Testing the excitability of human motoneurons

Chris J McNeil, Jane E Butler, Janet L Taylor, Simon C Gandevia, Chris J McNeil, Jane E Butler, Janet L Taylor, Simon C Gandevia

Abstract

The responsiveness of the human central nervous system can change profoundly with exercise, injury, disuse, or disease. Changes occur at both cortical and spinal levels but in most cases excitability of the motoneuron pool must be assessed to localize accurately the site of adaptation. Hence, it is critical to understand, and employ correctly, the methods to test motoneuron excitability in humans. Several techniques exist and each has its advantages and disadvantages. This review examines the most common techniques that use evoked compound muscle action potentials to test the excitability of the motoneuron pool and describes the merits and limitations of each. The techniques discussed are the H-reflex, F-wave, tendon jerk, V-wave, cervicomedullary motor evoked potential (CMEP), and motor evoked potential (MEP). A number of limitations with these techniques are presented.

Keywords: CMEP; F-wave; H-reflex; MEP; V-wave; motoneuron; tendon jerk.

Figures

Figure 1
Figure 1
Schematic representation of the volleys and pathways involved in the production of the H-reflex, tendon jerk, F-wave, and V-wave. Only the most critical elements are labeled so see text for a complete description of the factors which can influence each response. (A), #1—electrical stimulus evokes a single afferent volley which recruits motoneurons for the H-reflex according to the size principle; #2—presynaptic inhibition can influence afferent input to the motoneuron; #3—tendon tap evokes multiple volleys which arrive at the motoneuron over 25 ms. (B), #1—a small number of motoneurons may discharge to produce F-waves after antidromic impulses reach their soma; #2—at rest, F-waves are likely to be limited to large motoneurons due to reflex activation of smaller motoneurons and collision with the antidromic volley prior to the soma. (C), #1—in motor axons conducting orthodromic impulses of voluntary drive, voluntary and antidromic impulses will collide; #2—reflex response which travels along motor axons cleared by the collision described in point #1 will contribute to the V-wave; #3—presynaptic inhibition can influence afferent input to the motoneuron.
Figure 2
Figure 2
Schematic representation of the volleys and pathways involved in the production of the CMEP and MEP. Only the most critical elements are labeled so see text for a complete description of the factors which can influence each response. #1—transmastoid stimulation evokes a single volley which is not subject to conventional presynaptic inhibition; #2—transcranial magnetic stimulation evokes multiple descending volleys;#3—transcranial magnetic stimulation can cause multiple discharges of a single motoneuron so that MEP size can exceed that of the maximal compound muscle action potential (Mmax).

References

    1. Aagaard P., Simonsen E. B., Andersen J. L., Magnusson P., Dyhre-Poulsen P. (2002). Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J. Appl. Physiol. 92, 2309–2318 10.1152/japplphysiol.01185.2001
    1. Ashby P., Zilm D. (1982). Characteristics of postsynaptic potentials produced in single human motoneurons by homonymous group 1 volleys. Exp. Brain Res. 47, 41–48
    1. Bathien N., Morin C. (1972). [Comparing variations of spinal reflexes during intensive and selective attention (author's transl)]. Physiol. Behav. 9, 533–538
    1. Berardelli A., Inghilleri M., Rothwell J. C., Cruccu G., Manfredi M. (1991). Multiple firing of motoneurones is produced by cortical stimulation but not by direct activation of descending motor tracts. Electroencephalogr. Clin. Neurophysiol. 81, 240–242
    1. Bergmans J., Delwaide P. J., Gadea-Ciria M. (1978). Short-latency effects of low-threshold muscular afferent fibers on different motoneuronal pools of the lower limb in man. Exp. Neurol. 60, 380–385 10.1016/0014-4886(78)90091-2
    1. Binder M. D., Heckman C. J., Powers R. K. (1996). The physiological control of motoneuron activity, in Handbook of Physiology, eds Rowell L. B., Shepherd J. T. (Bethesda, MD: American Physiological Society; ), 3–53
    1. Birnbaum A., Ashby P. (1982). Postsynaptic potentials in individual soleus motoneurons in man produced by achilles tendon taps and electrical stimulation of tibial nerve. Electroencephalogr. Clin. Neurophysiol. 54, 469–471
    1. Buchthal F., Schmalbruch H. (1970). Contraction times of twitches evoked by H-reflexes. Acta Physiol. Scand. 80, 378–382
    1. Burke D., Adams R. W., Skuse N. F. (1989). The effects of voluntary contraction on the H reflex of human limb muscles. Brain 112, 417–433 10.1093/brain/112.2.417
    1. Burke D., Gandevia S. C., McKeon B. (1983). The afferent volleys responsible for spinal proprioceptive reflexes in man. J. Physiol. 339, 535–552
    1. Burke D., Gandevia S. C., McKeon B. (1984). Monosynaptic and oligosynaptic contributions to human ankle jerk and H-reflex. J. Neurophysiol. 52, 435–448
    1. Burke D., McKeon B., Skuse N. F. (1981). The irrelevance of fusimotor activity to the Achilles tendon jerk of relaxed humans. Ann. Neurol. 10, 547–550 10.1002/ana.410100609
    1. Burke R. E. (1981). Motor units: anatomy, physiology and functional organization, in Handbook of Physiology, Section, I, The Nervous System, ed Brooks V. B. (Bethesda, MD: American Physiological Society; ), 345–422
    1. Burke R. E., Levine D. N., Zajac F. E., 3rd. (1971). Mammalian motor units: physiological-histochemical correlation in three types in cat gastrocnemius. Science 174, 709–712 10.1126/science.174.4010.709
    1. Cavallari P., Katz R. (1989). Pattern of projections of group I afferents from forearm muscles to motoneurones supplying biceps and triceps muscles in man. Exp. Brain Res. 78, 465–478
    1. Crone C., Nielsen J. (1989). Methodological implications of the post activation depression of the soleus H-reflex in man. Exp. Brain Res. 78, 28–32
    1. Day B. L., Rothwell J. C., Thompson P. D., Dick J. P., Cowan J. M., Berardelli A., et al. (1987). Motor cortex stimulation in intact man. 2. Multiple descending volleys. Brain 110, 1191–1209 10.1093/brain/110.5.1191
    1. Denslow J. S., Hassett C. C. (1942). The central excitatory state associated with postural abnormalities. J. Neurophysiol. 5, 393–402
    1. Di Lazzaro V., Restuccia D., Oliviero A., Profice P., Ferrara L., Insola A., et al. (1998). Effects of voluntary contraction on descending volleys evoked by transcranial stimulation in conscious humans. J. Physiol. 508, 625–633 10.1111/j.1469-7793.1998.625bq.x
    1. Eccles J. C. (1955). The central action of antidromic impulses in motor nerve fibres. Pflugers Arch. 260, 385–415
    1. Eccles J. C., Eccles R. M., Magni F. (1961). Central inhibitory action attributable to presynaptic depolarization produced by muscle afferent volleys. J. Physiol. 159, 147–166
    1. Eccles J. C., Pritchard J. J. (1937). The action potential of motoneurones. J. Physiol. 89(Suppl.), 43P–45P
    1. Espiritu M. G., Lin C. S., Burke D. (2003). Motoneuron excitability and the F wave. Muscle Nerve 27, 720–727 10.1002/mus.10388
    1. Fisher M. A. (1992). AAEM Minimonograph #13: H reflexes and F waves: physiology and clinical indications. Muscle Nerve 15, 1223–1233 10.1002/mus.880151102
    1. Fournier E., Katz R., Pierrot-Deseilligny E. (1983). Descending control of reflex pathways in the production of voluntary isolated movements in man. Brain Res. 288, 375–377
    1. Frank K., Fuortes M. G. F. (1957). Presynaptic and postsynaptic inhibition of monosynaptic reflexes. Fed. Proc. 16, 39–40
    1. Gandevia S. C., Petersen N., Butler J. E., Taylor J. L. (1999). Impaired response of human motoneurones to corticospinal stimulation after voluntary exercise. J. Physiol. 521, 749–759 10.1111/j.1469-7793.1999.00749.x
    1. Giesebrecht S., Martin P. G., Gandevia S. C., Taylor J. L. (2011). Altered corticospinal transmission to the hand after maximum voluntary efforts. Muscle Nerve 43, 679–687 10.1002/mus.21938
    1. Gogan P., Gustafsson B., Jankowska E., Tyc-Dumont S. (1984). On re-excitation of feline motoneurones: its mechanism and consequences. J. Physiol. 350, 81–91
    1. Gracies J. M., Meunier S., Pierrot-Deseilligny E., Simonetta M. (1991). Pattern of propriospinal-like excitation to different species of human upper limb motoneurones. J. Physiol. 434, 151–167
    1. Gracies J. M., Pierrot-Deseilligny E., Robain G. (1994). Evidence for further recruitment of group I fibres with high stimulus intensities when using surface electrodes in man. Electroencephalogr. Clin. Neurophysiol. 93, 353–357
    1. Henneman E., Mendell L. M. (1981). Functional organization of motoneuron pool and its inputs, in Handbook of Physiology, Section I, The Nervous System, ed Brooks V. B. (Bethesda, MD: American Physiological Society; ), 423–508
    1. Hess C. W., Mills K. R., Murray N. M. (1987). Responses in small hand muscles from magnetic stimulation of the human brain. J. Physiol. 388, 397–419
    1. Hoehler F. K., McCann M. A., Bernick D. L. (1981). Habituation of the Hoffmann reflex. Brain Res. 220, 299–307 10.1016/0006-8993(81)91219-1
    1. Hoffmann P. (1918). Uber die beziehungen der sehnenreflexe zur willkurlichen bewegung und zum tonus. Z. Biol. 68, 351–370
    1. Hoffmann P. (1922). Untersuchungen Uber die Eigenreflexe (Sehnenreflexe) Menschlicher Muskeln. Berlin: Springer
    1. Hugon M. (1973). Methodology of the Hoffmann reflex in man, in New Developments in Electromyography and Clinical Neurophysiology, ed Desmedt J. E. (Basel: Karger; ), 277–293
    1. Hultborn H., Meunier S., Morin C., Pierrot-Deseilligny E. (1987). Assessing changes in presynaptic inhibition of I a fibres: a study in man and the cat. J. Physiol. 389, 729–756
    1. Hultborn H., Nielsen J. B. (1995). H-reflexes and F-responses are not equally sensitive to changes in motoneuronal excitability. Muscle Nerve 18, 1471–1474 10.1002/mus.880181219
    1. Hultborn H., Nielsen J. B. (1998). Modulation of transmitter release from ia afferents by their preceding activity - a ‘postactivation depression’, in Presynaptic Inhibition and Neural Control, eds Rudomin P., Romo R., Mendell L. (New York, NY: Oxford University Press; ), 178–191
    1. Jackson A., Baker S. N., Fetz E. E. (2006). Tests for presynaptic modulation of corticospinal terminals from peripheral afferents and pyramidal tract in the macaque. J. Physiol. 573, 107–120 10.1113/jphysiol.2005.100537
    1. Khan S. I., Giesebrecht S., Gandevia S. C., Taylor J. L. (2012). Activity-dependent depression of the recurrent discharge of human motoneurones after maximal voluntary contractions. J. Physiol. 590, 4957–4969 10.1113/jphysiol.2012.235697
    1. Kiernan M. C., Mogyoros I., Hales J. P., Gracies J. M., Burke D. (1997). Excitability changes in human cutaneous afferents induced by prolonged repetitive axonal activity. J. Physiol. 500, 255–264
    1. Klimstra M., Zehr E. P. (2008). A sigmoid function is the best fit for the ascending limb of the Hoffmann reflex recruitment curve. Exp. Brain Res. 186, 93–105 10.1007/s00221-007-1207-6
    1. Leis A. A., Stetkarova I., Beric A., Stokic D. S. (1995). Spinal motor neuron excitability during the cutaneous silent period. Muscle Nerve 18, 1464–1470 10.1002/mus.880181218
    1. Lin J. Z., Floeter M. K. (2004). Do F-wave measurements detect changes in motor neuron excitability? Muscle Nerve 30, 289–294 10.1002/mus.20110
    1. Magladery J. W., McDougal D. B., Jr. (1950). Electrophysiological studies of nerve and reflex activity in normal man. I. Identification of certain reflexes in the electromyogram and the conduction velocity of peripheral nerve fibers. Bull. Johns Hopkins Hosp. 86, 265–290
    1. Magladery J. W., Porter W. E., Park A. M., Teasdall R. D. (1951). Electrophysiological studies of nerve and reflex activity in normal man. IV. The two-neurone reflex and identification of certain action potentials from spinal roots and cord. Bull. Johns Hopkins Hosp. 88, 499–519
    1. Marchand-Pauvert V., Nicolas G., Burke D., Pierrot-Deseilligny E. (2002). Suppression of the H reflex in humans by disynaptic autogenetic inhibitory pathways activated by the test volley. J. Physiol. 542, 963–976 10.1113/jphysiol.2002.021683
    1. Marchand-Pauvert V., Nicolas G., Pierrot-Deseilligny E. (2000). Monosynaptic Ia projections from intrinsic hand muscles to forearm motoneurones in humans. J. Physiol. 525, 241–252 10.1111/j.1469-7793.2000.t01-1-00241.x
    1. Martin P. G., Butler J. E., Gandevia S. C., Taylor J. L. (2008). Noninvasive stimulation of human corticospinal axons innervating leg muscles. J. Neurophysiol. 100, 1080–1086 10.1152/jn.90380.2008
    1. McNeil C. J., Giesebrecht S., Gandevia S. C., Taylor J. L. (2011a). Behaviour of the motoneurone pool in a fatiguing submaximal contraction. J. Physiol. 589, 3533–3544 10.1113/jphysiol.2011.207191
    1. McNeil C. J., Giesebrecht S., Khan S. I., Gandevia S. C., Taylor J. L. (2011b). The reduction in human motoneurone responsiveness during muscle fatigue is not prevented by increased muscle spindle discharge. J. Physiol. 589, 3731–3738 10.1113/jphysiol.2011.210252
    1. McNeil C. J., Martin P. G., Gandevia S. C., Taylor J. L. (2011c). Long-interval intracortical inhibition in a human hand muscle. Exp. Brain Res. 209, 287–297 10.1007/s00221-011-2552-z
    1. McNeil C. J., Martin P. G., Gandevia S. C., Taylor J. L. (2009). The response to paired motor cortical stimuli is abolished at a spinal level during human muscle fatigue. J. Physiol. 587, 5601–5612 10.1113/jphysiol.2009.180968
    1. Meunier S., Penicaud A., Pierrot-Deseilligny E., Rossi A. (1990). Monosynaptic Ia excitation and recurrent inhibition from quadriceps to ankle flexors and extensors in man. J. Physiol. 423, 661–675
    1. Meunier S., Pierrot-Deseilligny E. (1989). Gating of the afferent volley of the monosynaptic stretch reflex during movement in man. J. Physiol. 419, 753–763
    1. Meunier S., Pierrot-Deseilligny E., Simonetta M. (1993). Pattern of monosynaptic heteronymous Ia connections in the human lower limb. Exp. Brain Res. 96, 534–544
    1. Miles T. S., Turker K. S., Le T. H. (1989). Ia reflexes and EPSPs in human soleus motor neurones. Exp. Brain Res. 77, 628–636
    1. Milner-Brown H. S., Stein R. B., Yemm R. (1973). The orderly recruitment of human motor units during voluntary isometric contractions. J. Physiol. 230, 359–370
    1. Nielsen J., Kagamihara Y. (1993). Differential projection of the sural nerve to early and late recruited human tibialis anterior motor units: change of recruitment gain. Acta Physiol. Scand. 147, 385–401
    1. Nielsen J., Petersen N. (1994). Is presynaptic inhibition distributed to corticospinal fibres in man? J. Physiol. 477, 47–58
    1. Paillard J. (1955). [Electrophysiologic analysis and comparison in man of Hoffmann's reflex and myotatic reflex]. Pflugers Arch. 260, 448–479
    1. Peter J. B., Barnard R. J., Edgerton V. R., Gillespie C. A., Stempel K. E. (1972). Metabolic profiles of three fiber types of skeletal muscle in guinea pigs and rabbits. Biochemistry 11, 2627–2633
    1. Petersen N. T., Taylor J. L., Gandevia S. C. (2002). The effect of electrical stimulation of the corticospinal tract on motor units of the human biceps brachii. J. Physiol. 544, 277–284 10.1113/jphysiol.2002.024539
    1. Pierrot-Deseilligny E., Burke D. (2005). The Circuitry of the Human Spinal Cord: Its Role in Motor Control and Movement Disorders. Cambridge: Cambridge University Press
    1. Pierrot-Deseilligny E., Fournier E. (1986). Control of transmission in spinal pathways during movement in man - functional significance, in Sensorimotor Plasticity: Theoretical, Experimental and Clinical Aspects, eds Ron S., Schmid R., Jeannerod M. (Paris: Les Editions INSERM; ), 385–395
    1. Pierrot-Deseilligny E., Mazevet D. (2000). The monosynaptic reflex: a tool to investigate motor control in humans. Interest and limits. Neurophysiol. Clin. 30, 67–80
    1. Pierrot-Deseilligny E., Morin C., Bergego C., Tankov N. (1981). Pattern of group I fibre projections from ankle flexor and extensor muscles in man. Exp. Brain Res. 42, 337–350
    1. Polus B. I., Patak A., Gregory J. E., Proske U. (1991). Effect of muscle length on phasic stretch reflexes in humans and cats. J. Neurophysiol. 66, 613–622
    1. Proske U., Morgan D. L., Gregory J. E. (1993). Thixotropy in skeletal muscle and in muscle spindles: a review. Prog. Neurobiol. 41, 705–721 10.1016/0301-0082(93)90032-N
    1. Rossi A., Rossi S., Ginanneschi F. (2012). Activity-dependent changes in intrinsic excitability of human spinal motoneurones produced by natural activity. J. Neurophysiol. 108, 2473–2480 10.1152/jn.00477.2012
    1. Rothwell J., Burke D., Hicks R., Stephen J., Woodforth I., Crawford M. (1994). Transcranial electrical stimulation of the motor cortex in man: further evidence for the site of activation. J. Physiol. 481, 243–250
    1. Rudomin P., Schmidt R. F. (1999). Presynaptic inhibition in the vertebrate spinal cord revisited. Exp. Brain Res. 129, 1–37 10.1007/s002210050933
    1. Schieppati M. (1987). The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog. Neurobiol. 28, 345–376 10.1016/0301-0082(87)90007-4
    1. Sherrington C. S. (1906). The Integrative Action of the Nervous System. New Haven, CT: Yale University Press
    1. Stein R. B., Estabrooks K. L., McGie S., Roth M. J., Jones K. E. (2007). Quantifying the effects of voluntary contraction and inter-stimulus interval on the human soleus H-reflex. Exp. Brain Res. 182, 309–319 10.1007/s00221-007-0989-x
    1. Stein R. B., Thompson A. K. (2006). Muscle reflexes in motion: how, what, and why? Exerc. Sport Sci. Rev. 34, 145–153 10.1249/01.jes.0000240024.37996.e5
    1. Taborikova H., Sax D. S. (1968). Motoneurone pool and the H-reflex. J. Neurol. Neurosurg. Psychiatry 31, 354–361
    1. Taylor J. L., Allen G. M., Butler J. E., Gandevia S. C. (1997). Effect of contraction strength on responses in biceps brachii and adductor pollicis to transcranial magnetic stimulation. Exp. Brain Res. 117, 472–478 10.1007/s002210050243
    1. Taylor J. L., Gandevia S. C. (2004). Noninvasive stimulation of the human corticospinal tract. J. Appl. Physiol. 96, 1496–1503 10.1152/japplphysiol.01116.2003
    1. Taylor J. L., Petersen N. T., Butler J. E., Gandevia S. C. (2002). Interaction of transcranial magnetic stimulation and electrical transmastoid stimulation in human subjects. J. Physiol. 541, 949–958 10.1113/jphysiol.2002.016782
    1. Thomas C. K., Bigland-Ritchie B., Westling G., Johansson R. S. (1990). A comparison of human thenar motor-unit properties studied by intraneural motor-axon stimulation and spike-triggered averaging. J. Neurophysiol. 64, 1347–1351
    1. Thomas C. K., Johansson R. S., Bigland-Ritchie B. (2002). Incidence of F waves in single human thenar motor units. Muscle Nerve 25, 77–82 10.1002/mus.10005
    1. Trontelj J. V. (1968). H-reflex of single motoneurons in man. Nature 220, 1043–1044
    1. Ugawa Y., Rothwell J. C., Day B. L., Thompson P. D., Marsden C. D. (1991). Percutaneous electrical stimulation of corticospinal pathways at the level of the pyramidal decussation in humans. Ann. Neurol. 29, 418–427 10.1002/ana.410290413
    1. Ugawa Y., Uesaka Y., Terao Y., Hanajima R., Kanazawa I. (1994). Magnetic stimulation of corticospinal pathways at the foramen magnum level in humans. Ann. Neurol. 36, 618–624 10.1002/ana.410360410
    1. Upton A. R., McComas A. J., Sica R. E. (1971). Potentiation of “late” responses evoked in muscles during effort. J. Neurol. Neurosurg. Psychiatry 34, 699–711
    1. Vagg R., Mogyoros I., Kiernan M. C., Burke D. (1998). Activity-dependent hyperpolarization of human motor axons produced by natural activity. J. Physiol. 507, 919–925 10.1111/j.1469-7793.1998.919bs.x
    1. Vila-Cha C., Falla D., Correia M. V., Farina D. (2012). Changes in H reflex and V wave following short-term endurance and strength training. J. Appl. Physiol. 112, 54–63 10.1152/japplphysiol.00802.2011
    1. Zehr E. P. (2002). Considerations for use of the Hoffmann reflex in exercise studies. Eur. J. Appl. Physiol. 86, 455–468 10.1007/s00421-002-0577-5

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