Evidence for Strong Synaptic Coupling Between Single Tactile Afferents From the Sole of the Foot and Motoneurons Supplying Leg Muscles

2005 ◽  
Vol 94 (6) ◽  
pp. 3795-3804 ◽  
Author(s):  
James B. Fallon ◽  
Leah R. Bent ◽  
Penelope A. McNulty ◽  
Vaughan G. Macefield

It has been known for some time that populations of cutaneous and muscle afferents can provide short-latency facilitation of motoneuron pools. Recently, it has been shown that the input from individual low-threshold mechanoreceptors in the glabrous skin of the hand can modulate ongoing activity in muscles acting on the fingers via spinally mediated pathways. We have extended this work to examine whether such strong synaptic coupling exists between tactile afferents in the sole of the foot and motoneurons supplying muscles that act about the ankle. We recorded from 53 low-threshold mechanoreceptors in the glabrous skin of the foot via microelectrodes inserted percutaneously into the tibial nerve of awake human subjects. Reflex modulation of ongoing whole muscle electromyography (EMG) was observed for each of the four classes of low-threshold cutaneous mechanoreceptors (17 of 21 rapidly adapting type I; 2 of 4 rapidly adapting type II; 7 of 18 slowly adapting type I; and 4 of 10 slowly adapting type II). Reflex modulation of the firing probability in single motor units (5 of 11) was also observed. These results indicate that strong synaptic coupling between tactile afferents and spinal motoneurons is not a specialization of the hand and emphasizes the potential importance of cutaneous inputs from the sole of the foot in the control of gait and posture.

1994 ◽  
Vol 72 (3) ◽  
pp. 1127-1139 ◽  
Author(s):  
A. Nambu ◽  
R. Llinas

1. We investigated the electrical properties of globus pallidus neurons intracellularly using brain slices from adult guinea pigs. Three types of neurons were identified according to their intrinsic electrophysiological properties. 2. Type I neurons (59%) were silent at the resting membrane level (-65 +/- 10 mV, mean +/- SD) and generated a burst of spikes, with strong accommodation, to depolarizing current injection. Calcium-dependent low-frequency (1-8 Hz) membrane oscillations were often elicited by membrane depolarization (-53 +/- 8 mV). A low-threshold calcium conductance and an A-current were also identified. The mean input resistance of this neuronal type was 70 +/- 22 M omega. 3. Type II neurons (37%) fired spontaneously at the resting membrane level (-59 +/- 9 mV). Their repetitive firing (< or = 200 Hz) was very sensitive to the amplitude of injected current and showed weak accommodation. Sodium-dependent high-frequency (20-100 Hz) subthreshold membrane oscillations were often elicited by membrane depolarization. This neuronal type demonstrated a low-threshold calcium spike and had the highest input resistance (134 +/- 62 M omega) of the three neuron types. 4. Type III neurons (4%) did not fire spontaneously at the resting membrane level (-73 +/- 5 mV). Their action potentials were characterized by a long duration (2.3 +/- 0.6 ms). Repetitive firing elicited by depolarizing current injection showed weak or no accommodation. This neuronal type had an A-current and showed the lowest input resistance (52 +/- 35 M omega) of the three neuron types. 5. Stimulation of the caudoputamen evoked inhibitory postsynaptic potentials (IPSPs) in Type I and II neurons. In Type II neurons the IPSPs were usually followed by rebound firing. Excitatory postsynaptic potentials and antidromic responses were also elicited in some Type I and II neurons. The estimated conduction velocity of the striopallidal projection was < 1 m/s (Type I neurons, 0.49 +/- 0.37 m/s; Type II neurons, 0.33 +/- 0.13 m/s).


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.


1988 ◽  
Vol 60 (6) ◽  
pp. 2138-2151 ◽  
Author(s):  
A. E. Olha ◽  
B. J. Jasmin ◽  
R. N. Michel ◽  
P. F. Gardiner

1. Rat plantaris muscles were subjected to chronic overload by the surgical removal of the soleus and most of the gastrocnemius muscles. Twelve to 16 wk later whole muscle and motor unit (ventral root dissection technique) contractile properties as well as histochemistry were determined. 2. Motor units were categorized as fast, fatigable (FF), fast, intermediate fatigue-resistant (FI), fast, fatigue-resistant (FR), and slow (S) based on contractile characteristics. Muscle fibers were identified as type I and type II according to myofibrillar ATPase staining. 3. Whole muscles demonstrated increases in wet weight, tetanic force, proportion of type I fibers, and mean cross-sectional areas of both type I and II fibers, as a result of chronic overload. 4. Tetanic tension increased by the same relative magnitude in all motor units whereas twitch tension remained unchanged. A significant change in the proportions of the motor unit types occurred in overloaded muscles, such that the latter contained higher proportions of FF and S units, and lower proportions of FI and FR units, than normal muscles. 5. The fatigue profile of a composite constructed from a summation of motor unit responses revealed that the overloaded plantaris displayed fatigue resistance similar to that of the normal plantaris for a given absolute force output. 6. Glycogen-depleted fibers of hypertrophied single motor units demonstrated uniform myofibrillar ATPase and SDH staining characteristics suggesting that metabolic adaptations among fibers of the same unit were similar after 12-16 wk of overload. 7. The finding that overload caused a uniform increase in the tetanic strength of all motor units, whereas alterations in fatigue resistance varied in degree and direction among unit types, demonstrate that these two properties are not controlled in parallel in this model. The smallest units maintain or even increase their fatigue resistance during the hypertrophic process, whereas high threshold units actually decrease in fatigue resistance.


1932 ◽  
Vol 55 (6) ◽  
pp. 853-865 ◽  
Author(s):  
Maxwell Finland ◽  
W. D. Sutliff

The blood of 63 human subjects selected because of the absence of recent infections, was studied for its content of specific antibodies against virulent strains of Types I, II, and III pneumococci before and after intracutaneous injections of minute amounts of pneumococcus products. The simultaneous injection of the specific polysaccharides of all three types of pneumococci and of proteins and autolysates derived from Types I and II pneumococci was followed by the appearance or increase of pneumococcidal power in the whole defibrinated blood and, in most instances, by the appearance of mouse-protective antibodies and agglutinins for one or more types. A single intracutaneous injection of 0.01 mg. of the protein-free type-specific polysaccharide of either Type I, Type II, or Type III pneumococci or 4 similar daily injections was followed, in most of 29 subjects, by the appearance of antibodies against the homologous, but not against the heterologous type pneumococci. Some subjects showed a simultaneous lowering of a preexisting pneumococcidal power for heterologous or homologous types. A single intracutaneous injection of O.1 mg. of pneumococcus protein in 13 individuals was not followed by the appearance of specific antibodies to any appreciable degree. Single intracutaneous injections of small amounts of autolysates derived from virulent strains of Type I, II, or III pneumococci were followed in 11 subjects by a more or less general rise in the pneumococcidal power with the appearance of homologous type agglutinins and protective antibodies in about one-third of the subjects.


1993 ◽  
Vol 69 (4) ◽  
pp. 1005-1008 ◽  
Author(s):  
C. J. Heckman ◽  
M. D. Binder

1. As a human subject slowly increases the amount of force exerted by a muscle, the discharge rates of low-threshold motor units saturate at a rather low level, whereas higher-threshold units continue to be recruited and undergo increases in their discharge rates. The presently known intrinsic properties of motor units do not produce this "rate limiting." 2. Using computer simulations of a model motoneuron pool, we tested the hypothesis that rate limiting can be accounted for on the basis of the known distributions of synaptic input from different sources. The properties of the simulated motor units and their synaptic inputs were based as closely as possible on the available experimental data. A variety of simulated synaptic input organizations were applied to the pool, and the resulting outputs were compared with the data on rate limiting in human subjects. 3. We found that the data on rate limiting in human subjects greatly constrained the possible organizations of characterized synaptic input systems. Only when the synaptic organization included a gradual "crossover" between two specific types of input systems could the human data be accurately reproduced. Low input/output levels relied on a system organized like the monosynaptic Ia input, which produces greater effective synaptic currents in low- than in high-threshold motor units. Above a sharply defined crossover level, all further increases in output were produced by a system organized like the oligosynaptic rubrospinal input, which generates the opposite pattern.


1993 ◽  
Vol 74 (6) ◽  
pp. 2718-2723 ◽  
Author(s):  
W. A. Whitelaw ◽  
K. P. Rimmer ◽  
H. S. Sun

Recruitment order of individual motor units in the early part of inspiration in parasternal intercostal muscles was observed in normal human subjects during wakefulness and non-rapid-eye-movement sleep. Electromyograms from bipolar fine wire intramuscular electrodes were recorded while the subjects lay supine in a sleep laboratory, and sleep stage was determined by polysomnography. From wakefulness to sleep there were numerous examples of shifts in order of recruitment among the low threshold units of early inspiration. There were corresponding shifts in the order of derecruitment of these units. Analysis of frequency of firing of units also suggested that the levels of excitatory input to one unit of a pair could be altered relative to the level of input of the other one. The data imply that there are at least minor differences in distribution of excitatory inputs from various sources among motoneurons of this muscle pool.


1994 ◽  
Vol 76 (6) ◽  
pp. 2411-2419 ◽  
Author(s):  
S. J. Garland ◽  
R. M. Enoka ◽  
L. P. Serrano ◽  
G. A. Robinson

The activity of 50 single motor units was recorded in the biceps brachii muscle of human subjects while they performed submaximal isometric elbow flexion contractions that were sustained to induce fatigue. The purposes of this study were to examine the influence of fatigue on motor unit threshold force and to determine the relationship between the threshold force of recruitment and the initial interimpulse interval on the discharge rates of single motor units during a fatiguing contraction. The discharge rate of most motor units that were active from the beginning of the contraction declined during the fatiguing contraction, whereas the discharge rates of most newly recruited units were either constant or increased slightly. The absolute threshold forces of recruitment and derecruitment decreased, and the variability of interimpulse intervals increased after the fatigue task. The change in motor unit discharge rate during the fatigue task was related to the initial rate, but the direction of the change in discharge rate could not be predicted from the threshold force of recruitment or the variability in the interimpulse intervals. The discharge rate of most motor units declined despite an increase in the excitatory drive to the motoneuron pool during the fatigue task.


1990 ◽  
Vol 68 (1) ◽  
pp. 26-34 ◽  
Author(s):  
M. A. Nordstrom ◽  
T. S. Miles

The spike-triggered averaging technique was used to determine the time course and extent of fatigue of single motor unit twitches in the human masseter. This is the first report of a fatigue test having been applied to masseter motor units in either animals or humans. The human masseter was found to be comprised predominantly of fast-twitch motor units with a broad spectrum of fatigability. Very few physiological type S units were found, despite histochemical evidence for a substantial population of type I fibers in the masseter. In addition, there was no significant correlation between fatigability and either twitch amplitude or contractile speed in the motor units studied. The latter observations are consistent with the unusual histological features of the masseter. Comparison with other human fatigue data suggests that the extent of fatigue in the present population of masseter motor units after approximately 3,000 activations is similar to that reported for populations of units in first dorsal interosseous and medial gastrocnemius.


1981 ◽  
Vol 24 (4) ◽  
pp. 567-576 ◽  
Author(s):  
Anne Smith ◽  
Gerald N. Zimmermann ◽  
Paul J. Abbas

Single motor units were recorded with intramuscular electrodes in sites selected to isolate units of the mentalis muscles of two human subjects. Order of recruitment of three groups of motor units was analyzed during repetition of syllables. Within each group motor units showed variable patterns of recruitment over repeated utterances. These recruitment patterns of labial motor units and the patterns observed by Sussman et al. in a jaw opening muscle are used to illustrate issues critical to interpretation of recruitment patterns of motor units active during speech. From extant data, inferences about the size of the motor units active cannot be made; however, the variability of recruitment patterns has significance for hypotheses about the underlying mechanisms of recruitment. Discussion includes the question of the size of motor units as inferred from action potential amplitude, differences in methodology between experiments in speech and those often used to interpret them, and the extent to which it is possible to isolate motor units from a single muscle in electromyography of facial muscles.


1975 ◽  
Vol 38 (4) ◽  
pp. 933-946 ◽  
Author(s):  
H. J. Freund ◽  
H. J. Budingen ◽  
V. Dietz

1. Microelectrode recordings from single motor units of the first dorsal interosseus and the extensor indicis muscles of normal human subjects were studied during voluntary, isometric contractions. The conduction velocity of the nerve fiber innervating the muscle unit was used as an estimator of the size of the motoneuron. 2. During slowly increasing contractions, the units were recruited at force levels which were closely correlated to conduction velocity. The units associated with low conduction velocity were recruited first, those with high conduction velocity, last. 3. If small, stepwise force increments were used instead of slowly, continuously increasing contractions, the units were first activated during the steps and became inactive during the subsequent plateaus. If higher steady-force levels were reached, the activity was maintained also during the plateaus. This steady force, where a unit remained continuously active independent of the rate of rise of tension, represents its tonic threshold. 4. The tonic threshold is positively correlated with conduction velocity, as is the threshold force of recruitment. As a consequence, high-threshold units have a large force range below tonic threshold where they can only be transiently activated, whereas low-threshold units have a large physiological force range above tonic threshold where they operate tonically. The phasic or tonic appearance of discharge pattern reflects quantitative differences in tonic threshold between units of different size. All units examined could be activated phasically (below) and tonically (above tonic threshold). No evidence was found indicating the existence of two qualitatively different classes of units corresponding to a tonic and phasic type, although both muscles investigated consist of about equal numbers of type I and type II muscle fibers. 5. The change in firing rate per unit force was inversely related to conduction velocity: the slower conducting units showed larger changes in firing rate per unit force than faster conducting units. This corresponds to the larger excitability of the smaller units indicated by their earlier recruitment. 6. The data of this study are consistent with the hypothesis that the functional characteristics of human motoneurons are determined by the graded excitability of motoneurons according to size.


Sign in / Sign up

Export Citation Format

Share Document