Abstract
The output from a motor nucleus is determined by the synaptic input to the motor neurons and their intrinsic properties. Here, we explore whether the source of synaptic inputs to the motor neurons (cats) and the age or post-stroke conditions (humans) may change the recruitment gain of the motor neuron pool. In cats, the size of Ia EPSPs in triceps surae motor neurons (input) and monosynaptic reflexes (MSRs; output) was recorded in the soleus and medial gastrocnemius motor nerves following graded stimulation of dorsal roots. The MSR was plotted against the EPSP thereby obtaining a measure of the recruitment gain. Conditioning stimulation of sural and peroneal cutaneous afferents caused significant increase in the recruitment gain of the medial gastrocnemius, but not the soleus motor neuron pool. In humans, the discharge probability of individual soleus motor units (input) and soleus H-reflexes (output) was performed. With graded stimulation of the tibial nerve, the gain of the motor neuron pool was assessed as the slope of the relation between probability of firing and the reflex size. The gain in young subjects was higher than in elderly subjects. The gain in post-stroke survivors was higher than in age-matched neurologically intact subjects. These findings provide experimental evidence that recruitment gain of a motor neuron pool contributes to the regulation of movement at the final output stage from the spinal cord and should be considered when interpreting changes in reflex excitability in relation to movement or injuries of the nervous system.
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References
Ashby P, Labelle K (1977) Effects of extensor and flexor group I afferent volleys on the excitability of individual soleus motoneurones in man. J Neurol Neurosurg Psychiatry 40:910–919
Ashby P, Zilm D (1982a) Characteristics of postsynaptic potentials produced in single human motoneurons by homonymous group 1 volleys. Exp Brain Res 47:41–48
Ashby P, Zilm D (1982b) Relationship between EPSP shape and cross-correlation profile explored by computer simulation for studies on human motoneurons. Exp Brain Res 47:33–40
Bawa P (2002) Neural control of motor output: can training change it? Exerc Sport Sci Rev 30:59–63
Bawa P, Lemon RN (1993) Recruitment of motor units in response to transcranial magnetic stimulation in man. J Physiol 471:445–464. https://doi.org/10.1113/jphysiol.1993.sp019909
Binder MD, Robinson FR, Powers RK (1998) Distribution of effective synaptic currents in cat triceps surae motoneurons. VI. Contralateral pyramidal tract. J Neurophysiol 80:241–248. https://doi.org/10.1152/jn.1998.80.1.241
Binder MD, Heckman CJ, Powers RK (2002) Relative strengths and distributions of different sources of synaptic input to the motoneurone pool: implications for motor unit recruitment. Adv Exp Med Biol 508:207–212
Burke RE (1967) Motor unit types of cat triceps surae muscle. J Physiol 193:141–160
Burke RE (1968) Group Ia synaptic input to fast and slow twitch motor units of cat triceps surae. J Physiol 196:605–630
Burke D (1988) Spasticity as an adaptation to pyramidal tract injury. Adv Neurol 47:401–423
Burke RE, Jankowska E, ten Bruggencate G (1970) A comparison of peripheral and rubrospinal synaptic input to slow and fast twitch motor units of triceps surae. J Physiol 207:709–732
Burke JR, Kamen G, Koceja DM (1989) Long-latency enhancement of quadriceps excitability from stimulation of skin afferents in young and old adults. J Gerontol 44:M158–M163
Butchart P, Farquhar R, Part NJ, Roberts RC (1993) The effect of age and voluntary contraction on presynaptic inhibition of soleus muscle Ia afferent terminals in man. Exp Physiol 78:235–242
Clough JF, Kernell D, Phillips CG (1968) The distribution of monosynaptic excitation from the pyramidal tract and from primary spindle afferents to motoneurones of the baboon’s hand and forearm. J Physiol 198:145–166. https://doi.org/10.1113/jphysiol.1968.sp008598
Crill WE, Schwindt P (1984) Ionic mechanisms underlying excitation-to-frequency transduction: studies by voltage clamp methods. Arch Ital Biol 122:31–41
Crone C, Hultborn H, Mazieres L, Morin C, Nielsen J, Pierrot-Deseilligny E (1990) Sensitivity of monosynaptic test reflexes to facilitation and inhibition as a function of the test reflex size: a study in man and the cat. Exp Brain Res 81:35–45
Crone C, Nielsen J, Petersen N, Ballegaard M, Hultborn H (1994) Disynaptic reciprocal inhibition of ankle extensors in spastic patients. Brain 117(Pt 5):1161–1168
Crone C, Petersen NT, Gimenez-Roldan S, Lungholt B, Nyborg K, Nielsen JB (2007) Reduced reciprocal inhibition is seen only in spastic limbs in patients with neurolathyrism. Exp Brain Res 181:193–197. https://doi.org/10.1007/s00221-007-0993-1
Deardorff AS, Romer SH, Sonner PM, Fyffe RE (2014) Swimming against the tide: investigations of the C-bouton synapse. Front Neural Circuits 8:106. https://doi.org/10.3389/fncir.2014.00106
Delwaide PJ, Oliver E (1988) Short-latency autogenic inhibition (IB inhibition) in human spasticity. J Neurol Neurosurg Psychiatry 51:1546–1550
Desmedt JE, Godaux E (1977a) Critical evaluation of the size principle of human motoneurons recruitment in ballistic movements and in vibration-induced inhibition or potentiation. Trans Am Neurol Assoc 102:104–108
Desmedt JE, Godaux E (1977b) Fast motor units are not preferentially activated in rapid voluntary contractions in man. Nature 267:717–719
deVries HA, Wiswell RA, Romero GT, Heckathorne E (1985) Changes with age in monosynaptic reflexes elicited by mechanical and electrical stimulation. Am J Phys Med 64:71–81
Eide E (1968) Input amplifier for intracellular potential and conductance measurements. Acta Physiol Scand 73:A1
Fetz EE, Gustafsson B (1983) Relation between shapes of post-synaptic potentials and changes in firing probability of cat motoneurones. J Physiol 341:387–410
Garcia-Mullin R, Mayer RF (1972) H reflexes in acute and chronic hemiplegia. Brain 95:559–572
Geertsen SS, Willerslev-Olsen M, Lorentzen J, Nielsen JB (2017) Development and aging of human spinal cord circuitries. J Neurophysiol 118:1133–1140. https://doi.org/10.1152/jn.00103.2017
Gollnick PD, Sjodin B, Karlsson J, Jansson E, Saltin B (1974) Human soleus muscle: a comparison of fiber composition and enzyme activities with other leg muscles. Pflugers Arch 348:247–255
Gowers WR (1886) A manual of diseases of the nervous system. J. & A. Churchill, London
Grey MJ, Klinge K, Crone C, Lorentzen J, Biering-Sorensen F, Ravnborg M, Nielsen JB (2008) Post-activation depression of soleus stretch reflexes in healthy and spastic humans. Exp Brain Res 185:189–197. https://doi.org/10.1007/s00221-007-1142-6
Gustafsson B, Pinter MJ (1985) Factors determining the variation of the after hyperpolarization duration in cat lumbar alpha-motoneurones. Brain Res 326:392–395
Heckman CJ, Lee RH, Brownstone RM (2003) Hyperexcitable dendrites in motoneurons and their neuromodulatory control during motor behavior. Trends Neurosci 26:688–695. https://doi.org/10.1016/j.tins.2003.10.002
Henneman E, Somjen G, Carpenter DO (1965) Functional Significance of Cell Size in Spinal Motoneurons. J Neurophysiol 28:560–580. https://doi.org/10.1152/jn.1965.28.3.560
Hounsgaard J, Hultborn H, Jespersen B, Kiehn O (1984) Intrinsic membrane properties causing a bistable behaviour of alpha-motoneurones. Exp Brain Res 55:391–394
Hultborn H, Denton ME, Wienecke J, Nielsen JB (2003) Variable amplification of synaptic input to cat spinal motoneurones by dendritic persistent inward current. J Physiol 552:945–952. https://doi.org/10.1113/jphysiol.2003.050971
Hultborn H, Brownstone RB, Toth TI, Gossard JP (2004) Key mechanisms for setting the input-output gain across the motoneuron pool. Prog Brain Res 143:77–95
Jahanmiri-Nezhad F, Hu X, Suresh NL, Rymer WZ, Zhou P (2014) EMG-force relation in the first dorsal interosseous muscle of patients with amyotrophic lateral sclerosis. NeuroRehabilitation 35:307–314. https://doi.org/10.3233/NRE-141125
Jones KE, Calancie B, Hall A, Bawa P (1996) Comparison of peripheral Ia and corticomotoneuronal composite EPSPs in human motoneurons. Electroencephalogr Clin Neurophysiol 101:431–437
Kanda K, Burke RE, Walmsley B (1977) Differential control of fast and slow twitch motor units in the decerebrate cat. Exp Brain Res 29:57–74
Kathe C, Hutson TH, McMahon SB, Moon LD (2016) Intramuscular Neurotrophin-3 normalizes low threshold spinal reflexes, reduces spasms and improves mobility after bilateral corticospinal tract injury in rats. Elife. https://doi.org/10.7554/eLife.18146
Kawamura Y, Dyck PJ (1977) Lumbar motoneurons of man: III. The number and diameter distribution of large- and intermediate-diameter cytons by nuclear columns. J Neuropathol Exp Neurol 36:956–963
Kawamura Y, O’Brien P, Okazaki H, Dyck PJ (1977) Lumbar motoneurons of man II: the number and diameter distribution of large- and intermediate-diameter cytons in “motoneuron columns” of spinal cord of man. J Neuropathol Exp Neurol 36:861–870
Kernell D, Hultborn H (1990) Synaptic effects on recruitment gain: a mechanism of importance for the input-output relations of motoneurone pools? Brain Res 507:176–179
Kido A, Tanaka N, Stein RB (2004) Spinal excitation and inhibition decrease as humans age. Can J Physiol Pharmacol 82:238–248. https://doi.org/10.1139/y04-017
LaBella LA, Kehler JP, McCrea DA (1989) A differential synaptic input to the motor nuclei of triceps surae from the caudal and lateral cutaneous sural nerves. J Neurophysiol 61:291–301. https://doi.org/10.1152/jn.1989.61.2.291
Lamy JC, Wargon I, Mazevet D, Ghanim Z, Pradat-Diehl P, Katz R (2009) Impaired efficacy of spinal presynaptic mechanisms in spastic stroke patients. Brain 132:734–748. https://doi.org/10.1093/brain/awn310
Larsson L, Ansved T (1995) Effects of ageing on the motor unit. Prog Neurobiol 45:397–458
Lexell J, Taylor CC, Sjostrom M (1988) What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84:275–294
Li Y, Gorassini MA, Bennett DJ (2004) Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J Neurophysiol 91:767–783. https://doi.org/10.1152/jn.00788.2003
Li X, Shin H, Zhou P, Niu X, Liu J, Rymer WZ (2014) Power spectral analysis of surface electromyography (EMG) at matched contraction levels of the first dorsal interosseous muscle in stroke survivors. Clin Neurophysiol 125:988–994. https://doi.org/10.1016/j.clinph.2013.09.044
Li X, Holobar A, Gazzoni M, Merletti R, Rymer WZ, Zhou P (2015) Examination of poststroke alteration in motor unit firing behavior using high-density surface EMG decomposition. IEEE Trans Biomed Eng 62:1242–1252. https://doi.org/10.1109/TBME.2014.2368514
Maffiuletti NA, Aagaard P, Blazevich AJ, Folland J, Tillin N, Duchateau J (2016) Rate of force development: physiological and methodological considerations. Eur J Appl Physiol 116:1091–1116. https://doi.org/10.1007/s00421-016-3346-6
Magladery JW, Teasdall RD, Park AM, Languth HW (1952) Electrophysiological studies of reflex activity in patients with lesions of the nervous system. I. A comparison of spinal motoneurone excitability following afferent nerve volleys in normal persons and patients with upper motor neurone lesions. Bull Johns Hopkins Hosp 91:219–244 passim
Mendell LM, Henneman E (1968) Terminals of single Ia fibers: distribution within a pool of 300 homonymous motor neurons. Science 160:96–98
Mendell LM, Henneman E (1971) Terminals of single Ia fibers: location, density, and distribution within a pool of 300 homonymous motoneurons. J Neurophysiol 34:171–187. https://doi.org/10.1152/jn.1971.34.1.171
Morita H, Olivier E, Baumgarten J, Petersen NT, Christensen LO, Nielsen JB (2000) Differential changes in corticospinal and Ia input to tibialis anterior and soleus motor neurones during voluntary contraction in man. Acta Physiol Scand 170:65–76. https://doi.org/10.1046/j.1365-201x.2000.00762.x
Mottram CJ, Suresh NL, Heckman CJ, Gorassini MA, Rymer WZ (2009) Origins of abnormal excitability in biceps brachii motoneurons of spastic-paretic stroke survivors. J Neurophysiol 102:2026–2038. https://doi.org/10.1152/jn.00151.2009
Muehlbauer T, Gollhofer A, Granacher U (2015) Associations between measures of balance and lower-extremity muscle strength/power in healthy individuals across the lifespan: a systematic review and meta-analysis. Sports Med 45:1671–1692. https://doi.org/10.1007/s40279-015-0390-z
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. https://doi.org/10.1111/j.1748-1716.1993.tb09515.x
Nielsen J, Hultborn H, Gossard J-P (1990) Changes of recruitment gain by stimulation of the caudal sural or superficial peroneal nerve in cat. Eur J Neurosci Suppl 3:193
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
Pollock LJ, Davis L (1923) Studies in decerebration I. A method of decerebration. Archiv Neurol Psychiatr 10:391–398
Powers RK, Robinson FR, Konodi MA, Binder MD (1993) Distribution of rubrospinal synaptic input to cat triceps surae motoneurons. J Neurophysiol 70:1460–1468. https://doi.org/10.1152/jn.1993.70.4.1460
Raffalt PC, Alkjaer T, Simonsen EB (2015) Changes in soleus H-reflex during walking in middle-aged, healthy subjects. Muscle Nerve 51:419–425. https://doi.org/10.1002/mus.24279
Sabbahi MA, Sedgwick EM (1982) Age-related changes in monosynaptic reflex excitability. J Gerontol 37:24–32
Scaglioni G, Narici MV, Maffiuletti NA, Pensini M, Martin A (2003) Effect of ageing on the electrical and mechanical properties of human soleus motor units activated by the H reflex and M wave. J Physiol 548:649–661. https://doi.org/10.1113/jphysiol.2002.032763
Schwindt P, Crill WE (1977) A persistent negative resistance in cat lumbar motoneurons. Brain Res 120:173–178
Scott JG, Mendell LM (1976) Individual EPSPs produced by single triceps surae Ia afferent fibers in homonymous and heteronymous motoneurons. J Neurophysiol 39:679–692. https://doi.org/10.1152/jn.1976.39.4.679
Sherrington CS (1906) The integrative action of the nervous system. Yale University Press
Suetta C, Aagaard P, Magnusson SP et al (2007) Muscle size, neuromuscular activation, and rapid force characteristics in elderly men and women: effects of unilateral long-term disuse due to hip-osteoarthritis. J Appl Physiol 102:942–948. https://doi.org/10.1152/japplphysiol.00067.2006
Suresh N, Li X, Zhou P, Rymer WZ (2011) Examination of motor unit control properties in stroke survivors using surface EMG decomposition: a preliminary report. Conf Proc IEEE Eng Med Biol Soc 2011:8243–8246. https://doi.org/10.1109/IEMBS.2011.6092032
Suresh NL, Concepcion NS, Madoff J, Rymer WZ (2015) Anomalous EMG-force relations during low-force isometric tasks in hemiparetic stroke survivors. Exp Brain Res 233:15–25. https://doi.org/10.1007/s00221-014-4061-3
Tomlinson BE, Irving D (1977) The numbers of limb motor neurons in the human lumbosacral cord throughout life. J Neurol Sci 34:213–219
Wright EA, Spink JM (1959) A study of the loss of nerve cells in the central nervous system in relation to age. Gerontologia 3:277–287
Zagoraiou L, Akay T, Martin JF, Brownstone RM, Jessell TM, Miles GB (2009) A cluster of cholinergic premotor interneurons modulates mouse locomotor activity. Neuron 64:645–662. https://doi.org/10.1016/j.neuron.2009.10.017
Acknowledgements
This work was supported by grants from the Danish Research Council and The Danish Society of Multiple Sclerosis. This work was funded by the Elsass Fonden (DK) (Grant No. 18-16).
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Nielsen, J.B., Morita, H., Wenzelburger, R. et al. Recruitment gain of spinal motor neuron pools in cat and human. Exp Brain Res 237, 2897–2909 (2019). https://doi.org/10.1007/s00221-019-05628-6
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DOI: https://doi.org/10.1007/s00221-019-05628-6