Skip to main content
SpringerLink
Log in
Book cover

Progress in Motor Control pp 33–40Cite as

Reconfiguration of the Electrical Properties of Motoneurons to Match the Diverse Demands of Motor Behavior

  • Conference paper
  • First Online:

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 826))

Abstract

Though long considered simple “threshold and fire” cells, motoneurons are now known to exhibit a wide range of electrical states. These state changes are induced by the interactions between three types of inputs: neuromodulatory, inhibitory, and N-methyl-d-aspartate (NMDA)-mediated. Perhaps the strongest neuromodulators are serotonin (5HT) and norepinephrine (NE), which are released by axons descending from the brainstem. Motoneurons are densely covered in synapses from both systems. Local neuromodulatory systems within the spinal cord also have strong effects. Generally, these neuromodulatory systems greatly enhance the excitability of motoneurons, increasing their input–output gain. Local inhibitory inputs may be able to reduce motoneuron gain by deactivating the persistent inward currents that are so strongly facilitated by 5HT and NE. The glutamate NMDA receptor tends to induce oscillatory behaviors and has recently been demonstrated to be strongly present in adult motoneurons. We propose that the interactions of these inputs can induce three different states in motoneurons: integration, variable gain amplification, and oscillation. We further suggest that these states are matched to the following motor behaviors: posture, volitional movements, and locomotion.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Aston-Jones G, Chen S, Zhu Y, Oshinsky ML. 2001. A neural circuit for circadian regulation of arousal. Nat Neurosci 4:732–738.

    Article  PubMed  CAS  Google Scholar 

  • Baldissera F, Hultborn H, Illert M. 1981. Integration in spinal neuronal systems. In: Brooks VB, editor. Handbook of Physiology. The Nervous System. Motor Control. Bethesda: American Physiological Society. pp. 509–595.

    Google Scholar 

  • Bennett DJ, Hultborn H, Fedirchuk B, Gorassini M. 1998. Synaptic activation of plateaus in hindlimb motoneurons of decerebrate cats. J Neurophysiol 80:2023–2037.

    PubMed  CAS  Google Scholar 

  • Bui TV, Grande G, Rose PK. 2008a. Relative location of inhibitory synapses and persistent inward currents determines the magnitude and mode of synaptic amplification in motoneurons. J Neurophysiol 99:583–594.

    Article  Google Scholar 

  • Bui TV, Grande G, Rose PK. 2008b. Multiple modes of amplification of synaptic inhibition to motoneurons by persistent inward currents. J Neurophysiol 99:571–582.

    Article  Google Scholar 

  • Cushing S, Bui T, Rose PK. 2005. Effect of nonlinear summation of synaptic currents on the input-output properties of spinal motoneurons. J Neurophysiol 94:3465–3478.

    Article  PubMed  CAS  Google Scholar 

  • Enriquez Denton M, Wienecke J, Zhang M, Hultborn H, Kirkwood PA. 2012. Voltage-dependent amplification of synaptic inputs in respiratory motoneurones. J Physiol 590:3067–3090.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Garraway SM, Hochman S. 2001. Modulatory actions of serotonin, norepinephrine, dopamine, and acetylcholine in spinal cord deep dorsal horn neurons. J Neurophysiol 86:2183–2194.

    PubMed  CAS  Google Scholar 

  • Harris-Warrick RM. 2011. Neuromodulation and flexibility in Central Pattern Generator networks. Curr Opin Neurobiol 21:685–692.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Heckman CJ, Enoka RM. 2012. Motor Unit. Compr Physiol 2:2629–2682.

    PubMed  CAS  Google Scholar 

  • Heckman CJ, Hyngstrom AS, Johnson MD. 2008. Active properties of motoneurone dendrites: diffuse descending neuromodulation, focused local inhibition. J Physiol 586:1225–1231.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hille B. 2001. Ionic Channels of Excitable Membranes, 3rd Edition. Sunderland, MA: Sinauer Assoc. Inc.

    Google Scholar 

  • Hochman S, Jordan LM, Schmidt BJ. 1994. TTX-resistant NMDA receptor-mediated voltage oscillations in mammalian lumbar motoneurons. J Neurophysiol 72:2559–2562.

    PubMed  CAS  Google Scholar 

  • Holstege JC, Kuypers HG. 1987. Brainstem projections to spinal motoneurons: an update. Neurosci 23:809–821.

    Article  CAS  Google Scholar 

  • Hornby TG, McDonagh JC, Reinking RM, Stuart DG. 2002. Motoneurons: a preferred firing range across vertebrate species? Muscle Nerve 25:632–648.

    Article  PubMed  Google Scholar 

  • Hounsgaard J, Hultborn H, Jespersen B, Kiehn O. 1988. Bistability of alpha-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J Physiol 405:345–367.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hultborn H. 2002. Plateau potentials and their role in regulating motoneuronal firing. Adv Exp Med Biol 508:213–218.

    Article  PubMed  Google Scholar 

  • Hultborn H, Lindstrom S, Wigstrom H. 1979. On the function of recurrent inhibition in the spinal cord. Exp Brain Res 37:399–403.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jacobs BL, Martin-Cora FJ, Fornal CA. 2002. Activity of medullary serotonergic neurons in freely moving animals. Brain Res Rev 40:45–52.

    Article  PubMed  CAS  Google Scholar 

  • Jankowska E. 2001. Spinal interneuronal systems: identification, multifunctional character and reconfigurations in mammals. J Physiol 533:31–40.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Johnson MD, Heckman CJ. 2010. Interactions between focused synaptic inputs and diffuse neuromodulation in the spinal cord. Ann NY Acad Sci 1198:35–41.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kuo JJ, Lee RH, Johnson MD, Heckman HM, Heckman CJ. 2003. Active dendritic integration of inhibitory synaptic inputs in vivo. J Neurophysiol 90:3617–3624.

    Article  PubMed  Google Scholar 

  • Lee RH, Heckman CJ. 1996. Influence of voltage-sensitive dendritic conductances on bistable firing and effective synaptic current in cat spinal motoneurons in vivo. J Neurophysiol 76:2107–2110.

    PubMed  CAS  Google Scholar 

  • Lee RH, Heckman CJ. 1998a. Bistability in spinal motoneurons in vivo: systematic variations in rhythmic firing patterns. J Neurophysiol 80:572–582.

    CAS  Google Scholar 

  • Lee RH, Heckman CJ. 1998b. Bistability in spinal motoneurons in vivo: systematic variations in persistent inward currents. J Neurophysiol 80:583–593.

    CAS  Google Scholar 

  • Lee RH, Heckman CJ. 1999. Enhancement of bistability in spinal motoneurons in vivo by the noradrenergic alpha(1) agonist methoxamine. J Neurophysiol 81:2164–2174.

    PubMed  CAS  Google Scholar 

  • Lee RH, Heckman CJ. 2000. Adjustable amplification of synaptic input in the dendrites of spinal motoneurons in vivo. J Neurosci 20:6734–6740.

    PubMed  CAS  Google Scholar 

  • Li X, Murray K, Harvey PJ, Ballou EW, Bennett DJ. 2007. Serotonin facilitates a persistent calcium current in motoneurons of rats with and without chronic spinal cord injury. J Neurophysiol 97:1236–1246.

    Article  PubMed  CAS  Google Scholar 

  • Lindsay AD, Binder MD. 1991. Distribution of effective synaptic currents underlying recurrent inhibition in cat triceps surae motoneurons. J Neurophysiol 65:168–177.

    PubMed  CAS  Google Scholar 

  • MacLean JN, Schmidt BJ, Hochman S.1997. NMDA receptor activation triggers voltage oscillations, plateau potentials and bursting in neonatal rat lumbar motoneurons in vitro. Eur J Neurosci 9:2702–2711.

    Article  PubMed  CAS  Google Scholar 

  • Manuel M, Li Y, Elbasiouny SM, Murray K, Griener A et al. 2012. NMDA induces persistent inward and outward currents that cause rhythmic bursting in adult rodent motoneurons. J Neurophysiol 108:2991–2998.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Miller JF, Paul KD, Lee RH, Rymer WZ, Heckman CJ. 1996. Restoration of extensor excitability in the acute spinal cat by the 5-HT2 agonist DOI. J Neurophysiol 75:620–628.

    PubMed  CAS  Google Scholar 

  • Montague SJ, Fenrich KK, Mayer-Macaulay C, Maratta R, Neuber-Hess MS et al. 2013. Nonuniform distribution of contacts from noradrenergic and serotonergic boutons on the dendrites of cat splenius motoneurons. J Comp Neurol 521:638–656.

    Article  PubMed  CAS  Google Scholar 

  • Power KE, McCrea DA, Fedirchuk B. 2010. Intraspinally mediated state-dependent enhancement of motoneurone excitability during fictive scratch in the adult decerebrate cat. J Physiol 588:2839–2857.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Powers RK, Binder MD. 2001. Input-output functions of mammalian motoneurons. Rev Physiol Biochem Pharmacol 143:137–263.

    Article  PubMed  CAS  Google Scholar 

  • Prather JF, Powers RK, Cope TC. 2001. Amplification and linear summation of synaptic effects on motoneuron firing rate. J Neurophysiol 85:43–53.

    PubMed  CAS  Google Scholar 

  • Svirskis G, Hounsgaard J. 1998. Transmitter regulation of plateau properties in turtle motoneurons. J Neurophysiol 79:45–50.

    PubMed  CAS  Google Scholar 

  • Wang D, Grillner S, Wallen P. 2013. Calcium dynamics during NMDA-induced membrane potential oscillations in lamprey spinal neurons—contribution of L-type calcium channels (CaV1.3). J Physiol 591(Pt 10):2509–2521.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zagoraiou L, Akay T, Martin JF, Brownstone RM, Jessell TM et al. 2009. A cluster of cholinergic premotor interneurons modulates mouse locomotor activity. Neuron 64:645–662.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhu H, Clemens S, Sawchuk M, Hochman S. 2007. Expression and distribution of all dopamine receptor subtypes (D(1)-D(5)) in the mouse lumbar spinal cord: a real-time polymerase chain reaction and non-autoradiographic in situ hybridization study. Neurosci 149:885–897.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The studies supporting the work reviewed here were supported by NIH NINDS grants NS034382, NS071951, and NS077863. The authors thank Rochelle Bright for assistance with writing.

Author information

Authors and Affiliations

  1. Departments of Physiology, Physical Medicine and Rehabilitation, Physical Therapy and Human Movement Sciences, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA

    C. J. Heckman & Michael D. Johnson

Authors
  1. C. J. Heckman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael D. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. J. Heckman .

Editor information

Editors and Affiliations

  1. School of Physical and Occupational Therapy, McGill University, Montreal, Québec, Canada

    Mindy F. Levin

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this paper

Cite this paper

Heckman, C., Johnson, M. (2014). Reconfiguration of the Electrical Properties of Motoneurons to Match the Diverse Demands of Motor Behavior. In: Levin, M. (eds) Progress in Motor Control. Advances in Experimental Medicine and Biology, vol 826. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1338-1_3

Download citation

Publish with us

Policies and ethics

Search

Navigation