Sustained Firing of Alpha and Gamma Hind Limb Motoneurons Induced by Stimulation of the Pudendal Nerve

2002 ◽  
Vol 88 (6) ◽  
pp. 3232-3242 ◽  
Author(s):  
Rafael Cueva-Rolón ◽  
Rodolfo Delgado-Lezama ◽  
J. G. Raya ◽  
M. Raya ◽  
R. Tecuanhuey ◽  
...  

Axons from receptors in the cat vaginal wall run in the sensory pudendal nerve (SPN), and brief (<10 s) vaginal probing (VP) in the decerebrate cat produces a long-lasting (>1 min) contraction of the triceps surae (TS) muscles. The aim of the present project was to find out whether brief SPN stimulation also produces sustained TS response and, eventually, to study the mechanisms involved in it. Decerebrate female cats were used. In some cats, TS electromyography (EMG) and tension response were recorded; stimulation of left SPN with single or repetitive trains of shocks produced a bilateral TS response that outlasted the stimulus >1 min as VP did. In paralyzed cats (pancuronium; Panc), intracellular recordings were made from hind limb motoneurons (MNs). SPN stimulation produced a depolarization ≤5 s long and occasional cell firing only lasting <2.5 s; this is in contrast with the prolonged TS postdischarge seen in nonparalyzed cats. If MNs were depolarized below the firing threshold by current injection, about half of them showed bistable firing that could last several minutes in response to SPN train. It is suggested that MNs might hyperpolarize after Panc injection. Before Panc injection, SPN train produced long-lasting (>1 min) electroneurographic (ENG) postdischarge in a small filament of the medial gastrocnemius (MG) nerve; the MG EMG postdischarge was also recorded. Large spikes (LS) and small spikes (SS) were distinguished in the ENG. During the postdischarge, LS frequency and the integrated EMG activity correlated well ( r > 0.9); no correlation was found between SS and EMG. After Panc injection, LS postdischarge was absent but the SS postdischarge remained. LS followed by EMG potential were also evoked by brief TS stretch (reflex LS); single shocks to SPN only elicited SS that were not followed by EMG potential. It is concluded that alpha axons and gamma axons produced LS and SS, respectively, and that SPN activates gamma axons. It is proposed that, in the nonparalyzed cats, the stimulation of SPN with trains of shocks might cause an increase in the afferent inflow from muscle spindles to alpha MNs through the sustained firing of gamma MNs. The increased excitatory inflow would depolarize alpha MNs and allow bistable MN firing; Panc would decrease this inflow by blocking transmission to the spindle fibers.

1987 ◽  
Vol 57 (2) ◽  
pp. 574-595 ◽  
Author(s):  
S. E. Grill ◽  
W. Z. Rymer

The discharge of spindle afferents from medial gastrocnemius and soleus muscles was recorded in the decerebrated cat preparation, under isometric conditions and during ramp and hold stretches. Motor output was varied systematically by manual stimulation of the contralateral hindlimb. Twenty-six of 34 afferents showed response patterns consistent with enhancement of dynamic and/or static fusimotor input with increasing muscle force. To establish whether force-related fusimotor effects were mediated at least partly by beta-input, beta-innervation to these same spindles was sought, using a ventral root stimulation protocol. Twenty-three of the 34 afferents were shown to receive beta-innervation, which was most often static in type. For two measures of fusimotor action, the slope of the afferent dynamic rate-length relation and the discharge rate measured during the last portion of ramp stretch, significant increases in the measure, which paralleled increases in muscle force, made it statistically more likely that the afferent received beta-innervation. Our measures did not successfully predict the type of beta-input (beta-static or beta-dynamic). Procaine block of gamma-fibers produced substantial reductions in fusimotor effect in seven spindle afferents (although modest residual fusimotor effects were detectable for 3/7 afferents). The severity of these reductions indicates that beta-action probably requires concurrent gamma-input to the spindle in order to be effective. In support of this possibility, the fusimotor effects of electrical stimulation of single beta-fibers were greatly reduced for five out of six afferents during procaine block of gamma-fibers, compared with the beta-effects recorded when modest levels of spontaneous gamma-activity were present. We conclude that beta-innervation to muscle spindles of triceps surae is common and that this innervation exerts significant fusimotor effects. It appears likely that beta-motoneurons are able to produce both static and dynamic effects above extrafusal threshold, but that the actions require on-going gamma-activity in order to be effective.


2004 ◽  
Vol 92 (1) ◽  
pp. 387-394 ◽  
Author(s):  
J. Guadalupe Raya ◽  
Alberto Ramírez ◽  
E. J. Muñoz-Martínez

The sensory pudendal nerve (SPN) was stimulated in decerebrate female cats. Spikes of single Ia muscle spindle afferents from the medial gastrocnemius (MG) muscle were recorded in dorsal root filaments. Electroneurography (ENG) was recorded in a cut nerve filament to the MG muscle; MG electromyography (EMG) was also recorded. Single shock to SPN induced discharges of small ENG spikes (SS) with similar amplitude to that of gamma spikes elicited by ventral root stimulation. Thus SS were identified as gamma spikes. The latency of the gamma discharge was ∼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.


1990 ◽  
Vol 63 (6) ◽  
pp. 1467-1476 ◽  
Author(s):  
S. H. Duenas ◽  
G. E. Loeb ◽  
W. B. Marks

1. In normal and thalamic walking cats electrical stimulation of muscle nerves via chronically implanted electrodes produced electromyographic (EMG) and neurographic responses that were modulated in amplitude depending on the phase of the step cycle. These responses were examined for possible indications of effects of primary afferent depolarization (PAD) during stepping. 2. Monosynaptic reflexes (MSRs) produced by stimulating the lateral gastrocnemius (LG) and medial gastrocnemius (MG) nerves were recorded as EMGs in MG or LG muscles during treadmill locomotion in normal cats. These heteronymous MSR responses were greatest during the stance (extensor) phase. 3. In the same animals, after decerebration, similar modulation of the heteronymous ankle extensor MSRs occurred during spontaneous locomotion with the use of the same stimulus and recording sites. 4. In both normal and thalamic cats the amplitude of neurogram responses recorded from LG or MG nerve after stimulation of the other muscle nerve varied with phase of stepping but did not parallel the variations of the MSR measured as EMG amplitude in the same muscle. The nerve responses were largest during the flexion phase of the step cycle and had a calculated central latency of 0.6-1.0 ms. These are interpreted as arising from antidromic activity in large-caliber afferent nerve fibers (i.e., dorsal root reflexes). 5. Spontaneous antidromic activity in severed L7 dorsal rootlet fibers to triceps surae was observed in the thalamic cats during episodes of locomotion and was closely correlated with flexion phase EMG activity in semitendinosus, a bifunctional muscle. 6. In decerebrate cats, dorsal root reflexes (DRRs) in severed filaments of L4-L7 dorsal roots were produced by stimulation of saphenous and posterior tibial nerves. These DRRs were always smaller during locomotion than during rest and were smallest during the flexion phase. 7. The short-latency antidromic activity produced in muscle nerves by stimulating heteronymous muscle nerves thus appears to be a DRR produced in Group I terminal arborizations that are depolarized close to threshold during the flexion phase. Such PAD could account for changes in the MSR that do not always parallel the levels of recruitment of the motor pools as manifest by background EMG amplitude.


1992 ◽  
Vol 67 (5) ◽  
pp. 1375-1384 ◽  
Author(s):  
A. M. Aniss ◽  
S. C. Gandevia ◽  
D. Burke

1. Reflex responses were elicited in muscles that act at the ankle by electrical stimulation of low-threshold afferents from the foot in human subjects who were reclining supine. During steady voluntary contractions, stimulus trains (5 pulses at 300 Hz) were delivered at two intensities to the sural nerve (1.2-4.0 times sensory threshold) or to the posterior tibial nerve (1.1-3.0 times motor threshold for the intrinsic muscles of the foot). Electromyographic (EMG) recordings were made from tibialis anterior (TA), peroneus longus (PL), soleus (SOL), medial gastrocnemius (MG), and lateral gastrocnemius (LG) muscles by the use of intramuscular wire electrodes. 2. As assessed by averages of rectified EMG, stimulation of the sural or posterior tibial nerves at nonpainful levels evoked a complex oscillation with onset latencies as early as 40 ms and lasting up to 200 ms in each muscle. The most common initial responses in TA were a decrease in EMG activity at an onset latency of 54 ms for sural stimuli, and an increase at an onset latency of 49 ms for posterior tibial stimuli. The response of PL to stimulation of the two nerves began with a strong facilitation of 44 ms (sural) and 49 ms (posterior tibial). With SOL, stimulation of both nerves produced early inhibition beginning at 45 and 50 ms, respectively. With both LG and MG, sural stimuli produced an early facilitation at 52-53 ms. However, posterior tibial stimuli produced different initial responses in these two muscles: facilitation in LG at 50 ms and inhibition in MG at 51 ms. 3. Perstimulus time histograms of the discharge of 61 single motor units revealed generally similar reflex responses as in multiunit EMG. However, different reflex components were not equally apparent in the responses of different single motor units: an individual motor unit could respond slightly differently with a change in stimulus intensity or background contraction level. The multiunit EMG record represents a global average that does not necessarily depict the precise pattern of all motor units contributing to the average. 4. When subjects stood erect without support and with eyes closed, reflex patterns were seen only in active muscles, and the patterns were similar to those in the reclining posture. 5. It is concluded that afferents from mechanoreceptors in the sole of the foot have multisynaptic reflex connections with the motoneuron pools innervating the muscles that act at the ankle. When the muscles are active in standing or walking, cutaneous feedback may play a role in modulating motoneuron output and thereby contribute to stabilization of stance and gait.


1991 ◽  
Vol 66 (4) ◽  
pp. 1127-1138 ◽  
Author(s):  
T. C. Cope ◽  
B. D. Clark

1. Recruitment order was studied in pairs of motor units of the medial gastrocnemius (MG) muscle of decerebrate cats with the use of dual microelectrode recording from intact ventral root filaments. Excitation was provided by stretch of MG, stretch of synergists [lateral gastrocnemius (LG), plantaris (PL), and soleus (SOL) muscles] or electrical stimulation of the caudal cutaneous sural (CCS) nerve. Motor units were characterized by axonal conduction velocity (CV), tetanic tension (Pmax), twitch contraction time (CT), and fatigue index (FI). 2. Consistent with the recruitment pattern described by others, most often in relation to either CV or Pmax, the first unit of a pair to be recruited by MG stretch was typically the one with the lower CV and Pmax, and the higher FI and CT. The proportion of pairs that agreed in rank order of each property and recruitment order was as follows: for CT, 94%; for CV, 87%; for Pmax, 84%; and for FI, 75%. With a single marginal exception (CT vs. FI), no motor-unit property proved to be significantly better than the others at predicting recruitment (G test; P greater than 0.05). 3. In all 11 tested pairs containing one slow (type S) and one fast (type F) unit, the S was more easily recruited by stretch. Type F units divided into groups with high (type FR), low (type FF), and intermediate (type FInt) values for FI were recruited in order from FR to FInt to FF in 8/11 pairs. Thus our findings were similar to earlier demonstrations that recruitment proceeds in order by type. 4. Stretch of MG synergists usually recruited units in the same order as MG stretch. In two S-S pairs, recruitment order was switched with synergist stretch. 5. Stimulation of the CCS nerve was generally excitatory to the MG units sampled. Most unit pairs were recruited by CCS stimulation in the same order as by MG stretch, but, for 6 of 39 pairs, CCS stimulation switched the order produced by stretch. Thus, whereas sural afferent input can preferentially excite some units over others as suggested by Kanda et al., that effect is not widespread or selective for unit type under these conditions. 6. Assuming that all MG motor units cooperate as a single functional pool in homonymous stretch reflexes, we support others in concluding that a motoneuron's recruitment threshold is not strictly determined by its size. However, our data do not distinguish other schemes that predict recruitment order more accurately than the size principle.(ABSTRACT TRUNCATED AT 400 WORDS)


1993 ◽  
Vol 70 (4) ◽  
pp. 1585-1592 ◽  
Author(s):  
J. S. Carp

1. Homonymous and heteronymous monosynaptic composite excitatory postsynaptic potentials (EPSPs) were evaluated by intracellular recordings from 89 motoneurons innervating triceps surae (n = 59) and more distal (n = 30) muscles in 14 pentobarbital-anesthetized monkeys (Macaca nemestrina). 2. Homonymous EPSPs were found in all motoneurons tested. The mean values +/- SD for maximum EPSP amplitude of triceps surae motoneurons were 2.5 +/- 1.3, 1.8 +/- 1.3 and 4.5 +/- 2.0 mV for medial gastrocnemius, lateral gastrocnemius, and soleus motoneurons, respectively. Heteronymous EPSPs were almost always smaller than their corresponding homonymous EPSPs. 3. Triceps surae EPSP amplitude was larger in motoneurons with higher input resistance. However, this relationship was weak, suggesting that factors related to input resistance play a limited role in determining the magnitude of the EPSP. 4. The mean ratio +/- SD of the amplitude of the EPSP elicited by combined stimulation of all triceps surae nerves to the amplitude of the algebraic sum of the three individual EPSPs was 0.95 +/- 0.05. This ratio was greater in motoneurons with lower rheobase. 5. Some patterns of synaptic connectivity in the macaque are consistent with previously reported differences between primates and cat (e.g., heteronymous EPSPs elicited by medial gastrocnemius nerve stimulation in soleus motoneurons are small in macaque and other primates but large in cat). However, no overall pattern emerges from a comparison of the similarities and differences in EPSPs among species in which they have been studied (i.e., macaque, baboon, and cat). That is, there are no two species in which EPSP properties are consistently similar to each other, but different from those of the third species.(ABSTRACT TRUNCATED AT 250 WORDS)


2012 ◽  
Vol 108 (11) ◽  
pp. 3034-3042 ◽  
Author(s):  
D. A. E. Bolton ◽  
J. E. Misiaszek

Electrical stimulation of the lateral gastrocnemius-soleus (LGS) nerve at group I afferent strength leads to adaptations in the amplitude and timing of extensor muscle activity during walking in the decerebrate cat. Such afferent feedback in the stance leg might result from a delay in stance onset of the opposite leg. Concomitant adaptations in hip abductor and adductor activity would then be expected to maintain lateral stability and balance until the opposite leg is able to support the body. As many hip abductors and adductors are also hip extensors, we hypothesized that stimulation of the LGS nerve at group I afferent strength would produce increased activation and prolonged burst duration in hip abductor and adductor muscles in the premammillary decerebrate walking cat. LGS nerve stimulation during the extensor phase of the locomotor cycle consistently increased burst amplitude of the gluteus medius and adductor femoris muscles, but not pectineus or gracilis. In addition, LGS stimulation prolonged the burst duration of both gluteus medius and adductor femoris. Unexpectedly, long-duration LGS stimulus trains resulted in two distinct outcomes on the hip abductor and adductor bursting pattern: 1) a change of burst duration and timing similar to medial gastrocnemius; or 2) to continue rhythmically bursting uninterrupted. These results indicate that activation of muscle afferents from ankle extensors contributes to the regulation of activity of some hip abductor and adductor muscles, but not all. These results have implications for understanding the neural control of stability during locomotion, as well as the organization of spinal locomotor networks.


1975 ◽  
Vol 91 (1) ◽  
pp. 151-155 ◽  
Author(s):  
Steven L. Wolf ◽  
William D. Letbetter

1984 ◽  
Vol 52 (2) ◽  
pp. 228-243 ◽  
Author(s):  
P. R. Murphy ◽  
R. B. Stein ◽  
J. Taylor

To determine the role of gamma-motoneurons in the control of locomotion, we isolated single units from nerves to triceps surae muscles in the premammillary cat. The limb used for recording was largely denervated, except for the muscles of interest, and fixed in place, while the other three limbs walked on a treadmill. One type of gamma-motoneuron (13 units) had a high impulse rate at rest, which changed little on average during walking, but was deeply modulated with each step (phasically modulated gamma-motoneuron or gamma p). Another type (19 units) had a low impulse rate at rest, which increased greatly on average during walking, but was not highly modulated with each step (tonically modulated gamma-motoneuron or gamma t). Peak gamma p rates generally occurred after peak EMG, often near the peak of tension. In contrast, peak gamma t activity generally preceded peak electromyograms (EMG). No significant difference was observed in conduction velocities for the two types of units. At rest all gamma t units were excited by natural stimulation of the fur over a large part of the body surface, whereas 3 of 11 gamma p units were inhibited. During locomotion the same natural stimuli had no observable effect on either type of unit. By recording in continuity from fine branches of the lateral and medial gastrocnemius nerves and stimulating ventral root filaments in continuity, we identified dynamic and static gamma-motoneurons in terms of their effects on muscle spindle afferents. After cutting the nerve branch distally and other ventral root filaments supplying the muscle, the resting discharge of dynamic and static gamma-motoneurons was recorded and found to correspond to that of the gamma p and gamma t units, respectively. Other evidence is presented for a correspondence between phasically and tonically modulated units and dynamic and static gamma-motoneurons, contrary to some suggestions in the literature.


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