. Progress in Clinical Neurophysiology. Vol. 8. Basel: Karger; 1980. pp. 181–202. [Google Scholar]
  37. Nishimori T, Sera M, Suemune S, Yoshida A, Tsuru K, Tsuiki Y, Akisaka T, Okamoto T, Dateoka Y, Shigenaga Y. The distribution of muscle primary afferents from the masseter nerve to the trigeminal sensory nuclei. Brain Research. 1986;372:375–381. doi: 10.1016/0006-8993(86)91148-0. [DOI] [PubMed] [Google Scholar]
  38. Pinganaud G, Bernat I, Buisseret P, Buisseret-Delmas C. Trigeminal projections to hypoglossal and facial motor nuclei in the rat. Journal of Comparative Neurology. 1999;415:91–104. doi: 10.1002/(sici)1096-9861(19991206)415:1<91::aid-cne7>3.0.co;2-a. [DOI] [PubMed] [Google Scholar]
  39. Poppele RE. The muscle spindle. In: Dyck PJ, Thomas PK, editors. Peripheral Neuropathy. 3. Vol. 1. Philadelphia: W. B. Saunders; 1993. pp. 121–140. [Google Scholar]
  40. Priori A, Berardelli A, Inghilleri M, Pedace F, Giovannelli M, Manfredi M. Electrical stimulation over muscle tendons in humans. Evidence favouring presynaptic inhibition of Ia fibres due to activation of group III tendon afferents. Brain. 1998a;121:373–380. doi: 10.1093/brain/121.2.373. [DOI] [PubMed] [Google Scholar]
  41. Priori A, Berardelli A, Mercuri B, Manfredi M. Physiological effect produced by botulinum toxin treatment of upper limb dystonia. Changes in reciprocal inhibition between forearm muscles. Brain. 1995;118:801–807. doi: 10.1093/brain/118.3.801. [DOI] [PubMed] [Google Scholar]
  42. Priori A, Truini A, Cruccu G. The excitability of heteronymous trigeminal Ia-motoneurone connection: an indirect estimate of the after-hyperpolarization. Journal of Physiology. 1998b;513.P:33P. [Google Scholar]
  43. Rothwell JC. Control of Human Voluntary Movements. 2. London: Chapmann & Hall; 1994. [Google Scholar]
  44. Rothwell JC, Colebatch JC, Britton TC, Priori A, Thompson PD, Day BL, Marsden CD. Physiological studies in a patient with mirror movements and agenesis of the corpus callosum. Journal of Physiology. 1991;438.P:34P. [Google Scholar]
  45. Schriefer TN, Mills KR, Murray NMF, Hess CW. Evaluation of proximal facial nerve conduction by transcranial magnetic stimulation. Journal of Neurology, Neurosurgery and Psychiatry. 1988;51:60–66. doi: 10.1136/jnnp.51.1.60. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Svensson P, De Laat A, Graven-Nielsen T, Arendt-Nielsen L, Macaluso GM. Effect of clenching levels on heteronymous H-reflex in human temporalis muscle. Experimental Brain Research. 1998;126:467–472. doi: 10.1007/s002210050754. [DOI] [PubMed] [Google Scholar]
  47. Talley EM, Sadr NN, Bayliss DA. Postnatal development of serotonergic innervation, 5-HT1A receptor expression, and 5-HT responses in rat motoneurones. Journal of Neuroscience. 1997;17:4473–4485. doi: 10.1523/JNEUROSCI.17-11-04473.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Turker KS, Brodin P, Miles TS. Reflex responses of motor units in human masseter muscle to mechanical stimulation of a tooth. Experimental Brain Research. 1994;100:307–315. doi: 10.1007/BF00227200. [DOI] [PubMed] [Google Scholar]
  49. Zytnicki D, Lafleur J, Horcholle-Bossavit G, Lamy F, Jami J. Reduction of Ib autogenetic inhibition in motoneurones during contractions on an ankle extensor muscle in the cat. Journal of Neurophysiology. 1990;64:1380–1389. doi: 10.1152/jn.1990.64.5.1380. [DOI] [PubMed] [Google Scholar]

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