Motoneuron and muscle-unit properties after long-term direct innervation of soleus muscle by medial gastrocnemius nerve in cat

1990 ◽  
Vol 64 (3) ◽  
pp. 847-861 ◽  
Author(s):  
R. C. Foehring ◽  
J. B. Munson
Keyword(s):  
Electrical Properties ◽  
Soleus Muscle ◽  
Previous Experiment ◽  
Muscle Fibers ◽  
Motor Units ◽  
Slow Muscle ◽  
Medial Gastrocnemius ◽  
Motor Axons ◽  
Lateral Gastrocnemius

1. This study addresses the following questions. 1) In a previous experiment, when the combined lateral gastrocnemius-soleus nerve was cross-innervated by the medial gastrocnemius (MG) nerve, was the predominance of slow muscle units in soleus muscle a result of selective routing of slow motor axons into soleus? 2) Is MG-nerve-induced conversion of soleus muscle fibers from slow to fast more complete at very long (18 mo vs. 9-11 mo) postoperative times? 3) Do MG motoneurons that cross-innervate soleus muscle recover their normal membrane electrical properties at very long postoperative times? 2. The proximal portion of approximately one-third of the MG nerve was coapted directly with the distally isolated soleus nerve. The MG muscle remained innervated by the unoperated portion of the MG nerve. At 6, 10, or 18 mos postoperative, motoneuron and/or muscle-unit properties were determined for MG motoneurons innervating MG, soleus, or neither muscle, and for axotomized soleus motoneurons. 3. In the partially denervated MG muscle, the proportions of motor units of each type were normal. This suggests that the population of MG motor axons that had been directed to the soleus nerve also contained a representative distribution of MG motoneuron types. 4. Most motor units (74%) in cross-innervated soleus (Xsoleus) were type S (based on muscle-unit contractile properties), in spite of the soleus nerve's having been cross-connected by approximately 75% fast MG motoneurons. Thus, even at very long postoperative times, slow soleus muscle units resisted conversion by fast MG motoneurons. 5. Thirty-two percent of MG motoneurons that had been cross-connected to soleus nerve elicited no measurable muscle contraction, compared with approximately 10% in previous reinnervation experiments in which the MG nerve was coapted with the MG or lateral gastrocnemius-soleus nerve. Thus MG motoneurons may be disadvantaged in their ability to innervate soleus muscle fibers. 6. It appears that at long postoperative times, those fast MG motoneurons tha had innervated large soleus muscle units had failed to convert those muscle fibers to fast types and had failed also to recover their normal motoneuron electrical properties. Conversion and recovery did occur for fast MG motoneurons that innervated small soleus muscle units and for slow MG motoneurons.

Motor-unit properties following cross-reinnervation of cat lateral gastrocnemius and soleus muscles with medial gastrocnemius nerve. II. Influence of muscle on motoneurons

1987 ◽  
Vol 57 (4) ◽  
pp. 1227-1245 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson
Keyword(s):  
Electrical Properties ◽  
Motor Unit ◽  
Conduction Velocity ◽  
Decay Time ◽  
Motor Units ◽  
Input Resistance ◽  
Medial Gastrocnemius ◽  
Lateral Gastrocnemius ◽  
Mean Values ◽  
Axonal Conduction

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)

Properties of self-reinnervated motor units of medial gastrocnemius of cat. II. Axotomized motoneurons and time course of recovery

1986 ◽  
Vol 55 (5) ◽  
pp. 947-965 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson
Keyword(s):  
Electrical Properties ◽  
Motor Unit ◽  
Fatigue Resistance ◽  
Time Course ◽  
Muscle Fibers ◽  
Motor Units ◽  
Input Resistance ◽  
Medial Gastrocnemius ◽  
Muscle Properties ◽  
Fast Twitch

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)

Properties of self-reinnervated motor units of medial gastrocnemius of cat. I. Long-term reinnervation

1986 ◽  
Vol 55 (5) ◽  
pp. 931-946 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson
Keyword(s):  
Electrical Properties ◽  
Muscle Contraction ◽  
Motor Unit ◽  
Fatigue Resistance ◽  
Muscle Fibers ◽  
Motor Units ◽  
Contractile Properties ◽  
Medial Gastrocnemius ◽  
Unit Type ◽  
Fast Twitch

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)

Motor-unit properties following cross-reinnervation of cat lateral gastrocnemius and soleus muscles with medial gastrocnemius nerve. I. Influence of motoneurons on muscle

1987 ◽  
Vol 57 (4) ◽  
pp. 1210-1226 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson
Keyword(s):  
Motor Unit ◽  
Muscle Fibers ◽  
Motor Units ◽  
Contractile Properties ◽  
Medial Gastrocnemius ◽  
Similar Degree ◽  
Muscle Properties ◽  
Lateral Gastrocnemius ◽  
Type Distribution ◽  
Unit Type

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.

Plasticity of medial gastrocnemius motor units following cordotomy in the cat

1986 ◽  
Vol 55 (4) ◽  
pp. 619-634 ◽  
Author(s):  
J. B. Munson ◽  
R. C. Foehring ◽  
S. A. Lofton ◽  
J. E. Zengel ◽  
G. W. Sypert
Keyword(s):  
Electrical Properties ◽  
Motor Unit ◽  
Muscle Fibers ◽  
Motor Units ◽  
Contractile Properties ◽  
Medial Gastrocnemius ◽  
Lumbar Spinal Cord ◽  
Partial Recovery ◽  
Cross Sectional ◽  
Group I

Experiments were performed in adult cats to determine the effects of lumbar cordotomy on synaptic potentials, motoneuron membrane electrical properties, muscle-unit contractile properties, and whole-muscle histochemical properties of a heterogeneous skeletal muscle. Medial gastrocnemius (MG) motor units were examined 1 wk to 7 mo following complete transection of the lumbar spinal cord (cordotomy). Motor units were classified on the basis of their contractile properties as type FF, FI, FR, or S (8, 68). Muscle fibers were classified as type FG, FOG, or SO on the basis of histochemical staining (59). Motoneuron electrical properties (axonal conduction velocity, action-potential amplitude, rheobase, input resistance, afterhyperpolarization), group I EPSPs, and muscle-unit contractile properties (unpotentiated and potentiated twitch, unfused and fused tetanus, fatigability) were measured. Reduced numbers of type FR motor units and increased numbers of types FI + FF motor units were found in electrophysiological experiments 2 wk to 7 mo following cordotomy. Corroborative data were obtained from histochemical studies of the same MG muscles. Electrical properties of the motoneurons of each motor-unit type were normal following cordotomy. The close correspondence between motoneuron electrical properties and muscle-unit contractile properties found in normal MG muscle (68) was preserved following cordotomy. Contractile strength of muscle units of all types was severely reduced following cordotomy; partial recovery occurred 4-7 mo following cordotomy. Cross-sectional area of muscle fibers was reduced at all times investigated (2 wk to 7 mo). In three cats, homonymous group Ia single-fiber-motoneuron EPSPs were studied 1 or 2 mo following cordotomy at spinal level L4-5 or L5. EPSP amplitude and afferent-to-motoneuron projection frequency were normal. In 12 other cats, composite heteronymous group I EPSPs were studied 2 wk to 7 mo following cordotomy at various levels. Amplitude of these EPSPs was increased, dependent upon level of cordotomy and postoperative time. Hypotheses concerning the influence of motoneurons on muscle, and of muscle on motoneurons, are presented as possible mechanisms whereby the close relation between motoneuron electrical and muscle-unit contractile properties is preserved in the face of redistributed motor-unit populations.

Motor units and histochemistry in rat lateral gastrocnemius and soleus muscles: evidence for dissociation of physiological and histochemical properties after reinnervation

1987 ◽  
Vol 57 (4) ◽  
pp. 921-937 ◽  
Author(s):  
M. J. Gillespie ◽  
T. Gordon ◽  
P. R. Murphy
Keyword(s):  
Motor Unit ◽  
Muscle Fibers ◽  
Motor Units ◽  
Slow Muscle ◽  
Muscle Fiber Types ◽  
Fiber Types ◽  
Lateral Gastrocnemius ◽  
Fast And Slow Muscle ◽  
Individual Muscle ◽  
Significant Change

A reexamination of the question of specificity of reinnervation of fast and slow muscle was undertaken using the original "self" nerve supply to the fast lateral gastrocnemius (LG) and slow soleus muscles in the rat hindlimb. This paradigm takes advantage of the unusual situation of a common nerve branch, which supplies both a fast and slow muscle, and of the opportunity to keep the reinnervating nerve in its normal position. In addition it provides a test of the effects of cross-reinnervation among muscles of the same functional group. The properties of soleus and LG muscles and of individual muscle units were characterized in normal rats and in rats 4-14 mo after cutting the lateral gastrocnemius-soleus (LGS) nerve and suture of the proximal stump to the dorsal surface of the LG muscle. Individual muscle units were functionally isolated by stimulation of single motor axons to LG or soleus muscle contained in teased filaments in the L4 and L5 ventral roots. Motor units were classified as fast contracting fatiguable (FF), fast contracting fatigue resistant (FR), and slow (S) on the basis of criteria described in the cat by Burke et al. and applied to rat muscle units by Gillespie et al. Muscle fibers were classified as fast glycolytic (FG), fast oxidative glycolytic (FOG), and slow oxidative (SO) on the basis of histochemical staining for myosin ATPase, nicotinamide-adenine dinucleotide diaphorase (NADH-D), and alpha-glycerophosphate (alpha-GPD). Reinnervated muscles developed less force and weighed less in accordance with having fewer than normal motor units and having lost denervated muscle fibers. Normal LG contained a small proportion of S-type motor units (9%), whereas the majority (80%) of control soleus units were S type. After reinnervation, each muscle contained similar proportions of fast and slow motor units with S-type units constituting 30% of units in both muscles. When compared with the normal motor-unit sample, there was no significant change in average twitch and tetanic force in reinnervated muscles for each type of motor unit. However, the range within each type was greater, and there was considerable overlap between types. Twitch contraction time was inversely correlated with force in normal and reinnervated muscles as shown previously in self- and cross-reinnervated LGS in the cat. Changes in proportions of motor units in reinnervated LG were accompanied by corresponding changes in histochemical muscle types. This contrasted with reinnervated soleus in which the proportion of muscle fiber types was not significantly changed from normal despite significant change in motor-unit proportions.(ABSTRACT TRUNCATED AT 400 WORDS)

Immunity to nerve growth factor and the effect on motor unit reinnervation in the rabbit

1992 ◽  
Vol 262 (5) ◽  
pp. R813-R818 ◽  
Author(s):  
D. I. Finkelstein ◽  
A. R. Luff ◽  
J. A. Schuijers
Keyword(s):  
Nerve Growth Factor ◽  
Growth Factor ◽  
Neural Crest ◽  
Conduction Velocity ◽  
Motor Units ◽  
Medial Gastrocnemius ◽  
Afferent Neuron ◽  
Motor Axons ◽  
Nerve Growth ◽  
Myelin Thickness

The trophic effects of nerve growth factor (NGF) on sympathetic, peripheral afferent, and other neural crest-derived cells have been intensively investigated. More recently, NGF has been shown to have an influence on motoneurons. This study was undertaken to investigate whether NGF had any influence on the mechanical or histological properties of reinnervated motor units. Three groups of rabbits were used: normal rabbits, rabbits in which the nerve to medial gastrocnemius (MG) was cut and allowed to reinnervate for 56 days, and rabbits in which the MG nerve reinnervated in the presence of immunity to NGF. Immunity to NGF did not affect the ability of motor axons to reinnervate a muscle, nor were the contractile characteristics of the motor units altered. The size of horseradish peroxidase-labeled motoneurons was not influenced by immunization against NGF; however, the distribution of afferent neuron sizes was altered. Conduction velocity of motor axons proximal to the neuroma was significantly faster after immunization against NGF. Transection and subsequent reinnervation by a peripheral nerve normally causes an increase in myelin thickness proximal to the neuroma. However, immunization against NGF appeared to decrease the magnitude of myelin thickening. It was concluded that immunization against NGF affects motor axonal conduction velocity via an influence on the neural crest-derived Schwann cells.

Recovery of the soleus muscle after short- and long-term disuse induced by hindlimb unloading: effects on the electrical properties and myosin heavy chain profile

2005 ◽  
Vol 18 (2) ◽  
pp. 356-365 ◽  
Author(s):  
Jean-François Desaphy ◽  
Sabata Pierno ◽  
Antonella Liantonio ◽  
Annamaria De Luca ◽  
M. Paola Didonna ◽  
...  
Keyword(s):  
Electrical Properties ◽  
Myosin Heavy Chain ◽  
Soleus Muscle ◽  
Heavy Chain ◽  
Hindlimb Unloading ◽  
Short And Long Term

Properties of medial gastrocnemius motor units and muscle fibers reinnervated by embryonic ventral spinal cord cells

2003 ◽  
Vol 180 (1) ◽  
pp. 25-31 ◽  
Author(s):  
Christine K Thomas ◽  
Sanjay Sesodia ◽  
Daniel E Erb ◽  
Robert M Grumbles
Keyword(s):  
Spinal Cord ◽  
Muscle Fibers ◽  
Motor Units ◽  
Medial Gastrocnemius ◽  
Ventral Spinal Cord

Progress of Age-Related Changes in Properties of Motor Units in the Gastrocnemius Muscle of Rats

2004 ◽  
Vol 92 (3) ◽  
pp. 1357-1365 ◽  
Author(s):  
Miho Sugiura ◽  
Kenro Kanda
Keyword(s):  
Gastrocnemius Muscle ◽  
Muscle Tension ◽  
Muscle Fibers ◽  
Motor Units ◽  
Medial Gastrocnemius ◽  
Motor Nucleus ◽  
Twitch Contraction ◽  
Age Related ◽  
Old Rats ◽  
Whole Muscle

The mechanical properties of individual motor units in the medial gastrocnemius muscle, as well as the whole muscle properties and innervating motor nucleus, were investigated in dietary-restricted, male Fischer 344/DuCrj rats at ages of 4, 7, 12, 21/22, 27, 31, and 36 mo. The tetanic tension of the type S units continuously increased until the age of 36 mo. Those of type FF and FR units declined from 21/22 to 27 mo of age but did not change further while the whole muscle tension decreased greatly. The atrophy of muscle fibers, the decline in motoneuron number and axonal conduction velocity, and the decrease in the posttetanic potentiation of twitch contraction of motor units seemed to start after 21/22 mo of age and were accelerated with advancing age. Prolongation of twitch contraction time was evident for only type S and FR units in 36-mo-old rats. The fatigue index was greatly increased for type FF units in 36-mo-old rats. These findings indicated that the progress of changes in various properties occurring in the senescent muscle was different in terms of their time course and degree and also dependent on the types of motor unit. The atrophy and decrease in specific tension of muscle fibers affected the decline in tension output of motor units. This was effectively compensated for by the capture of denervated muscle fibers over time.

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