Contractile Properties of Human Motor Units: Is Man a Gat?

A major goal in neuroscience is to understand how the CNS controls posture and movement in humans. This requires an understanding of individual human motor unit properties and how they interact within the muscle to perform different tasks. This article describes differences and similarities between the contractile properties of human motor units and those of the cat prototype medial gastrocnemius (MG) muscle, on which so many studies have been conducted. The article describes the methods available for measuring human motor unit properties and their limitations, and it discusses how far the behavior of whole muscles can be predicted from their histochemistry. It questions the extent to which human motor units conform to the conventional criteria by which S (slow, fatigue resistant), FR (fast but fatigue resistant) and FF (fast, fatigable) unit types are usually classified. An important difference between human and cat MG data is that weak human motor units are not necessarily slow, nor strong ones fast; that is, generally, human unit force is not correlated with contractile speed. Also, unlike cat MG, the few human muscles studied so far contain few if any FF units but a high proportion of units with intermediate fatigue resistance (Flnt). These apparently aberrant human properties, however, are also found in other cat and rat muscles. Thus, cat MG may not be the best model for motor unit behavior generally. Finally, the influence of human motor unit properties on force output by recruitment and/or rate coding is discussed.

[1]  E. Noble,et al.  Shifts in rat plantaris motor unit characteristics with aging and compensatory overload. , 1991, Journal of applied physiology.

[2]  J. Stephens,et al.  Study of human motor unit contractions by controlled intramascular microstimulation , 1976, Brain Research.

[3]  H. Clamann,et al.  Nonlinear force addition of newly recruited motor units in the cat hindlimb , 1988, Muscle & nerve.

[4]  R. Stein,et al.  Reorganization of motor-unit properties in reinnervated muscles of the cat. , 1982, Journal of neurophysiology.

[5]  A Lev-Tov,et al.  The motor-unit population of the cat tenuissimus muscle. , 1988, Journal of neurophysiology.

[6]  R B Stein,et al.  The orderly recruitment of human motor units during voluntary isometric contractions , 1973, The Journal of physiology.

[7]  E. Henneman,et al.  PROPERTIES OF MOTOR UNITS IN A HETEROGENEOUS PALE MUSCLE (M. GASTROCNEMIUS) OF THE CAT. , 1965, Journal of neurophysiology.

[8]  D. Levine,et al.  Physiological types and histochemical profiles in motor units of the cat gastrocnemius , 1973, The Journal of physiology.

[9]  T. Miles,et al.  Effect of motor unit firing pattern on twitches obtained by spike‐triggered averaging , 1989, Muscle & nerve.

[10]  Lars Larsson Is the motor unit uniform? , 1992, Acta physiologica Scandinavica.

[11]  H. Clamann,et al.  Elsevier/North-Holland Biomedical Press COMPARISON OF THE RECRUITMENT AND DISCHARGE PROPERTIES OF MOTOR UNITS IN H U M A N BRACHIAL BICEPS AND A D D U C T O R POLLICIS D U R I N G ISOMETRIC CONTRACTIONS , 2018 .

[12]  W. Engel,et al.  The histographic analysis of human muscle biopsies with regard to fiber types , 1969, Neurology.

[13]  R Yemm,et al.  The orderly recruitment of motor units of the masseter and temporal muscles during voluntary isometric contraction in man. , 1977, The Journal of physiology.

[14]  P F Gardiner,et al.  Physiological properties of motoneurons innervating different muscle unit types in rat gastrocnemius. , 1993, Journal of neurophysiology.

[15]  S. Riek,et al.  Recruitment of motor units in human forearm extensors. , 1992, Journal of neurophysiology.

[16]  S. Andreassen,et al.  Muscle fibre conduction velocity in motor units of the human anterior tibial muscle: a new size principle parameter. , 1987, The Journal of physiology.

[17]  F E Zajac,et al.  Relationship among recruitment order, axonal conduction velocity, and muscle-unit properties of type-identified motor units in cat plantaris muscle. , 1985, Journal of neurophysiology.

[18]  R S Johansson,et al.  Force-frequency relationships of human thenar motor units. , 1991, Journal of neurophysiology.

[19]  R Dengler,et al.  Axonal conduction velocity and force of single human motor units , 1988, Muscle & nerve.

[20]  W. Weijs,et al.  Contraction characteristics and myosin heavy chain composition of rabbit masseter motor units. , 1995, Journal of neurophysiology.

[21]  B. Calancie,et al.  Limitations of the spike‐triggered averaging technique , 1986, Muscle & nerve.

[22]  R. Johansson,et al.  Tactile sensory coding in the glabrous skin of the human hand , 1983, Trends in Neurosciences.

[23]  T. Cope,et al.  Motor-unit recruitment in the decerebrate cat: several unit properties are equally good predictors of order. , 1991, Journal of neurophysiology.

[24]  B Bigland-Ritchie,et al.  Motor-unit discharge rates in maximal voluntary contractions of three human muscles. , 1983, Journal of neurophysiology.

[25]  A J Fuglevand,et al.  Contractile properties of single motor units in human toe extensors assessed by intraneural motor axon stimulation. , 1996, Journal of neurophysiology.

[26]  T. Gordon,et al.  Innervation ratio is an important determinant of force in normal and reinnervated rat tibialis anterior muscles. , 1992, Journal of neurophysiology.

[27]  T Gordon,et al.  Organization of motor units following cross‐reinnervation of antagonistic muscles in the cat hind limb. , 1986, The Journal of physiology.

[28]  A. McComas,et al.  Fast and slow twitch units in a human muscle , 1971, Journal of neurology, neurosurgery, and psychiatry.

[29]  R S Johansson,et al.  Measurement of contractile and electrical properties of single human thenar motor units in response to intraneural motor-axon stimulation. , 1990, Journal of neurophysiology.

[30]  R M Reinking,et al.  A commentary on muscle unit properties in cat hindlimb muscles , 1980, Journal of morphology.

[31]  Michael J. O'Donovan,et al.  Motor unit organization of human medial gastrocnemius. , 1979, The Journal of physiology.

[32]  R. Dengler,et al.  Parameters of human motor unit twitches obtained by intramuscular microstimulation , 1992, Neuromuscular Disorders.

[33]  C. Olson,et al.  A functional and histochemical characterization of motor units in a heterogeneous muscle (flexor digitorum longus) of the cat , 1966 .

[34]  J. Petit,et al.  Correlation between axonal conduction velocity and tetanic tension of motor units in four muscles of the cat hind limb , 1975, Brain Research.

[35]  P. Murphy,et al.  Reinnervation of the lateral gastrocnemius and soleus muscles in the rat by their common nerve. , 1986, The Journal of physiology.

[36]  R S Johansson,et al.  Attempts to physiologically classify human thenar motor units. , 1991, Journal of neurophysiology.

[37]  J Kimura,et al.  Is the F wave elicited in a select group of motoneurons? , 1984, Muscle & nerve.

[38]  T. P. Usherwood,et al.  The mechanical properties of human motor units with special reference to their fatiguability and recruitment threshold , 1977, Brain Research.

[39]  A. Vallbo,et al.  Activity from skin mechanoreceptors recorded percutaneously in awake human subjects. , 1968, Experimental neurology.

[40]  J. Fleshman,et al.  Rheobase, input resistance, and motor-unit type in medial gastrocnemius motoneurons in the cat. , 1981, Journal of neurophysiology.

[41]  B. Saltin,et al.  Skeletal Muscle Adaptability: Significance for Metabolism and Performance , 1985 .

[42]  E Eldred,et al.  Maximal force as a function of anatomical features of motor units in the cat tibialis anterior. , 1987, Journal of neurophysiology.

[43]  K. Kanda,et al.  Factors causing difference in force output among motor units in the rat medial gastrocnemius muscle. , 1992, The Journal of physiology.

[44]  Steen Andreassen,et al.  Estimation of Motor Unit Twitches , 1983, IEEE Transactions on Biomedical Engineering.

[45]  M. Johnson,et al.  Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. , 1973, Journal of the neurological sciences.

[46]  R. Johansson,et al.  Twitch properties of human thenar motor units measured in response to intraneural motor-axon stimulation. , 1990, Journal of neurophysiology.

[47]  B R Botterman,et al.  Classification of motor units in flexor carpi radialis muscle of the cat. , 1985, Journal of neurophysiology.

[48]  B Bigland-Ritchie,et al.  Evidence for a fatigue-induced reflex inhibition of motoneuron firing rates. , 1987, Journal of neurophysiology.

[49]  D. Kernell,et al.  Average but not continuous speed match between motoneurons and muscle units of rat tibialis anterior. , 1993, Journal of neurophysiology.

[50]  R. G. Williamson,et al.  Motor units and fiber types of primary ankle extensors of the skunk (Mephitis mephitis). , 1977, Journal of neurophysiology.

[51]  B R Botterman,et al.  Gradation of isometric tension by different activation rates in motor units of cat flexor carpi radialis muscle. , 1986, Journal of neurophysiology.

[52]  T Gordon,et al.  Motor-unit categorization based on contractile and histochemical properties: a glycogen depletion analysis of normal and reinnervated rat tibialis anterior muscle. , 1992, Journal of neurophysiology.

[53]  R L Lieber,et al.  12 Force Transmission in Skeletal Muscle: from Actomyosin to External Tendons , 1997, Exercise and sport sciences reviews.

[54]  T J Doherty,et al.  A method for the longitudinal study of human thenar motor units , 1994, Muscle & nerve.

[55]  R B Stein,et al.  New methods for analysing motor function in man and animals. , 1972, Brain research.

[56]  F Buchthal,et al.  Motor unit of mammalian muscle. , 1980, Physiological reviews.

[57]  J. Mateika,et al.  Contractile properties of human nasal dilator motor units. , 1998, Journal of neurophysiology.

[58]  R S Johansson,et al.  A comparison of human thenar motor-unit properties studied by intraneural motor-axon stimulation and spike-triggered averaging. , 1990, Journal of neurophysiology.

[59]  Robert M. Reinking,et al.  Tetrapartite classification of motor units of cat tibialis posterior. , 1980, Journal of neurophysiology.

[60]  C C Hunt,et al.  Proportion of fatigue‐resistant motor units in hindlimb muscles of cat and their relation to axonal conduction velocity. , 1988, The Journal of physiology.

[61]  B. Calancie,et al.  Human motor-unit recruitment during isometric contractions and repeated dynamic movements. , 1987, Journal of neurophysiology.