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A Simulation Study to Examine the Effect of Common Motoneuron Inputs on Correlated Patterns of Motor Unit Discharge

Journal of Computational Neuroscience volume 19, pages 107–124 (2005)Cite this article

Abstract

The influence of common oscillatory inputs to the motoneuron pool on correlated patterns of motor unit discharge was examined using model simulations. Motor unit synchronization, in-phase fluctuations in mean firing rates known as ‘common drive’, and the coefficient of variation of the muscle force were examined as the frequency and amplitude of common oscillatory inputs to the motoneuron pool were varied. The amount of synchronization, the peak correlation between mean firing rates and the coefficient of variation of the force varied with both the frequency and amplitude of the common input signal. Values for ‘common drive’ and the force coefficient of variation were highest for oscillatory inputs at frequencies less than 5 Hz, while synchronization reached a maximum when the frequency of the common input was close to the average motor unit firing rate. The frequency of the common input signal for which the highest levels of synchronization were observed increased as motoneuron firing rates increased in response to higher target force levels. The simulation results suggest that common low-frequency oscillations in motor unit firing rates and short-term synchronization result from oscillatory activity in different bands of the frequency spectrum of shared motoneuron inputs. The results also indicate that the amount of synchronization between motor unit discharges depends not only on the amplitude of the shared input signal, but also on its frequency in relation to the present firing rates of the individual motor units.

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References

  • Adams L, Datta AK, Guz A (1989) Synchronization of motor unit firing during different respiratory and postural tasks in human sternocleidomastoid muscle. J. Physiol. 413: 213–231.

    PubMed  Google Scholar 

  • Bakels R, Kernell D (1993) Matching between motoneurone and muscle unit properties in rat medial gastrocnemius. J. Physiol. 463: 307–324.

    PubMed  Google Scholar 

  • Baker SN, Lemon RN (1998) Computer simulation of post-spike facilitation in spike-triggered averages of rectified EMG. J. Neurophysiol. 80: 1391–1406.

    PubMed  Google Scholar 

  • Baker SN, Olivier E, Lemon RN (1997) Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation. J. Physiol. 501 (Pt 1): 225–241.

    Article  PubMed  Google Scholar 

  • Baldissera F, Gustafsson B (1974) Firing behaviour of a neurone model based on the afterhyperpolarization conductance time course. First interval firing. Acta Physiologica Scandinavica 91: 528–544.

    Google Scholar 

  • Binder MD, Powers RK (2001) Relationship between simulated common synaptic input and discharge synchrony in cat spinal motoneurons. J. Neurophysiol. 86: 2266–2275.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Bremner FD, Baker JR, Stephens JA (1991) Correlation between the discharges of motor units recorded from the same and from different finger muscles in man. J. Physiol. 432: 355– 380.

    PubMed  Google Scholar 

  • Calvin WH, Stevens CF (1968) Synaptic noise and other sources of randomness in motoneuron interspike intervals. J. Neurophysiol. 31: 574–587.

    PubMed  Google Scholar 

  • Carpentier A, Duchateau J, Hainaut K (2001) Motor unit behaviour and contractile changes during fatigue in the human first dorsal interosseus. J. Physiol. 534: 903–912.

    Article  PubMed  Google Scholar 

  • Carr LJ, Harrison LM, Stephens JA (1994) Evidence for bilateral innervation of certain homologous motoneurone pools in man. J. Physiol. 475: 217–227.

    PubMed  Google Scholar 

  • Datta AK, Stephens JA (1990) Synchronization of motor unit activity during voluntary contraction in man. J. Physiol. 422: 397–419.

    PubMed  Google Scholar 

  • Davey NJ, Ellaway PH, Friedland CL, Short DJ (1990) Motor unit discharge characteristics and short term synchrony in paraplegic humans. Journal of Neurology, Neurosurgery and Psychiatry 53: 764–769.

    Google Scholar 

  • De Luca CJ, Erim Z (1994) Common drive of motor units in regulation of muscle force. Trends in Neurosci. 17: 299–305.

    Article  Google Scholar 

  • De Luca CJ, Roy AM, Erim Z (1993) Synchronization of motor-unit firings in several human muscles. J. Neurophysiol. 70: 2010–2023.

    PubMed  Google Scholar 

  • De Luca CJ, Foley PJ, Erim Z (1996) Motor unit control properties in constant-force isometric contractions. J. Neurophysiol. 76: 1503–1516.

    PubMed  Google Scholar 

  • De Luca CJ, LeFever RS, McCue MP, Xenakis AP (1982) Control scheme governing concurrently active human motor units during voluntary contractions. J. Physiol. 329: 129–142.

    PubMed  Google Scholar 

  • Ellaway PH (1978) Cumulative sum technique and its application to the analysis of peristimulus time histograms. Electroencephalography and Clinical Neurophysiol. 45: 302– 304.

    Article  Google Scholar 

  • Erim Z, Beg MF, Burke DT, de Luca CJ (1999) Effects of aging on motor-unit control properties. J. Neurophysiol. 82: 2081–2091.

    PubMed  Google Scholar 

  • Farmer SF, Bremner FD, Halliday DM, Rosenberg JR, Stephens JA (1993) The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. J. Physiol. 470: 127–155.

    PubMed  Google Scholar 

  • Farmer SF, Sheean GL, Mayston MJ, Rothwell JC, Marsden CD, Conway BA, Halliday DM, Rosenberg JR, Stephens JA (1998) Abnormal motor unit synchronization of antagonist muscles underlies pathological co-contraction in upper limb dystonia. Brain 121 (Pt 5): 801–814.

    Article  PubMed  Google Scholar 

  • Fuglevand AJ, Winter DA, Patla AE (1993) Models of recruitment and rate coding organization in motor-unit pools. J. Neurophysiol. 70: 2470–2488.

    PubMed  Google Scholar 

  • Garland SJ, Miles TS (1997) Control of motor units in human flexor digitorum profundus under different proprioceptive conditions. J. Physiol. 502 (Pt 3): 693–701.

    Article  PubMed  Google Scholar 

  • Gossen ER, Ivanova TD, Garland SJ (2003) The time course of the motoneurone afterhyperpolarization is related to motor unit twitch speed in human skeletal muscle. J. Physiol. 552: 657–664.

    Article  PubMed  Google Scholar 

  • Gustafsson B, Pinter MJ (1984) An investigation of threshold properties among cat spinal alpha-motoneurones. J. Physiol. 357: 453–483.

    PubMed  Google Scholar 

  • Halliday DM (2000) Weak, stochastic temporal correlation of large scale synaptic input is A major determinant of neuronal bandwidth. Neural Comput. 12: 693–707.

    Article  PubMed  Google Scholar 

  • Heckman CJ, Binder MD (1991) Computer simulation of the steady-state input-output function of the cat medial gastrocnemius motoneuron pool. J. Neurophysiol. 65: 952–967.

    PubMed  Google Scholar 

  • Henneman E (1957) Relation between size of neurons and their susceptability to discharge. Science 126: 1345–1347.

    PubMed  Google Scholar 

  • Hultborn H, Katz R, Mackel R (1988) Distribution of recurrent inhibition within a motor nucleus. II. Amount of recurrent inhibition in motoneurones to fast and slow units. Acta Physiologica Scandinavica 134: 363–374.

    PubMed  Google Scholar 

  • Kamen G, De Luca CJ (1992) Firing rate interactions among human orbicularis oris motor units. International J. Neurosci. 64: 167–175.

    Google Scholar 

  • Kamen G, Greenstein SS, De Luca CJ (1992) Lateral dominance and motor unit firing behavior. Brain Res 576: 165–167.

    Article  PubMed  Google Scholar 

  • Keen DA, Fuglevand AJ (2004) Common input to motor neurons innervating the same and different compartments of the human extensor digitorum muscle. J. Neurophysiol. 91: 57–62.

    Article  PubMed  Google Scholar 

  • Kernell D (1968) The repetitive impulse discharge of a simple neurone model compared to that of spinal motoneurones. Brain Res 11: 685–687.

    Article  PubMed  Google Scholar 

  • Kernell D, Eerbeek O, Verhey BA (1983) Relation between isometric force and stimulus rate in cat’s hindlimb motor units of different twitch contraction time. Exp. Brain Res. 50: 220–227.

    PubMed  Google Scholar 

  • Kirkwood PA, Sears TA, Tuck DL, Westgaard RH (1982) Variations in the time course of the synchronization of intercostal motoneurones in the cat. J. Physiol. 327: 105–135.

    PubMed  Google Scholar 

  • Kossev A, Elek JM, Wohlfarth K, Schubert M, Dengler R, Wolf W (1994) Assessment of human motor unit twitches—a comparison of spike-triggered averaging and intramuscular microstimulation. Electroencephalography and Clinical Neurophysiol. 93: 100–105.

    Article  Google Scholar 

  • Lemon RN (1993) The G. L. Brown Prize Lecture. Cortical control of the primate hand. Exp. Physiol. 78: 263–301.

    Google Scholar 

  • Mattei B, Schmied A, Mazzocchio R, Decchi B, Rossi A, Vedel JP (2003) Pharmacologically induced enhancement of recurrent inhibition in humans: effects on motoneurone discharge patterns. J. Physiol. 548: 615–629.

    Article  PubMed  Google Scholar 

  • Matthews PB (1996) Relationship of firing intervals of human motor units to the trajectory of post-spike after-hyperpolarization and synaptic noise. J. Physiol. 492 (Pt 2): 597–628.

    PubMed  Google Scholar 

  • Matthews PB (1997) Spindle and motoneuronal contributions to the phase advance of the human stretch reflex and the reduction of tremor. J. Physiol. 498 (Pt 1): 249–275.

    PubMed  Google Scholar 

  • McAuley JH, Rothwell JC, Marsden CD (1997). Frequency peaks of tremor, muscle vibration and electromyographic activity at 10, 20 and 40 Hz during human finger muscle contraction may reflect rhythmicities of central neural firing. Experimental Brain Res. 114: 525–541.

    Google Scholar 

  • McNulty PA, Falland KJ, Macefield VG (2000) Comparison of contractile properties of single motor units in human intrinsic and extrinsic finger muscles. J. Physiol. 526 (Pt 2): 445– 456.

    Article  PubMed  Google Scholar 

  • Milner-Brown HS, Stein RB, Yemm R (1973) The contractile properties of human motor units during voluntary isometric contractions. J. Physiol. 228: 285–306.

    PubMed  Google Scholar 

  • Murthy VN, Fetz EE (1996) Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. J. Neurophysiol. 76: 3968–3982.

    PubMed  Google Scholar 

  • Myers L, Erim Z, Lowery MM (2004) Time and frequency domain methods for quantifying common modulation of motor unit firing patterns. J. Neuroengineering and Rehabilitation 1: 2.

    Google Scholar 

  • Nielsen J, Kagamihara Y (1994) Synchronization of human leg motor units during co-contraction in man. Experimental Brain Research 102: 84–94.

    Google Scholar 

  • Nordstrom MA, Fuglevand AJ, Enoka RM (1992) Estimating the strength of common input to human motoneurons from the cross-correlogram. J. Physiol. 453: 547–574.

    PubMed  Google Scholar 

  • Nussbaumer RM, Ruegg DG, Studer LM, Gabriel JP (2002) Computer simulation of the motoneuron pool-muscle complex. I. Input system and motoneuron pool. Biological Cybernetics 86: 317–333.

    Article  PubMed  Google Scholar 

  • Person RS, Kudina LP (1972) Discharge frequency and discharge pattern of human motor units during voluntary contraction of muscle. Electroencephalography and Clinical Neurophysiol. 32: 471–483.

    Article  Google Scholar 

  • Powers RK (1993) A variable-threshold motoneuron model that incorporates time- and voltage-dependent potassium and calcium conductances. J. Neurophysiol. 70: 246–262.

    PubMed  Google Scholar 

  • Powers RK, Binder MD (1996) Experimental evaluation of input-output models of motoneuron discharge. J. Neurophysiol. 75: 367–379.

    PubMed  Google Scholar 

  • Powers RK, Binder MD (2000) Relationship between the time course of the afterhyperpolarization and discharge variability in cat spinal motoneurones. J. Neurophysiol. 528 Pt 1: 131–150.

    Google Scholar 

  • Powers RK, Vanden Noven S, Rymer WZ (1989) Evidence of shared, direct input to motoneurons supplying synergist muscles in humans. Neurosci. Lett. 102: 76–81.

    Article  PubMed  Google Scholar 

  • Schmied A, Vedel JP, Pagni S (1994) Human spinal lateralization assessed from motoneurone synchronization: dependence on handedness and motor unit type. J. Physiol. 480 (Pt 2): 369– 387.

    PubMed  Google Scholar 

  • Schmied A, Pagni S, Sturm H, Vedel JP (2000) Selective enhancement of motoneurone short-term synchrony during an attention-demanding task. Exp. Brain Res. 133: 377– 390.

    Article  PubMed  Google Scholar 

  • Sears TA, Stagg D (1976) Short-term synchronization of intercostal motoneurone activity. J. Physiol. 263: 357–381.

    PubMed  Google Scholar 

  • Semmler JG, Nordstrom MA (1995) Influence of handedness on motor unit discharge properties and force tremor. Exp. Brain Res. 104: 115–125.

    Article  PubMed  Google Scholar 

  • Semmler JG, Nordstrom MA (1998) Motor unit discharge and force tremor in skill- and strength-trained individuals. Exp. Brain Res. 119: 27–38.

    Article  PubMed  Google Scholar 

  • Semmler JG, Nordstrom MA (1999) A comparison of cross-correlation and surface EMG techniques used to quantify motor unit synchronization in humans. J. Neurosci. Methods 90: 47–55.

    Article  PubMed  Google Scholar 

  • Slifkin AB, Vaillancourt DE, Newell KM (2000) Intermittency in the control of continuous force production. J. Neurophysiol. 84: 1708–1718.

    PubMed  Google Scholar 

  • Spauschus A, Marsden J, Halliday DM, Rosenberg JR, Brown P (1999) The origin of ocular microtremor in man. Exp. Brain Res. 126: 556–562.

    Article  PubMed  Google Scholar 

  • Svirskis G, Hounsgaard J (2003) Influence of membrane properties on spike synchronization in neurons: Theory and experiments. Network-Computation in Neural Systems 14: 747– 763.

    Article  Google Scholar 

  • Tanji J, Kato M (1973) Firing rate of individual motor units in voluntary contraction of abductor digiti minimi muscle in man. Exp. Neurology 40: 771–783.

    Article  Google Scholar 

  • Taylor AM, Enoka RM (2004) Quantification of the factors that influence discharge correlation in model motor neurons. J. Neurophysiol. 91: 796–814.

    Article  PubMed  Google Scholar 

  • Turker KS, Powers RK (2001) Effects of common excitatory and inhibitory inputs on motoneuron synchronization. J. Neurophysiol. 86: 2807–2822.

    PubMed  Google Scholar 

  • Turker KS, Powers RK (2002) The effects of common input characteristics and discharge rate on synchronization in rat hypoglossal motoneurones. J. Physiol. 541: 245–260.

    Article  PubMed  Google Scholar 

  • Yao W, Fuglevand RJ, Enoka RM (2000) Motor-unit synchronization increases EMG amplitude and decreases force steadiness of simulated contractions. J. Neurophysiol. 83: 441–452.

    PubMed  Google Scholar 

  • Zengel JE, Reid SA, Sypert GW, Munson JB (1985) Membrane electrical properties and prediction of motor-unit type of medial gastrocnemius motoneurons in the cat. J. Neurophysiol. 53: 1323–1344.

    PubMed  Google Scholar 

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Affiliations

  1. Sensory Motor Performance Program, Rehabilitation Institute of Chicago, Illinois, USA

    Madeleine M. Lowery & Zeynep Erim

  2. Department of Physical Medicine and Rehabilitation, Northwestern University, Illinois, USA

    Madeleine M. Lowery & Zeynep Erim

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  1. Madeleine M. Lowery
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  2. Zeynep Erim
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Correspondence to Madeleine M. Lowery.

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Lowery, M.M., Erim, Z. A Simulation Study to Examine the Effect of Common Motoneuron Inputs on Correlated Patterns of Motor Unit Discharge. J Comput Neurosci 19, 107–124 (2005). https://doi.org/10.1007/s10827-005-0898-6

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  • DOI: https://doi.org/10.1007/s10827-005-0898-6

Keywords

  • motor unit
  • synchronization
  • common drive
  • model