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Alpha Linkage and Persistent Firing of Ia Fibers by Pudendal Nerve Stimulation in the Decerebrate Cat
1Departamento de Fisiología, Biofísica y Neurociencias y Sección de Bioelectrónica and 2Departamento de Ingeniería Eléctrica, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, 07000 México, D.F., Mexico
Submitted 18 November 2003; accepted in final form 11 February 2004
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ABSTRACT |
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15 ms. As expected, the onset of the gamma discharge preceded a discharge of Ia spikes; the time difference between both discharges was 5 ms. After the initial bursts, the Ia and the gamma activities paused during 20–30 ms but later increased again to last 1 s. After the shock, the EMG activity was depressed during 50 ms; later, motor-unit spikes may show transient activation. Thus the onset of the gamma activation preceded the activation of motor units (gamma
alpha link). Trains of shocks (1 or 100 Hz) to SPN induced a sustained increase in the frequency of gamma spikes, Ia spikes, and motor units that outlasted the train by 20–120 s. The sustained firing of Ia fibers might trigger or help to trigger and maintain the response of alpha-motoneurons. |
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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). It was then suggested that this persistent firing might reflect the bistable behavior (bistability) of motoneurons (MNs) that was previously described (Hounsgaard et al. 1984, 1988). Afferent fibers from the vaginal wall run in the sensory branch of the pudendal nerve (SPN) (Cueva-Rolón et al. 1994). Stimulation of this nerve branch with trains of shocks reproduces the motor effects of VP, and in cats that were paralyzed by a curarizing agent, bistable MN firing was elicited. (Cueva-Rolón et al. 2002). This mode of firing, however, was only obtained by depolarizing the MN membrane 2–3 mV below the firing threshold before the SPN was stimulated; at the resting membrane potential, bistable MN firing could not be obtained (Cueva-Rolón et al. 2002; see also Paroschy and Shefchyk 2000). In fact, membrane depolarization below the firing threshold is a condition for the MNs to show bistability (Hounsgaard et al. 1984). It was proposed that in paralyzed cats the MNs membrane potential might be below the voltage needed for bistability (Cueva-Rolón et al. 2002).
In nonparalyzed cats, SPN stimulation induced a sustained postdischarge of axon spikes from both alpha-motoneurons (
-MNs) and gamma-motoneurons (
-MNs) to the medial gastrocnemious muscles (Cueva-Rolón et al. 2002); the response of spikes outlasted that of spikes. Thus the prolonged firing of MNs might induce an equally prolonged discharge of primary muscle spindle afferents that could induce the depolarization of MNs that is needed for bistability. From previous findings two facts can be expected. First, the firing frequency of primary (Ia) muscle spindle afferents should increase in response to SPN stimulation. Second, this increase might outlast the firing of motor units. To test these predictions was an aim of the present experiments. The results show that SPN stimulation causes a several-fold increase in the firing frequency of Ia spikes; this increase may outlast by several seconds the muscle response.
On the other hand, the activation of - and -MNs by a given input is usually referred as - co-activation. In response to SPN stimulation, gamma-axons discharge at a time that the electromyograph (EMG) paused; 50–100 ms later the EMG activity increased. Then the term linkage might be more adequate than - co-activation to describe the initial motor response to SPN stimulation.
This paper contains part of the thesis of J. G. Raya to obtain the degree of Químico, Bacteriólogo y Parasitólogo in the Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, México.
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METHODS |
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The sensory pudendal nerve (SPN) of the left side was dissected in the ischiatic cavity for stimulation. The threshold (T) of SPN to electric stimulation was found by recording the afferent volley at the entrance to the spinal cord of S2 dorsal root. The nerves to the ipsilateral medial gastrocnemius (MG) muscle and lateral gatrocnemius and soleus (LG-Sol) muscles were dissected and kept intact for stimulation, except for a cut, small MG filament used for recording. Silver bipolar hook electrodes were used for both stimulation and recording.
The vertebral column was attached to a frame. The left femur and fibula were stabilized. The Achilles tendon was attached through the calcaneous process to a modified strain-gauge transducer (compliance, 1 mm/2 or 10 kg) (Delgado-Lezama et al. 1997). A lumbar laminectomy was performed and the left dorsal root of the first sacral segment (S1) was exposed but kept intact. In some experiments, the ipsilateral ventral root of the seventh lumbar segment (L7) was also exposed. S1 dorsal root filaments were dissected for recording single spikes of Ia afferents from the MG muscle. In some experiments, filaments of the L7 or S1 ventral root were dissected and stimulated. The nerve-root conduction distance was measured at the end of the experiment. The SPN threshold to electric shocks was found through the recording of the afferent volley at the entrance of the corresponding root (S2 for SPN and S1 for MG and LG-Sol nerves). Data were digitally sampled, stored, and analyzed using Axotape and Axoscope software (Axon Instruments). Continuous records were taken during no more than 40 s because signal digitalization at the acquisition rate of 
10 kHz imposed limits to the acquisition time; using acquisition rates <10 kHz do not sample adequately biphasic spikes lasting 1 ms. In addition, series of unitary Ia spikes acquired at low rate (<10 kHz) but for longer periods are too much compressed for illustration.
At the end of the experiment, the cats were killed by an intravenous overdose of barbiturate.
Window-selected spikes
Single negative-positive (up-and-down) electroneurographic (ENG) or EMG spikes were selected using a software program (UDP) written by one of us (Ramírez) on Matlab (MathWorks). Briefly, two pairs of voltage levels were chosen for each spike: one pair included the negative peak and the other pair included the positive one. Each pair of the voltage levels was separated by 10% of the corresponding peak voltage to allow for spike amplitude fluctuations. The counting of spikes in multiunit recordings has some uncertainty. On one hand, some spikes with similar shape and amplitude might not fit in the window if adding to spikes from other units. On the other hand, different ENG or EMG units might produce spikes with 
10% difference with respect to the amplitude of each component of the selected spike. Thus more than one unit might generate the counted spikes. In spite of uncertainties, the spikes frequency changed importantly by SPN stimulation.
The instantaneous frequency (IF) of unitary (Ia) and multi-unit (gamma and motor unit) spikes was determined automatically using UDP. To find the combined IF of 4–10 pooled ENG or EMG spikes, the window voltage levels were adjusted to include all selected spikes; the smaller selected spike had peaks amplitudes of at least double the noise amplitude. The correlation between Ia spikes and 4–15 pooled gamma spikes and motor-unit spikes was estimated at 0.2- to 1-s consecutive intervals.
Statistical analysis of data
The t-test was used to know if IF distributions before and after SPN stimulation were significantly different. The IF control distribution of Ia fibers appeared to be normally distributed; thus it was assumed that the control IF population was in fact a normal distribution. The t-test gives limited information if it is applied to time series showing large changes in the moving average. A method, single event probability, (SEP) was devised to estimate the probability that single IF values in a test series of spikes (the response) might be included in a given normal distribution (the control IF). The method is based on the properties of the normal distribution: the probability (P) that a given event (x) might be included in the normal distribution z is determined by the mean (µ) and the SD (
). The conversion x P for the standard normal distribution can be found in JMP software program (SAS). If µ is 
0, for x = µ, P = 1 and, for example, if x = µ ± , P = 0.317; x = µ ± 1.5 , P = 0.114; x = µ ± 2, P = 0.0455; x = µ ± 3, P = 0.0027; x = µ ± 4; P = 0.000064. Depending on whether x is larger or smaller than µ, P is associated to increased or decreased IF; this information is not provided by the t-test or any other test that compares samples.
Additional details are given in RESULTS.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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The method used to identify the Ia fibers (n = 12) as well as the general aspects of the fibers response to stimulation of the sensory pudendal nerve (SPN) are shown in Fig. 1. Ten Ia fibers were activated by stimulation of the MG nerve and the LG-Sol nerve activated two other Ia fibers. The conduction velocity between MG or LG-Sol muscles and S1 dorsal root was 92–103 m/s (Fig. 1A); in three fibers, the antidromic Ia spike was followed by early discharges (Cameron et al. 1981; Granit et al. 1959; Hunt and Kuffler 1951). The fibers ceased firing during the muscle twitch evoked by nerve stimulation (Fig. 1B) and showed dynamic response to small (<5 mm) and fast (<1 s) stretch of the muscle (Fig. 1C).
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; see also Cueva-Rolón et al. 1993); the stimulus also induced a sustained increase in the firing rate of Ia spikes (n = 12). The onset of this increase always preceded the muscle response and outlasted it (Fig. 1, D–F). Usually, the motor response to a single train lasted <30 s, and several trains were needed to obtain a longer-lasting response (90 s) (Cueva-Rolón et al. 2002); this was also the case for the Ia response. The response of the Ia fiber outlasted the motor response for several seconds (Fig. 1, D and E) The increase in the firing frequency varied in different Ia fibers and in a single trial may show large up-and-down fluctuations, which were in some cases clearly related to the muscle tension response (Fig. 1, D–F).
The response to SPN stimulation was followed by a period of depression (see following text and Fig. 5C). Several SPN stimuli were applied 20–30 min apart to avoid the response depression that was seen with repetitive trains (unpublished observations). This determined that each Ia fiber was recorded during 3 h; only one to three Ia fibers were studied in each cat.
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0; Fig. 1, E and F). The SEP test indicated that in >95% (100% in 9 of 12 cases) of the individual IF values, the probability of these values to be included in the control distribution also was 0 (see labeled circles on Fig. 1F). All results were analyzed using the t-test and the SEP test (see METHODS); the lowest value (t-test) for the 12 studied fibers was P = 7.14 (10–12).
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As previously described, single shock to SPN evoked a brief discharge (30 ms) of small spikes (SS) in a cut MG filament; the SS latency was 15 ms (Fig. 2, top). It was no clear whether after the initial discharge, the SS and the Ia frequency changed respect to the control frequency. Figure 3, A and B, shows a second increase of both Ia and SS spikes.
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- or 
-MNs. SS were taken as spikes from -MNs (Cueva-Rolón et al. 2002). In three cats, dissected filaments of the L7 or S1 ventral root were stimulated one at the time with single shock. Stimulating some filaments produced large -spikes with conduction velocity (CV) of 86–99 m/s and (or) three to six times smaller spikes with CV of 17–38 m/s (Fig. 3; see the inset at the right side of the ENG tracings). The small spikes were taken as -spikes. The amplitude of -spikes evoked from the spinal root was within the amplitude range of SS evoked by single shock to SPN. This supports further that SS are -spikes.
Spikes from -efferents were recorded in seven cats. Each -efferent fired once or twice 30–60 ms after the shock (Fig. 3A) or fired later. Ia fibers fired two to three spikes at high instantaneous frequency (IF; maximal IF, 240/s) 5–10 ms after the onset of the SS burst. After this discharge the firing paused during 100 ms, which is close to the control inter-spike interval (75–111 ms in Fig. 3B). Later the spike frequency rose again and remained increased with respect to control during 1–3 s (Fig. 3B).
The low firing rate of unitary -spikes did not allow establishing IF correlation with Ia spikes, which fired at much higher rate. Figure 3B show four -spikes (bottom) that were admitted by the software window (see METHODS); the compound IF was obtained (Fig. 3B, 
). Similarities are found between scatter IF diagram for the Ia spikes (
) and the -spikes (). The two initial IF peaks in both diagrams are separated by a phase of relative depression, which is close to the average control interval of Ia spikes (see preceding text). In addition, the frequency of both, Ia spikes and -spikes remained increased after the second peak during 1 s. The increase in frequency of -spikes and Ia spikes varied greatly in different experiments. For example, the maximal IF of Ia spikes varied from 30 to 250/s after single shock. In response to this stimulus, motor units may remain silent, fire only once or fire several times during the next few seconds (Figs. 2A, EMG, and 5, A and B). The discharge of -spikes always preceded the Ia response, which preceded the EMG activation (Fig. 2). This sequence of activation suggests a linkage rather than a - co-activation.
The statistical significance of the increased IF of Ia fiber and units in response to single shock was also estimated (t-test). As shown in Fig. 3B, P 0 for the Ia fiber and P = 0.0078 for the units. The same data were analyzed taking the number of spikes at intervals 200 ms long (Fig. 3C); the P values are different in Fig. 3, B and C, particularly in the case of Ia spikes. This is because the number of values in the samples (Fig. 3C) is much less than in the case of IF values (Fig. 3B). Also, the lower significance of the response as compared with the Ia response (Fig. 3B) might be attributed to the lesser number of values in the samples. Similar results to those shown in Fig. 3 were obtained in two other experiments.
In addition to the t-test, the correlation between the -firing and the Ia firing was also estimated. The correlation coefficient (r) in three experiments was 0.86, 0.89 (Fig. 3C), and 0.94.
Response to train of stimulation
Train of shocks to SPN at 1 Hz elicited a much more prolonged response than single shock did. The frequency of -spikes, Ia spikes, and some motor-unit spikes increased gradually during the stimulus (see 
in Fig. 4, ENG recording), and showed postdischarge, which outlasted the last shock >20 s; other motor-unit spikes of much larger amplitude only fired transiently after the third and subsequent shocks (see 
above the EMG recording of Fig. 4) and did not show postdischarge. The correlation coefficient (r) between the number of -spikes versus Ia spikes (Ia-), Ia spikes versus tonic motor-unit spikes (Ia-mu), and -spikes versus tonic motor-unit spikes (-mu) was determined; spikes from 4 to 10 ENG units and 10 to 12 EMG units were selected separately but added later at intervals of 0.2 or 1 s. In seven analyzed cases, r 0.78 for the three correlations during the period of stimulation at 1 Hz; the higher correlation (r > 0.9, 0.99 in Fig. 4) was found between -spikes and Ia spikes. During the postdischarge, all correlations decreased. The correlation coefficient between the firing of Ia spikes and motor-unit spikes was the lowest (0.32-0.67) taking in consideration the entire response, which may reflect the influence of the mechanical activity of the muscle on Ia fibers (see Fig. 1, D–F).
In two cats, the firing of MG -spikes was compared with the firing of Ia spikes and motor-unit spikes of the Gl-Sol muscles. In the case illustrated in Fig. 5A, two motor units from the soleus muscle showed tonic firing that outlasted the stimulus, but no response of MG motor units was detected, which can be attributed to a lesser excitability of the MG -MNs. However, the response frequency of the frequency diagrams of MG -spikes, LG-Sol Ia spikes, and LG-Sol motor-unit spikes are highly correlated (Fig. 4E); r = 0.87 for -Ia discharge and Ia motor-unit postdischarge, and r = 0.64 for -motor-unit postdischarge. Thus it can be inferred that the response of -efferents is alike in both nerves.
A single shock to SPN produces no motor response or transient firing of one or a few motor units, but trains of stimulation produce a more intense and sustained postdischarge The response of Ia spikes and -spikes to train of stimulation is also more intense and prolonged than the response produced by single shock (Fig. 5B).
After a postdischarge, the motor response was depressed or it could not be produced during the next 15–20 min (see preceding text). The evoked firing of -spikes and Ia spikes was also depressed when the SPN stimulation caused little or no motor response (compare diagrams 5, B and C).
The t-test showed a better use to estimate the statistical significance of IF values when the response is declining to control values. In the experiment that is illustrated in Fig. 5B, the average IF of the control Ia firing was 10.1 ± 1.13 (SD), and the IF average between 25 and 35 s was 11.34 ± 1.37. For these samples, P = 3.57 (10–6). The IF averages of -spikes were 14.69 ± 19.54 and 51.75 ± 127.6 and P = 0.016. IF diagrams are not shown in Fig. 5.
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DISCUSSION |
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-MNs and Ia fibers were initially excited, but -MNs were inhibited as indicated by EMG depression, which also excludes excitation of skeletofusiomotor or -MNs. (Maltenfort and Burke 2003; see also Appelberg et al. 1983a; Wuerker and Henneman 1963). Third, afferent fibers that are originated in the pudendal skin and in the external genitalia induce firing of -MNs to hind limb muscles.
Skin afferents from the cat hind limb produce synaptic effects on -MNs (Johansson and Sojka 1985). A train of stimulation to these afferents accelerates the firing of Ia fibers from hind limb muscles but only during the stimulating period; single shock did not increase significantly the Ia firing (Wuerker and Henemann 1963) or the firing increased during <200 ms (Lewis 1973). In the present project, the Ia response to a single shock prolongs for >1 s, and increased Ia firing outlasts a train of stimulation for several seconds. The difference between previous and present results might be related to the type of preparation. Previous experiments were performed in the spinal or the anesthetized cat.
The activation of -MNs has been frequently inferred from the increase in the firing frequency of Ia fibers (see, for example, Al-Falahe et al. 1990; Cabelguen 1981; Lewis 1973; Perret and Buser 1972; Prochazca and Gorassini 1998; Taylor et al. 2000a; Wuerker and Henneman 1963). In the present results, this inference is supported by the high correlation between the firing of axons from -MNs and of Ia fibers. The -MNs that responded to SPN stimulation might be static, dynamic, or both (see, for example, Mathews 1962; Murphy 2002; Murphy et al. 2002; Taylor et al. 2000b); static -MNs might be involved in the initial increase of the Ia firing, which occurred when the MG muscle was at constant length.
The initial EMG depression and -MNs activation was followed by increased EMG activity. Thus there was not an - co-activation but linkage; the latter might also occur during the cat locomotion (Taylor et al. 2000a). During the sustained afterdischarge, it is not possible to distinguish between - co-activation and linkage. In principle, - co-activation might be provided by spinal circuits capable of self-excitation (positive feedback). However, there is not evidence of this type of circuits in the spinal cord.
A train of stimulation to SPN produces in paralyzed cats a delayed MN depolarization (LD) that may trigger cell firing lasting <2.5 s (Cueva-Rolón et al. 2002). In these cats, -MNs cannot induce contraction of the spindle muscle fibers (Eyzaguirre 1960; Yamamoto et al. 1994). Thus LD does not result from Ia fibers discharge but might be sufficient initiate the motor response in nonparalyzed cats.
Bistable MN firing might explain the sustained motor response. In paralyzed cats, however, bistable firing was induced by SPN stimulation only if the MN was depolarized in advance 2-3 mV below the firing threshold by current injection (Cueva-Rolón et al. 2002); the membrane voltage that is needed to produce the MN bistable behavior is below the firing threshold (Hounsgaard et al. 1984). We propose that the Ia postdischarge is needed for the -MNs to reach the threshold for bistability. The MN depolarization that might be induced by the sustained firing of Ia fibers in nonparalyzed cats would be equivalent to the depolarization that was induced by current injection in paralyzed cats.
The sustained firing of -MNs does not depend on the Ia firing, at least not entirely because it is also produced although in a lesser degree in paralyzed cats (see preceding text). Gamma-MNs might develop plateau potentials and bistable firing as -MNs do (see Cueva Rolón et al. 2002; Hounsgaard et al. 1988;). In addition, a positive feedback with a peripheral component could be brought into play and contribute to the maintenance of -MNs firing. That is, spindle afferents might also depolarize and induce firing in -MNs. Experimental data strongly suggest that both - and -MNs are excited by spindle afferents (Grill and Rymer 1985, 1987). Predictions of spindle models agree with the empirical findings (Maltenfort and Burke 2003; see for review Prochazka and Gorassini 1998). It is unlikely, however, that the increase in Ia firing reported here might activate -MNs. Appelberg et al. (1983a) reported that group I afferents produce little effect in a small proportion of homonymous -MNs, but group II afferents produces autogenetic excitation in 40% of these MNs (Appelberg et al. 1983b). In addition, it cannot be excluded that the sustained Ia firing might activate -MNs (Grill and Rymer 1985, 1987; Maltenfort and Burke 2003). It would be interesting to test whether the stimulation of SPN produces sustained firing of group II afferents and -MNs.
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: E. J. Muñoz-Martínez, Dept. de Fisiologica, Biofisica y Neurosciencias, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, A.P. 14-740. 0700 México D.F., Mexico (E-mail: jmunoz{at}fisio.cinvestav.mx).
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, motor-unit spike. The time scales are in seconds.
