Rheobase, input resistance, and motor-unit type in medial gastrocnemius motoneurons in the cat

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


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)


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)


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.


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)


1978 ◽  
Vol 41 (2) ◽  
pp. 496-508 ◽  
Author(s):  
J. V. Walsh ◽  
R. E. Burke ◽  
W. Z. Rymer ◽  
P. Tsairis

1. Compensatory hypertrophy of the medial gastrocnemius (MG) muscle was produced by denervating or removing its synergists (i.e., the lateral gastrocnemius, soleus, and plantaris muscles) in adult cats. Following survival times of 14-32 wk, intracellular recording and stimulation techniques were used to study the motor-unit population in MG. The data obtained were compared with results from MG motor units in normal unoperated cats of the same body size and weight. 2. Using criteria employed for normal motor units, the units in hypertrophic MG muscles were readily classified into the same groups (types FF, F(int), FR, and S) as in normal MG. There was no detectable difference in the distribution of motor-unit types after hypertrophy. 3. When compared with a normal motor-unit sample, there was a large increase in mean tetanic tension, but no significant change in twitch tension, for each motor-unit type in the hypertrophied muscles. The most marked increase was found among the fatigue-resistant type S and type FR motor units. There was no alteration of twitch contraction times or fatigue resistance in any unit type after hypertrophy. 4. For each motor-unit type, the mean homonymous (MG) group Ia EPSP amplitude was the same in normal and hypertrophic MG populations. There was, however, a significant increase in the average conduction velocity of MG motor axons in the animals with uncomplicated MG synergist removal and maximal MG hypertrophy. 5. On the basis of histochemical staining, muscle fibers from comparable sections of hypertrophic and contralateral (unoperated) MG muscles were presumptively identified as belonging to FF, FR, or S units. There was no significant difference between hypertrophic and contralateral MG muscles in the percentage of each fiber type, although there was some variability in muscle composition from one cat to another. One muscle pair was studied in detail for fiber cross-sectional area. In this cat, with marked hypertrophy by muscle weight, there was a modest increase in the mean fiber areas of histochemical S and FR muscle fibers, but no evident change in FF fibers, on the hypertrophic side. 6. MG motor units were examined in several cats in which synergist removal resulted in scarring and marked limitation of passive ankle mobility, and no evident weight gain in MG. Motor units of all types in these animals showed a decrease in twitch tension and in mean twitch/tetanus ratios, with little alteration in mean tetanic tensions. 7. The main effect of compensatory hypertrophy under the present conditions was a large increase in tetanic tension output from individual motor units due, at least in part, to an increase in fiber cross-sectional area. There was no evidence indicating any "conversion" of motor units or of their muscle fibers from one type to another.


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)


1984 ◽  
Vol 52 (3) ◽  
pp. 410-420 ◽  
Author(s):  
P. Bawa ◽  
M. D. Binder ◽  
P. Ruenzel ◽  
E. Henneman

Motor units of soleus and medial gastrocnemius (MG) muscles were studied in pairs during stretch reflexes in the decerebrate cat to determine the relation between their recruitment orders and axonal conduction velocities. In 97% of soleus pairs, the motor unit with the lower axonal conduction velocity was recruited first. Since the soleus is a homogeneous muscle in the cat, differences in motor-unit type are, therefore, not a sine qua non for orderly recruitment nor is recruitment random within homogeneous populations of motor units, as recently proposed (28). In the medial gastrocnemius, a heterogeneous muscle, the same high correlation (97%) between recruitment sequence and conduction velocity was observed. Thus, the factors that determine recruitment order in heterogeneous muscles are as closely correlated with axonal diameter as they are in homogeneous muscles. Comparison of axonal conduction velocities in our sample of MG units with those in three samples of type-identified MG units studied by other investigators also suggests that motor-unit type is not the critical factor controlling the sequence of activation in heterogeneous muscles. It is concluded that the combined effects of all presynaptic and postsynaptic factors that determine susceptibility to discharge in motoneurons during stretch reflexes are strictly correlated with their axonal conduction velocities, as predicted by the size principle.


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