Online citations, reference lists, and bibliographies.
← Back to Search

The Resilience Of The Size Principle In The Organization Of Motor Unit Properties In Normal And Reinnervated Adult Skeletal Muscles.

T. Gordon, C. Thomas, J. Munson, R. Stein
Published 2004 · Medicine, Biology

Cite This
Download PDF
Analyze on Scholarcy
Share
Henneman's size principle relates the input and output properties of motoneurons and their muscle fibers to size and is the basis for size-ordered activation or recruitment of motor units during movement. After nerve injury and surgical repair, the relationship between motoneuron size and the number and size of the muscle fibers that the motoneuron reinnervates is initially lost but returns with time, irrespective of whether the muscles are self- or cross-reinnervated by the regenerated axons. Although the return of the size relationships was initially attributed to the recovery of the cross-sectional area of the reinnervated muscle fibers and their force per fiber, direct enumeration of the innervation ratio and the number of muscle fibers per motoneuron demonstrated that a size-dependent branching of axons accounts for the size relationships in normal muscle, as suggested by Henneman and his colleagues. This same size-dependent branching accounts for the rematching of motoneuron size and muscle unit size in reinnervated muscles. Experiments were carried out to determine whether the daily amount of neuromuscular activation of motor units accounts for the size-dependent organization and reorganization of motor unit properties. The normal size-dependent matching of motoneurons and their muscle units with respect to the numbers of muscle fibers per motoneuron was unaltered by synchronous activation of all of the motor units with the same daily activity. Hence, the restored size relationships and rematching of motoneuron and muscle unit properties after nerve injuries and muscle reinnervation sustain the normal gradation of muscle force during movement by size-ordered recruitment of motor units and the process of rate coding of action potentials. Dynamic modulation of size of muscle fibers and their contractile speed and endurance by neuromuscular activity allows for neuromuscular adaptation in the context of the sustained organization of the neuromuscular system according to the size principle.
This paper references
10.1007/BFB0036123
Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation.
D. Pette (1992)
10.1016/S0074-7696(02)16006-2
Molecular and cellular mechanisms involved in the generation of fiber diversity during myogenesis.
P. Wigmore (2002)
10.1152/JN.1987.57.6.1730
Maximal force as a function of anatomical features of motor units in the cat tibialis anterior.
S. Bodine (1987)
10.1113/jphysiol.1987.sp016365
Fibre sizes and histochemical staining characteristics in normal and chronically stimulated fast muscle of cat.
Y. Donselaar (1987)
10.1212/WNL.18.5.447
“Type grouping” in skeletal muscles after experimental reinnervation
C. Karpati (1968)
10.1152/JN.1982.48.5.1175
Reorganization of motor-unit properties in reinnervated muscles of the cat.
T. Gordon (1982)
10.1136/jnnp.33.3.319
Mapping of motor units in experimentally reinnervated rat muscle
E. Kugelberg (1970)
10.1113/jphysiol.1984.sp015278
Effects of fast and slow patterns of tonic long‐term stimulation on contractile properties of fast muscle in the cat.
O. Eerbeek (1984)
10.1111/j.1469-7793.1998.909bm.x
Incomplete rematching of nerve and muscle properties in motor units after extensive nerve injuries in cat hindlimb muscle
V. Rafuse (1998)
10.1152/JN.1987.57.4.1227
Motor-unit properties following cross-reinnervation of cat lateral gastrocnemius and soleus muscles with medial gastrocnemius nerve. II. Influence of muscle on motoneurons.
R. Foehring (1987)
10.1152/JN.1985.54.4.818
Cross-reinnervated motor units in cat muscle. I. Flexor digitorum longus muscle units reinnervated by soleus motoneurons.
R. Dum (1985)
10.1152/JN.1992.67.5.1385
Innervation ratio is an important determinant of force in normal and reinnervated rat tibialis anterior muscles.
J. E. Tötösy de Zepetnek (1992)
10.1007/978-1-4615-0713-0_25
Relative strengths and distributions of different sources of synaptic input to the motoneurone pool: implications for motor unit recruitment.
M. D. Binder (2002)
10.1113/jphysiol.1969.sp008771
The influence of activity on some contractile characteristics of mammalian fast and slow muscles
S. Salmons (1969)
10.1152/JN.1986.55.5.1017
Motor-unit recruitment in human first dorsal interosseous muscle for static contractions in three different directions.
C. Thomas (1986)
10.1002/MUS.880110209
Axonal conduction velocity and force of single human motor units
R. Dengler (1988)
10.1523/JNEUROSCI.08-12-04415.1988
Control of contractile properties within adaptive ranges by patterns of impulse activity in the rat
R. Westgaard (1988)
10.1113/jphysiol.1986.sp016021
Reinnervation of the lateral gastrocnemius and soleus muscles in the rat by their common nerve.
M. J. Gillespie (1986)
10.1098/RSPB.1930.0032
Numbers and Contraction-Values of Individual Motor-Units Examined in some Muscles of the Limb
J. Eccles (1930)
10.1152/AJPCELL.1995.268.2.C527
Further evidence of incomplete neural control of muscle properties in cat tibialis anterior motor units.
G. Unguez (1995)
10.1097/00003677-200210000-00003
Motoneuron and Sensory Neuron Plasticity to Varying Neuromuscular Activity Levels
A. Ishihara (2002)
10.1002/CPHY.CP010210
Motor Units: Anatomy, Physiology, and Functional Organization
R. E. Burke (1981)
10.1523/JNEUROSCI.13-06-02730.1993
Motor axons preferentially reinnervate motor pathways
T. Brushart (1993)
10.1152/JN.1996.75.1.268
Self-reinnervated cat medial gastrocnemius muscles. I. comparisons of the capacity for regenerating nerves to form enlarged motor units after extensive peripheral nerve injuries.
V. Rafuse (1996)
10.1152/JN.1985.53.5.1323
Membrane electrical properties and prediction of motor-unit type of medial gastrocnemius motoneurons in the cat.
J. Zengel (1985)
10.1152/JN.1974.37.6.1338
Rank order of motoneurons within a pool: law of combination.
E. Henneman (1974)
10.1152/JN.1991.66.4.1127
Motor-unit recruitment in the decerebrate cat: several unit properties are equally good predictors of order.
T. Cope (1991)
10.1113/jphysiol.1986.sp016090
Organization of motor units following cross‐reinnervation of antagonistic muscles in the cat hind limb.
T. Gordon (1986)
10.1523/JNEUROSCI.20-07-02602.2000
Brief Electrical Stimulation Promotes the Speed and Accuracy of Motor Axonal Regeneration
A. Al-Majed (2000)
10.1152/JN.1974.37.6.1328
Quantitative measures of output of a motoneuron pool during monosynaptic reflexes.
H. Clamann (1974)
10.1152/JN.1986.55.5.931
Properties of self-reinnervated motor units of medial gastrocnemius of cat. I. Long-term reinnervation.
R. Foehring (1986)
10.1152/JN.1965.28.3.560
FUNCTIONAL SIGNIFICANCE OF CELL SIZE IN SPINAL MOTONEURONS.
E. Henneman (1965)
10.1152/JN.1990.64.3.847
Motoneuron and muscle-unit properties after long-term direct innervation of soleus muscle by medial gastrocnemius nerve in cat.
R. Foehring (1990)
10.1098/RSPB.1929.0010
On the Nature of Postural Reflexes
D. Dennybrown (1929)
10.1152/JN.1997.77.5.2585
Fast-to-slow conversion following chronic low-frequency activation of medial gastrocnemius muscle in cats. I. Muscle and motor unit properties.
T. Gordon (1997)
10.1152/JN.1965.28.1.71
PROPERTIES OF MOTOR UNITS IN A HOMOGENEOUS RED MUSCLE (SOLEUS) OF THE CAT.
A. M. McPhedran (1965)
10.1152/JN.1985.53.5.1303
Relationship among recruitment order, axonal conduction velocity, and muscle-unit properties of type-identified motor units in cat plantaris muscle.
F. Zajac (1985)
10.1113/jphysiol.1973.sp010193
Changes in firing rate of human motor units during linearly changing voluntary contractions
H. Milner-Brown (1973)
10.1136/jnnp.37.6.670
Contractile and electrical properties of human motor units in neuropathies and motor neurone disease
H. Milner-Brown (1974)
10.1152/jn.1987.58.3.614
Effects of physiological amounts of high- and low-rate chronic stimulation on fast-twitch muscle of the cat hindlimb. II. Endurance-related properties.
D. Kernell (1987)
10.1113/jphysiol.1973.sp010192
The orderly recruitment of human motor units during voluntary isometric contractions
H. Milner-Brown (1973)
10.1113/jphysiol.1997.sp021970
Innervation ratio and motor unit force in large muscles: a study of chronically stimulated cat medial gastrocnemius.
V. Rafuse (1997)
10.1152/JN.1997.77.5.2605
Fast-to-slow conversion following chronic low-frequency activation of medial gastrocnemius muscle in cats. II. Motoneuron properties.
J. Munson (1997)
10.1152/JN.1996.75.1.282
Self-reinnervated cat medial gastrocnemius muscles. II. analysis of the mechanisms and significance of fiber type grouping in reinnervated muscles.
V. Rafuse (1996)
10.4449/AIB.V130I1.622
Organized variability in the neuromuscular system: a survey of task-related adaptations.
D. Kernell (1992)
10.1152/JN.1965.28.1.85
PROPERTIES OF MOTOR UNITS IN A HETEROGENEOUS PALE MUSCLE (M. GASTROCNEMIUS) OF THE CAT.
A. M. McPhedran (1965)
10.1136/jnnp.50.3.259
Patterns of reinnervation and motor unit recruitment in human hand muscles after complete ulnar and median nerve section and resuture.
C. Thomas (1987)
10.1152/JN.1992.67.5.1404
Motor-unit categorization based on contractile and histochemical properties: a glycogen depletion analysis of normal and reinnervated rat tibialis anterior muscle.
J. E. Tötösy de Zepetnek (1992)
10.1002/(SICI)1097-4598(199702)20:2<212::AID-MUS12>3.0.CO;2-4
Motor unit forces and recruitment patterns after cervical spinal cord injury
C. Thomas (1997)
10.1113/jphysiol.1982.sp014074
Time course and extent of recovery in reinnervated motor units of cat triceps surae muscles
T. Gordon (1982)
10.1152/JN.1986.55.5.947
Properties of self-reinnervated motor units of medial gastrocnemius of cat. II. Axotomized motoneurons and time course of recovery.
R. Foehring (1986)
10.1016/S0079-6123(08)62856-3
Limited plasticity of adult motor units conserves recruitment order and rate coding.
T. Gordon (1999)
10.1249/00003677-199301000-00011
Plasticity of Muscle Fiber and Motor Unit Types
T. Gordon (1993)
10.1152/JN.1987.57.4.1210
Motor-unit properties following cross-reinnervation of cat lateral gastrocnemius and soleus muscles with medial gastrocnemius nerve. I. Influence of motoneurons on muscle.
R. Foehring (1987)
10.1001/ARCHNEUR.1968.00480060061008
Orderly Recruitment of Muscle Action Potentials: Motor Unit Threshold and EMG Amplitude
Camille B. Olson (1968)
10.1113/jphysiol.1973.sp010369
Physiological types and histochemical profiles in motor units of the cat gastrocnemius
R. Burke (1973)
10.1111/J.1748-1716.1956.TB01347.X
Tonic and phasic ventral horn cells differentiated by post-tetanic potentiation in cat extensors.
R. Granit (1956)
10.1113/jphysiol.1986.sp016089
Innervation and function of hind‐limb muscles in the cat after cross‐union of the tibial and peroneal nerves.
T. Gordon (1986)
10.1152/JN.1987.57.4.921
Motor units and histochemistry in rat lateral gastrocnemius and soleus muscles: evidence for dissociation of physiological and histochemical properties after reinnervation.
M. J. Gillespie (1987)
10.1152/JN.1988.60.1.365
Comparison of physiological and histochemical properties of motor units after cross-reinnervation of antagonistic muscles in the cat hindlimb.
T. Gordon (1988)
10.1007/s004180100268
Transitions of muscle fiber phenotypic profiles
D. Pette (2001)
10.1113/jphysiol.1963.sp007229
Delayed depolarization and the repetitive response to intracellular stimulation of mammalian motoneurones
R. Granit (1963)
10.1113/jphysiol.1960.sp006395
Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses
A. Buller (1960)
10.1152/JN.1985.54.4.837
Cross-reinnervated motor units in cat muscle. II. Soleus muscle reinnervated by flexor digitorum longus motoneurons.
R. Dum (1985)
10.1152/JN.1992.68.4.1261
Proportional enlargement of motor units after partial denervation of cat triceps surae muscles.
V. Rafuse (1992)
10.1152/JN.1965.28.3.599
Excitability and inhibitability of motoneurons of different sizes.
E. Henneman (1965)



This paper is referenced by
10.1016/j.resp.2013.06.025
Impact of diaphragm muscle fiber atrophy on neuromotor control
C. Mantilla (2013)
Regulatory mechanisms driving motor neuron functional diversification
M. N. Khan (2018)
10.1519/SSC.0b013e318270616d
Underlying Mechanisms and Physiology of Muscular Power
William J. Kraemer (2012)
10.1007/978-1-4614-4466-4_12
Tongue Structure and Function
A. Sokoloff (2012)
10.1080/14789450.2018.1429923
Proteomic serum biomarkers for neuromuscular diseases
Sandra Murphy (2018)
10.1113/jphysiol.2011.210518
Recovery of proprioceptive feedback from nerve crush
J. F. Prather (2011)
Interested in publishing with us ? Contact book
Dan W. Stashuk (2018)
Chapter 5 Clinical Quantitative Electromyography
Tameem Adel (2013)
10.1016/B978-0-444-53825-3.00020-6
Chapter 15--chew before you swallow.
J. Lund (2011)
10.1113/JP278117
Absence of hyperexcitability of spinal motoneurons in patients with amyotrophic lateral sclerosis
V. Marchand-Pauvert (2019)
10.1089/scd.2013.0049
Bone marrow transplantation in dysferlin-deficient mice results in a mild functional improvement.
B. Flix (2013)
10.1152/jn.00565.2015
Increased intensity and reduced frequency of EMG signals from feline self-reinnervated ankle extensors during walking do not normalize excessive lengthening.
A. Pantall (2016)
10.1016/j.hcl.2015.12.001
Nerve Regeneration: Understanding Biology and Its Influence on Return of Function After Nerve Transfers.
T. Gordon (2016)
10.1152/japplphysiol.01212.2012
Neuromotor control in chronic obstructive pulmonary disease.
C. Mantilla (2013)
10.1113/jphysiol.2010.190389
Sprouting capacity of lumbar motoneurons in normal and hemisected spinal cords of the rat
T. Gordon (2010)
Contents lists available at SciVerse ScienceDirect
Yoshiko Shibuta (2013)
10.1016/j.exger.2013.01.011
The Motor Unit Number Index (MUNIX) in sarcopenic patients
M. Drey (2013)
10.1007/s00421-016-3439-2
The impact of repetition mechanics on the adaptations resulting from strength-, hypertrophy- and cluster-type resistance training
G. Nicholson (2016)
10.1152/jn.00661.2017
Time course of functional recovery during the first 3 mo after surgical transection and repair of nerves to the feline soleus and lateral gastrocnemius muscles.
R. Gregor (2018)
The role of wild-type SOD1 in SOD1 mouse models of ALS
R. Bunton-Stasyshyn (2014)
10.3233/NRE-141135
Does use of the optokinetic chart stimulation based OKCSIB protocol improve recovery of upper and lower limb movements, function and quality of life at 3 year follow up in dense strokes? A retrospective case control series.
Benjamin Chitambira (2014)
The Impact of Reduced-Exertion High-Intensity Interval Training on Insulin Sensitivity and Aerobic Capacity
Richard S Metcalfe (2015)
10.1016/J.PNEUROBIO.2006.03.001
Plasticity from muscle to brain
J. Wolpaw (2006)
10.1007/s11910-015-0537-1
Neurogenic Changes in the Upper Airway of Obstructive Sleep Apnoea
J. P. Saboisky (2015)
10.1017/9781316417614
Comprehensive Electromyography: With Clinical Correlations and Case Studies
M. Ferrante (2018)
10.1016/J.NBD.2007.07.003
Time course of preferential motor unit loss in the SOD1G93A mouse model of amyotrophic lateral sclerosis
J. Hegedus (2007)
10.1044/PERSP2.SIG13.93
Mechanisms for Successful Rehabilitation of Cough in Parkinson's Disease Using Expiratory Muscle Strength Training
Alyssa D. Huff (2017)
10.1111/cpf.12195
Relation between muscle mass, motor units and type of training in master athletes
M. Drey (2016)
10.1152/japplphysiol.00812.2010
Recruitment and rate-coding strategies of the human genioglossus muscle.
J. P. Saboisky (2010)
10.4018/978-1-4666-6090-8.CH001
Neural Control of Muscle
P. Bawa (2014)
10.1016/j.mayocp.2014.12.004
Optical stimulation for restoration of motor function after spinal cord injury.
Grant W. Mallory (2015)
10.3233/NRE-2011-0638
Use of an optokinetic chart stimulation intervention for restoration of voluntary movement, postural control and mobility in acute stroke patients and one post intensive care polyneuropathy patient: A case series.
Benjamin Chitambira (2011)
See more
Semantic Scholar Logo Some data provided by SemanticScholar