Presynaptic inhibition, EPSP amplitude, and motor-unit type in triceps surae motoneurons in the cat

1983 ◽  
Vol 49 (4) ◽  
pp. 922-931 ◽  
Author(s):  
J. E. Zengel ◽  
S. A. Reid ◽  
G. W. Sypert ◽  
J. B. Munson

1. Composite group Ia excitatory postsynaptic potentials (EPSPs) produced by heteronymous nerve stimulation were recorded from triceps surae motoneurons of barbiturate-anesthetized cats. Motoneuron rheobase, input resistance, and axonal conduction velocity were measured, and motor units were classified on the basis of the mechanical responses of their muscle units. 2. The amplitude of EPSPs recorded from 33 medial gastrocnemius (MG) motoneurons ranged from 0.6 to 4.3 mV. The mean EPSP amplitude differed among the major MG motor-unit types, increasing in the order fast twitch, fast fatiguing (FF); fast twitch, fatigue resistant (FR); slow twitch, fatigue resistant (S) (FF less than FR less than S). The amplitude of EPSPs recorded from 15 soleus motoneurons ranged from 0.3 to 3.4 mV, with a mean of 1.4 mV. 3. Presynaptic inhibition of EPSPs was produced by trains of conditioning volleys in the posterior biceps-semitendinosus (PBST) nerve. In 33 MG cells PBST conditioning stimulation reduced the amplitude of EPSPs by 11-50%, with a mean inhibition of 27%. The amplitude of EPSPs in 15 soleus motoneurons was decreased by 5-84%, with a mean inhibition of 37%. 4. When the magnitude of presynaptic inhibition was expressed as percent inhibition, there was no relation between presynaptic inhibition and either motor-unit type or the amplitude of the EPSP. However, when presynaptic inhibition was expressed as the absolute amount of inhibition in millivolts, the magnitude of inhibition was highly correlated with EPSP amplitude both across the entire triceps surae population (MG, lateral gastrocnemius, soleus) as well as within each muscle population. This correlation was also significant within the MG FF and FR motor-unit populations. 5. We conclude that EPSP amplitude and not motor-unit type is the major determinant of the magnitude of presynaptic inhibition. However, because of the effect of motor-unit type on EPSP amplitude, the net effect is that presynaptic inhibition increases in the order FF less than FR less than S.

1986 ◽  
Vol 55 (5) ◽  
pp. 947-965 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson

This study tested the hypothesis that functional connection to muscle is necessary for expression of normal motoneuron electrical properties. Also examined was the time course of self-reinnervation. Properties of individual medial gastrocnemius (MG) motor units were examined following section and reanastomosis of the MG nerve. Stages examined were 3-5 wk (prior to reinnervation, no-re), 5-6 wk (low-re), 9-10 wk (med-re), and 9 mo (long-re, preceding paper) after nerve section. Motor units were classified on the basis of their mechanical response as type fast twitch, fast fatiguing (FF), fast twitch with intermediate fatigue resistance (FI), fast twitch, fatigue resistant (FR), or slow twitch, fatigue resistant (S) (11, 24). Motoneuron electrical properties were measured. Muscle fibers were classified using histochemical methods as type fast glycolytic (FG), fast oxidative glycolytic (FOG), or slow oxidative (SO) (60). Prior to functional reinnervation, MG motoneurons exhibited increased input resistance, decreased rheobase, decreased rheobase/input resistance, and decreased axonal conduction velocity. There was no change in mean afterhyperpolarization (AHP) half-decay time. Normal relationships between motoneuron electrical properties were lost. These data are consistent with dedifferentiation of motoneuron properties following axotomy (35, 47). At 5-6 wk after reanastomosis, motor-unit tensions were small, and motoneuron membrane electrical properties were unchanged from the no-re stage. There were no differences in motoneuron electrical properties between cells that elicited muscle contraction and those that did not. Motor-unit types were first recognizable at the med-re stage. The proportions of fast and slow motor units were similar to normal MG. Within the fast units, there were fewer type-FF units and more type-FI and type-FR units than normal, reflecting a general increase in fatigue resistance at this stage. Neither motoneuron membrane electrical properties nor muscle contractile properties had reached normal values, although both were changed in that direction from the low-re stage. Normal relationships between muscle properties, between motoneuron properties, and between motoneuron and muscle properties were re-established. The correspondence between motor-unit type and motoneuron type was similar to normal or 9 mo reinnervated MG. Muscle-unit tetanic tensions became larger with time after reinnervation. Most of the increase in muscle tension beyond the med-re stage could be accounted for by increase in muscle fiber area. There was an increased proportion of SO muscle fibers observed in the med-re muscles, as at the long-re stage.(ABSTRACT TRUNCATED AT 400 WORDS)


1986 ◽  
Vol 55 (5) ◽  
pp. 931-946 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson

This work tested whether the membrane electrical properties of cat motoneurons, the contractile properties of their muscle units, and the normal relationships among them would be restored 9 mo after section and resuture of their muscle nerve. Properties of medial gastrocnemius (MG) motor units were examined 9 mo following section and resuture of the MG nerve in adult cats. Motoneuron electrical properties and muscle-unit contractile properties were measured. Motor units were classified on the basis of their contractile properties as type fast twitch, fast fatiguing (FF), fast twitch with intermediate fatigue resistance (FI), fast twitch, fatigue resistant (FR), or slow twitch, fatigue resistant (S) (8, 20). Muscle fibers were classified as type fast glycolytic (FG), fast oxidative glycolytic (FOG), or slow oxidative (SO) on the basis of histochemical staining for myosin adenosine triphosphatase, nicotinamide adenine dinucleotide diaphorase, and alpha-glycerophosphate dehydrogenase (48). Following 9 mo self-reinnervation, the proportions of each motor-unit type were the same as in normal control animals. Motoneuron membrane electrical properties [axonal conduction velocity, afterhyperpolarization (AHP) half-decay time, rheobase, and input resistance] also returned to control levels in those motoneurons that made functional reconnection with the muscle (as determined by ability to elicit measurable tension). The relationships among motoneuron electrical properties were normal in motoneurons making functional reconnection. Approximately 10% of MG motoneurons sampled did not elicit muscle contraction. These cells' membrane electrical properties were different from those that did elicit muscle contraction. Contractile speed and fatigue resistance of reinnervated muscle units had recovered to control levels at 9 mo postoperation. Force generation did not recover fully in type-FF units. The reduced tensions were apparently due to failure of recovery of FG muscle fiber area. Following reinnervation, relationships between motoneuron electrical and muscle-unit contractile properties were similar to controls. This was reflected in a degree of correspondence between motor-unit type and motoneuron type similar to normal units (84 vs. 86%, as defined by Ref. 61). There was a significantly increased proportion of type-SO muscle fibers and a decrease in the fast muscle fibers (especially type FOG) in 9 mo reinnervated MG. Together with the unchanged proportions of motor-unit types, this led to an estimate of average innervation ratios being increased in type-S motor units and decreased in type-FR units.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 71 (4) ◽  
pp. 1480-1490 ◽  
Author(s):  
S. Hochman ◽  
D. A. McCrea

1. In this paper we continue an examination of changes in composite Ia excitatory postsynaptic potentials (EPSPs) in ankle extensor motoneurons after 6-wk (L1-L2) spinal cordotomy. The ratio of rheobase to input resistance was used to divide motoneurons into three groups approximating fast-fatigable (FF), fast fatigue-resistant (FR), and slow (S) motor units in barbiturate-anesthetized cats. Homonymous monosynaptic Ia EPSPs evoked by low-strength [1.2 times threshold (T)] electrical stimulation and heteronymous EPSPs evoked by 2T stimulation were compared between groups of motoneurons in unlesioned and chronic spinal preparations. 2. The distribution of motor unit types of triceps surae and plantaris (PL) motoneurons according to the present classification scheme agrees well with that obtained elsewhere using mechanical typing. Chronic spinalization resulted in an increased proportion of type FF motoneurons in PL and type FR motoneurons in lateral gastrocnemius (LG) motoneurons. There was a numeric but insignificant increase in the proportion of fast medial gastrocnemius motor units. 3. Membrane time constant (tau m) and estimated total cell capacitance were significantly reduced in FF and S motoneurons in chronic spinal preparations. FF motoneurons from chronic spinal animals also had a reduced afterhyperpolarization duration. Mean values of membrane electrical properties in FR motoneurons were unaltered after spinalization. 4. Homonymous Ia EPSP changes after chronic spinalization occurred preferentially in type FR and S motor units. Amplitudes increased 69% in type FR and 38% type S motor units but were unchanged in type FF units. Furthermore, the amplitudes of heteronymous Ia EPSPs in type FF and S units in the chronic spinal preparation were almost double those in unlesioned preparations. 5. Homonymous EPSP 10-90% rise times decreased 25% in type FR motor units and 15% in type S motor units and were unchanged in type FF motor units. Homonymous EPSP half-width decreased in all three motoneuron groups. Normalization of EPSP rise time and half-width to tau m reduced the difference between EPSP shape indexes in unlesioned and chronic spinal preparations in type FF and S motoneurons but less so in type FR motoneurons. Normalized EPSP shape indexes in some type FR units were shorter after chronic spinalization than any in unlesioned preparations. 6. The increased amplitude and decreased rise time of Ia EPSPs in type FR motoneurons after spinalization occurred without changes in the electrical properties of type FR motor units.(ABSTRACT TRUNCATED AT 400 WORDS)


1985 ◽  
Vol 53 (5) ◽  
pp. 1323-1344 ◽  
Author(s):  
J. E. Zengel ◽  
S. A. Reid ◽  
G. W. Sypert ◽  
J. B. Munson

Membrane electrical properties [time constant, action potential afterhyperpolarization (AHP), rheobase, input resistance, and axonal conduction velocity] were measured in motoneurons of cat medial gastrocnemius (MG) motor units. Motor units were classified on the basis of their mechanical responses as fast twitch, fast fatiguing (FF); fast twitch with intermediate fatigue resistance (FI); fast twitch, fatigue resistant (FR); or slow twitch, fatigue resistant (S; 11, 22). Motoneuron membrane time constant, estimated from the voltage response at the onset or termination of long (50-100 ms) current pulses and corrected for voltage-response nonlinearities (32), was found to differ significantly among the major motor-unit types, increasing in the order FF less than FR less than S. Afterhyperpolarization magnitude, half-decay time, and duration were all significantly greater for the fast (FF + FI + FR) versus the slow (S) motor units. The AHP half-decay time was correlated with muscle unit twitch time over the entire motoneuron population and within the type S motor-unit population. There was no significant correlation between twitch time and AHP half-decay time among the types FF and FR motor-unit populations. In agreement with previous studies, we found a significant difference in both rheobase and input resistance among the major motor-unit types, with rheobase increasing in the order S less than FR less than FF and input resistance decreasing in that order (S greater than FR greater than FF). The differences in input resistance were present both before and after correcting for voltage-response nonlinearities (32). Also in agreement with previous studies, the mean axonal conduction velocity was significantly faster among the fast (FF + FI + and FR) compared with the slow (S) motor units. These data were used to examine the properties alone to determine motor-unit type, which has traditionally been defined on the basis of the muscle unit's mechanical properties (11, 22). We used a discriminant analysis program to classify 73 mechanically typed motor units for which we had measures of rheobase, input resistance, membrane time constant, and AHP half-decay time. This model was able to properly classify 71 of the 73 motor units of this data set, indicating that the motor units of this data set could be grouped into three categories representing the three major motor-unit types (FF, FR, and S) on the basis of their rheobase, input resistance, membrane time constant, and AHP half-decay time.(ABSTRACT TRUNCATED AT 400 WORDS)


1987 ◽  
Vol 57 (4) ◽  
pp. 1227-1245 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson

We tested whether the muscle innervated may influence the expression of motoneuron electrical properties. Properties of individual motor units were examined following cross-reinnervation (X-reinnervation) of cat lateral gastrocnemius (LG) and soleus muscles by the medial gastrocnemius (MG) nerve. We examined animals at two postoperative times: 9-10 wk (medX) and 9-11 mo (longX). For comparison, normal LG and soleus motoneuron properties were also studied. Motor units were classified on the basis of their contractile responses as fast contracting fatigable, fast intermediate fast contracting fatigue resistant, and slow types FF, FI, FR, or S, respectively) (9, 21). Motoneuron electrical properties (rheobase, input resistance, axonal conduction velocity, afterhyperpolarization) were measured. After 9-11 mo, MG motoneurons that innervated LG muscle showed recovery of electrical properties similar to self-regenerated MG motoneurons. The relationships between motoneuron electrical properties were largely similar to self-regenerated MG. For MG motoneurons that innervated LG, motoneuron type (65) predicted motor-unit type in 74% of cases. LongX-soleus motoneurons differed from longX-LG motoneurons or self-regenerated MG motoneurons in mean values for motoneuron electrical properties. The differences in overall means reflected the predominance of type S motor units. The relationships between motoneuron electrical properties were also different than in self-regenerated MG motoneurons. In all cases, the alterations were in the direction of properties of type S units, and the relationship between normal soleus motoneurons and their muscle units. Within motor-unit types, the mean values were typical for that type in self-regenerated MG. Motoneuron type (65) was a fairly strong predictor of motor-unit type in longX soleus. MG motoneurons that innervated soleus displayed altered values for axonal conduction velocity, rheobase, and input resistance, which could indicate incomplete recovery from the axotomized state. However, although mean afterhyperpolarization (AHP) half-decay time was unaltered by axotomy (25), this parameter was significantly lengthened in MG motoneurons that innervated soleus muscle. There were, however, individual motoneuron-muscle-unit mismatches, which suggested that longer mean AHP half-decay time may also be due to incomplete recovery of a subpopulation of motoneurons. Those MG motoneurons able to specify soleus muscle-fiber type exhibited motoneuron electrical properties typical of that same motoneuron type in self-regenerated MG.(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)


1996 ◽  
Vol 75 (1) ◽  
pp. 38-50 ◽  
Author(s):  
K. E. Tansey ◽  
B. R. Botterman

1. The aim of this study was to examine the nature of motoneuron firing-rate modulation in type-identified motor units during smoothly graded contractions of the cat medial gastrocnemius (MG) muscle evoked by stimulation of the mesencephalic locomotor region (MLR). Motoneuron discharge patterns, firing rates, and the extent of firing-rate modulation in individual units were studied, as was the extent of concomitant changes in firing rates within pairs of simultaneously active units. 2. In 21 pairs of simultaneously active motor units, studied during 41 evoked contractions, the motoneurons' discharge rates and patterns were measured by processing the cells' recorded action potentials through windowing devices and storing their timing in computer memory. Once recruited, most motoneurons increased their firing rates over a limited range of increasing muscle tension and then maintained a fairly constant firing rate as muscle force continued to rise. Most motoneurons also decreased their firing rates over a slightly larger, but still limited, range of declining muscle force before they were derecruited. Although this was the most common discharge pattern recorded, several other interesting patterns were also seen. 3. The mean firing rate for slow twitch (type S) motor units (27.8 imp/s, 5,092 activations) was found to be significantly different from the mean firing rate for fast twitch (type F) motor units (48.4 imp/s, 11,272 activations; Student's t-test, P < 0.001). There was no significant difference between the mean firing rates of fast twitch, fatigue-resistant (type FR) and fast twitch, fatigable (type FF) motor units. When the relationship between motoneuron firing rate and whole-muscle force was analyzed, it was noted that, in general, smaller, lower threshold motor units began firing at lower rates and reached lower peak firing rates than did larger, higher threshold motor units. These results confirm both earlier experimental observations and predictions made by other investigators on the basis of computer simulations of the cat MG motor pool, but are in contrast to motor-unit discharge behavior recorded in some human motor-unit studies. 4. The extent of concomitant changes in firing rate within pairs of simultaneously active motor units was examined to estimate the extent of simultaneous motoneuron firing-rate modulation across the motoneuron pool. A smoothed (5 point sliding average) version of the two motoneurons' instantaneous firing rates was plotted against each other, and the slope and statistical significance of the relationship was determined. In 16 motor-unit pairs, the slope of the motoneurons' firing-rate relationship was significantly distinct from 0. Parallel firing-rate modulation (< 10-fold difference in firing rate change reflected by a slope of > 0.1) was noted only in pairs containing motor units of like physiological type and then only if they were of similar recruitment threshold. 5. Other investigators have demonstrated that changes in a motoneuron's "steady-state" firing rate predictably reflect changes in the amount of effective synaptic current that cell is receiving. The finding in the present study of limited parallel firing-rate modulation between simultaneously active motoneurons would suggest that changes in the synaptic drive to the various motoneurons of the pool is unevenly distributed. This finding, in addition to the findings of orderly motor-unit recruitment and the relationship between motor-unit recruitment threshold and motoneuron firing rate, cannot be adequately accommodated for by the existing models of the synaptic organization in motoneuron pools. Therefore a new model of the synaptic organization within the motoneuron pool has been proposed.


1987 ◽  
Vol 57 (4) ◽  
pp. 1210-1226 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson

This study addresses two questions: is reinnervation of mammalian skeletal muscle selective with respect to motor-unit type? And to what degree may muscle-unit contractile properties be determined by the motoneuron? Properties of individual motor units were examined following cross-reinnervation (X-reinnervation) of lateral gastrocnemius (LG) and soleus muscles by the medial gastrocnemius (MG) nerve in the cat. We examined animals at two postoperative times: 9-10 wk (medX) and 9-11 mo (longX). For comparison, properties of normal LG and soleus motor units were studied. Motor units were classified on the basis of their contractile response as fast contracting fatigable, fast intermediate, fast contracting fatigue resistant, or slow (types FF, FI, FR, or S, respectively) (13,29). Muscle fibers were classified on the basis of histochemical properties as fast glycolytic, fast oxidative glycolytic, or slow oxidative (types FG, FOG, or SO, respectively) (61). Reinnervation of LG and soleus was not selective with respect to motor-unit type. Both muscles were innervated by a full complement of MG motoneuron types, apparently in normal MG proportions. MG motoneurons determined LG muscle fibers' properties to a similar degree as reinnervated MG muscle fibers. In contrast, soleus muscle fibers "resisted" the influence of MG motoneurons. Thus, although longX-reinnervated LG muscle (longX LG) had a motor-unit type distribution similar to normal or self-reinnervated MG, longX soleus contained predominantly type S motor units. Overall mean values for muscle-unit contractile properties reflected this motor-unit type distribution. Muscle units in longX LG and longX soleus had contractile properties typical of the same motor-unit type in normal LG or soleus, respectively. Motor-unit types were recognizable at 10 wk X-reinnervation, although muscle-unit tensions were lower than after 10 mo. The proportions of fast and slow motor units in medX LG were similar to longX LG, although a greater proportion of fast units were resistant to fatigue at 10 wk. There were fewer fast units in medX soleus than longX soleus, which suggested that motor-unit type conversion or innervation of muscle fibers by fast motoneurons is not complete at 10 wk. We conclude that reinnervation of the LG and soleus muscles by MG motoneurons was not selective with respect to motor-unit type. MG motoneurons determined LG muscle properties to a similar degree as self-reinnervated MG muscle fibers. Soleus muscle fibers resisted the influence of MG motoneurons, representing a limit to neural determination of muscle properties.


1996 ◽  
Vol 75 (1) ◽  
pp. 26-37 ◽  
Author(s):  
K. E. Tansey ◽  
B. R. Botterman

1. The recruitment order of 64 pairs of motor units, comprising 21 type-identified units, was studied during centrally evoked muscle contractions of the cat medial gastrocnemius (MG) muscle in an unanesthetized, high decerebrate preparation. Motor units were functionally isolated within the MG nerve by intra-axonal (or intramyelin) penetration with conventional glass microelectrodes. 2. Graded stimulation of the mesencephalic locomotor region (MLR) was used to evoke smoothly graded contractions, which under favorable conditions was estimated to reach 40% of maximum tetanic tension of the MG muscle. With this method of activation, 100% of slow twitch (type S) units, 95% of fast twitch, fatigue-resistant (type FR) units, 86% of fast twitch, fatigue-intermediate (type FI) units, and 49% of fast twitch, fatigable (type FF) units studied were recruited. 3. Motoneuron size as estimated by axonal conduction velocity (CV) was correlated with muscle-unit size as estimated by maximum tetanic tension (Po). Although the correlation between these properties was significant among type S and FR units, no significant correlation was found for these properties among type FI and FF units. 4. Motor-unit recruitment was ordered by physiological type (S > F, 100% of pairs; S > FR > FI > FF, 93% of pairs). Although none of the motor-unit properties studied predicted recruitment order perfectly, motor-unit recruitment was found to proceed by increasing Po (89% of pairs), decreasing contraction time (79% of pairs), decreasing fatigue index (80% of pairs), and increasing CV (76% of pairs). These percentages were significantly different from random (i.e., 50%). Statistically, all four motor-unit properties were equivalent in predicting recruitment order. These results are similar to those reported by other investigators for motor-unit recruitment order evoked from other supraspinal centers, as well as from peripheral sites. 5. When, however, motor-unit recruitment within pairs of motor units containing two fast-twitch (type F) units was examined, Po was a significantly better predictor of recruitment order than CV (85% vs. 52% of pairs). One explanation for this observation is that the correlation between Po and CV is high among type S, type FR units, and possibly among the lower-tension type FF units, but not among the remaining higher-tension type FF units. 6. The reproducibility of recruitment order in multiple contractions was investigated in 16 motor-unit pairs. Recruitment order was found to be variable in only three motor-unit pairs, all of which contained units of similar physiological type and recruitment threshold. 7. Analysis of recruitment order by pair-wise testing confirms the general conclusion reached in human studies that the muscle force level at recruitment for a motor unit is highly correlated with its strength. As an additional confirmation, the whole-muscle force level at recruitment for 41 units was measured in a series of contractions in which the rate of rise of muscle tension was limited to rates < 1,000 g/s. For these contractions, a significant correlation was found between muscle tension at recruitment and motor-unit Po.


1981 ◽  
Vol 46 (6) ◽  
pp. 1326-1338 ◽  
Author(s):  
J. W. Fleshman ◽  
J. B. Munson ◽  
G. W. Sypert ◽  
W. A. Friedman

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