Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Intrinsic electrical properties of spinal motoneurons vary with joint angle

Nature Neuroscience volume 10, pages 363–369 (2007)Cite this article

Abstract

The dendrites of spinal motoneurons amplify synaptic inputs to a marked degree through persistent inward currents (PICs). Dendritic amplification is subject to neuromodulatory control from the brainstem by axons releasing the monoamines serotonin and norepinephrine; however, the monoaminergic projection to the cord is diffusely organized and does not allow independent adjustment of amplification in different motor pools. Using in vivo voltage-clamp techniques, here we show that dendritic PICs in ankle extensor motoneurons in the cat are reduced about 50% by small rotations (±10°) of the ankle joint. This reduction is primarily due to reciprocal inhibition, a tightly focused input shared only among strict muscle antagonists. These results demonstrate how a specific change in limb position can regulate intrinsic cellular properties set by a background of diffuse descending neuromodulation.

Access through your institution
Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The hindlimb and the robotic arm.
Figure 2: Ankle joint positions during the reciprocal inhibition intact condition.
Figure 3: Modulation of PIC amplitude as a function of ankle joint position in the reciprocal inhibition intact condition.
Figure 4: PIC amplitude as a function of joint position for the reciprocal inhibition intact and diminished conditions.
Figure 5: Leak-subtracted I-V relationship of one cell from the reciprocal inhibition diminished condition.

Similar content being viewed by others

References

  1. Lee, R.H. & Heckman, C.J. Influence of voltage-sensitive dendritic conductances on bistable firing and effective synaptic current in cat spinal motoneurons in vivo. J. Neurophysiol. 76, 2107–2110 (1996).

    Article  CAS  Google Scholar 

  2. Hounsgaard, J. & Kiehn, O. Calcium spikes and calcium plateaux evoked by differential polarization in dendrites of turtle motoneurones in vitro. J. Physiol. (Lond.) 468, 245–259 (1993).

    Article  CAS  Google Scholar 

  3. Bennett, D.J., Hultborn, H., Fedirchuk, B. & Gorassini, M. Synaptic activation of plateaus in hindlimb motoneurons of decerebrate cats. J. Neurophysiol. 80, 2023–2037 (1998).

    Article  CAS  Google Scholar 

  4. Carlin, K.P., Jones, K.E., Jiang, Z., Jordan, L.M. & Brownstone, R.M. Dendritic L-type calcium currents in mouse spinal motoneurons: implications for bistability. Eur. J. Neurosci. 12, 1635–1646 (2000).

    Article  CAS  Google Scholar 

  5. Heckman, C.J., Lee, R.H. & Brownstone, R.M. Hyperexcitable dendrites in motoneurons and their neuromodulatory control during motor behavior. Trends Neurosci. 26, 688–695 (2003).

    Article  CAS  Google Scholar 

  6. Hultborn, H., Brownstone, R.B., Toth, T.I. & Gossard, J.P. Key mechanisms for setting the input-output gain across the motoneuron pool. Prog. Brain Res. 143, 77–95 (2004).

    PubMed  Google Scholar 

  7. Alaburda, A., Perrier, J.F. & Hounsgaard, J. Mechanisms causing plateau potentials in spinal motoneurones. Adv. Exp. Med. Biol. 508, 219–226 (2002).

    Article  Google Scholar 

  8. Hultborn, H., Denton, M.E., Wienecke, J. & Nielsen, J.B. Variable amplification of synaptic input to cat spinal motoneurones by dendritic persistent inward current. J. Physiol. (Lond.) 552, 945–952 (2003).

    Article  CAS  Google Scholar 

  9. Lee, R.H. & Heckman, C.J. Adjustable amplification of synaptic input in the dendrites of spinal motoneurons in vivo. J. Neurosci. 20, 6734–6740 (2000).

    Article  CAS  Google Scholar 

  10. Cushing, S., Bui, T. & Rose, P.K. Effect of nonlinear summation of synaptic currents on the input-output properties of spinal motoneurons. J. Neurophysiol. 94, 3465–3478 (2005).

    Article  CAS  Google Scholar 

  11. Jacobs, B.L., Martin-Cora, F.J. & Fornal, C.A. Activity of medullary serotonergic neurons in freely moving animals. Brain Res. Brain Res. Rev. 40, 45–52 (2002).

    Article  CAS  Google Scholar 

  12. Aston-Jones, G., Chen, S., Zhu, Y. & Oshinsky, M.L. A neural circuit for circadian regulation of arousal. Nat. Neurosci. 4, 732–738 (2001).

    Article  CAS  Google Scholar 

  13. Björklund, A. & Skagerberg, G. Descending monoaminergic projections to the spinal cord. in Brain Stem Control of Spinal Mechanisms (eds. Sjolund, B. & Bjorklund, A.) 55–88 (Elsevier Biomedical Press, Amsterdam, 1982).

    Google Scholar 

  14. Kuo, J.J., Lee, R.H., Johnson, M.D., Heckman, H.M. & Heckman, C.J. Active dendritic integration of inhibitory synaptic inputs in vivo. J. Neurophysiol. 90, 3617–3624 (2003).

    Article  Google Scholar 

  15. Fyffe, R.E.W. Spinal motoneurons: synaptic inputs and receptor organization. in Motor Biology of the Spinal Cord (ed. Cope, T.C.) 21–46 (CRC, London, 2001).

    Chapter  Google Scholar 

  16. Hounsgaard, J., Hultborn, H., Jespersen, B. & Kiehn, O. Bistability of α-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J. Physiol. (Lond.) 405, 345–367 (1988).

    Article  Google Scholar 

  17. Lee, R.H., Kuo, J.J., Jiang, M.C. & Heckman, C.J. Influence of active dendritic currents on input-output processing in spinal motoneurons in vivo. J. Neurophysiol. 89, 27–39 (2003).

    Article  CAS  Google Scholar 

  18. Lee, R.H. & Heckman, C.J. Bistability in spinal motoneurons in vivo: systematic variations in rhythmic firing patterns. J. Neurophysiol. 80, 572–582 (1998).

    Article  CAS  Google Scholar 

  19. Lee, R.H. & Heckman, C.J. Bistability in spinal motoneurons in vivo: systematic variations in persistent inward currents. J. Neurophysiol. 80, 583–593 (1998).

    Article  CAS  Google Scholar 

  20. Jankowska, E. Interneuronal relay in spinal pathways from proprioceptors. Prog. Neurobiol. 38, 335–378 (1992).

    Article  CAS  Google Scholar 

  21. Nichols, T.R., Cope, T.C. & Abelew, T.A. Rapid spinal mechanisms of motor coordination. Exerc. Sport. Sci. Rev. 27, 255–284 (1999).

    Article  CAS  Google Scholar 

  22. Svirskis, G. & Hounsgaard, J. Depolarization-induced facilitation of a plateau-generating current in ventral horn neurons in the turtle spinal cord. J. Neurophysiol. 78, 1740–1742 (1997).

    Article  CAS  Google Scholar 

  23. Bennett, D.J., Hultborn, H., Fedirchuk, B. & Gorassini, M. Short-term plasticity in hindlimb motoneurons of decerebrate cats. J. Neurophysiol. 80, 2038–2045 (1998).

    Article  CAS  Google Scholar 

  24. Powers, R.K. & Binder, M.D. Input-output functions of mammalian motoneurons. Rev. Physiol. Biochem. Pharmacol. 143, 137–263 (2001).

    Article  CAS  Google Scholar 

  25. Rose, P.K., Keirstead, S.A. & Vanner, S.J. A quantitative analysis of the geometry of cat motoneurons innervating neck and shoulder muscles. J. Comp. Neurol. 239, 89–107 (1985).

    Article  CAS  Google Scholar 

  26. Cullheim, S., Fleshman, J.W., Glenn, L.L. & Burke, R.E. Three-dimensional architecture of dendritic trees in type-identified α-motoneurons. J. Comp. Neurol. 255, 82–96 (1987).

    Article  CAS  Google Scholar 

  27. LaBella, L.A. & McCrea, D.A. Evidence for restricted central convergence of cutaneous afferents on an excitatory reflex pathway to medial gastrocnemius motoneurons. J. Neurophysiol. 64, 403–412 (1990).

    Article  CAS  Google Scholar 

  28. Stephens, J.A., Reinking, R.M. & Stuart, D.G. Tendon organs of cat medial gastrocnemius: responses to active and passive forces as a function of muscle length. J. Neurophysiol. 38, 1217–1231 (1975).

    Article  CAS  Google Scholar 

  29. Cleland, C.L. & Rymer, W.Z. Neural mechanisms underlying the clasp-knife reflex in the cat. I. Characteristics of the reflex. J. Neurophysiol. 64, 1303–1318 (1990).

    Article  CAS  Google Scholar 

  30. Hammar, I. & Jankowska, E. Modulatory effects of α1-, α2-, and β-receptor agonists on feline spinal interneurons with monosynaptic input from group I muscle afferents. J. Neurosci. 23, 332–338 (2003).

    Article  CAS  Google Scholar 

  31. Matthews, P.B.C. Mammalian muscle receptors and their central actions. in Monographs of the Physiological Society, Vol. 23 (eds. Davson, H., Greenfield, A.D.M., Whittam, R. & Brindley, G.S.) 1–630 (Edward Arnold Ltd., London, 1972).

    Google Scholar 

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

    Article  CAS  Google Scholar 

  33. Machacek, D.W., Garraway, S.M., Shay, B.L. & Hochman, S. Serotonin 5-HT2 receptor activation induces a long-lasting amplification of spinal reflex actions in the rat. J. Physiol. (Lond.) 537, 201–207 (2001).

    Article  CAS  Google Scholar 

  34. Binder, M.D., Robinson, F.R. & Powers, R.K. Distribution of effective synaptic currents in cat triceps surae motoneurons. VI. Contralateral pyramidal tract. J. Neurophysiol. 80, 241–248 (1998).

    Article  CAS  Google Scholar 

  35. Powers, R.K., Robinson, F.R., Konodi, M.A. & Binder, M.D. Distribution of rubrospinal synaptic input to cat triceps surae motoneurons. J. Neurophysiol. 70, 1460–1468 (1993).

    Article  CAS  Google Scholar 

  36. Heckman, C.J. & Binder, M.D. Analysis of effective synaptic currents generated by homonymous Ia afferent fibers in motoneurons of the cat. J. Neurophysiol. 60, 1946–1966 (1988).

    Article  CAS  Google Scholar 

  37. Binder, M.D. & Stuart, D.G. Motor unit-muscle receptor interactions: design features of the neuromuscular control system. in Spinal and Supraspinal Mechanisms of Voluntary Motor Control and Locomotion Vol. 8 (ed. Desmedt, J.E.) 72–98 (Karger, Basel, 1981).

    Google Scholar 

  38. Shefchyk, S.J. & Jordan, L.M. Motoneuron input-resistance changes during fictive locomotion produced by stimulation of the mesencephalic locomotor region. J. Neurophysiol. 54, 1101–1108 (1985).

    Article  CAS  Google Scholar 

  39. Brownstone, R.M., Gossard, J.P. & Hultborn, H. Voltage-dependent excitation of motoneurones from spinal locomotor centres in the cat. Exp. Brain Res. 102, 34–44 (1994).

    Article  CAS  Google Scholar 

  40. Fedirchuk, B. & Dai, Y. Monoamines increase the excitability of spinal neurones in the neonatal rat by hyperpolarizing the threshold for action potential production. J. Physiol. (Lond.) 557, 355–361 (2004).

    Article  CAS  Google Scholar 

  41. Krawitz, S., Fedirchuk, B., Dai, Y., Jordan, L.M. & McCrea, D.A. State-dependent hyperpolarization of voltage threshold enhances motoneurone excitability during fictive locomotion in the cat. J. Physiol. (Lond.) 532, 271–281 (2001).

    Article  CAS  Google Scholar 

  42. Svirskis, G. & Hounsgaard, J. Transmitter regulation of plateau properties in turtle motoneurons. J. Neurophysiol. 79, 45–50 (1998).

    Article  CAS  Google Scholar 

  43. Baldissera, F., Hultborn, H. & Illert, M. Integration in spinal neuronal systems. in Handbook of Physiology. Section 1: The Nervous System. Vol. 2: Motor Control, part 1 (ed. Brooks, V.B.) 509–595 (American Physiological Society, Bethesda, 1981).

    Google Scholar 

  44. Curtis, D.R. & Lacey, G. Prolonged GABAB receptor-mediated synaptic inhibition in the cat spinal cord: an in vivo study. Exp. Brain Res. 121, 319–333 (1998).

    Article  CAS  Google Scholar 

  45. Bowery, N.G. et al. International Union of Pharmacology. XXXIII. Mammalian γ-aminobutyric acid B receptors: structure and function. Pharmacol. Rev. 54, 247–264 (2002).

    Article  CAS  Google Scholar 

  46. Crone, C., Hultborn, H., Jespersen, B. & Nielsen, J. Reciprocal Ia inhibition between ankle flexors and extensors in man. J. Physiol. (Lond.) 389, 163–185 (1987).

    Article  CAS  Google Scholar 

  47. Wargon, I. et al. The disynaptic group I inhibition between wrist flexor and extensor muscles revisited in humans. Exp. Brain Res. 168, 203–217 (2006).

    Article  CAS  Google Scholar 

  48. Nielsen, J., Crone, C., Sinkjaer, T., Toft, E. & Hultborn, H. Central control of reciprocal inhibition during fictive dorsiflexion in man. Exp. Brain Res. 104, 99–106 (1995).

    Article  CAS  Google Scholar 

  49. Chen, X.Y., Chen, L., Chen, Y. & Wolpaw, J.R. Operant conditioning of reciprocal inhibition in rat soleus muscle. J. Neurophysiol. 96, 2144–2150 (2006).

    Article  Google Scholar 

  50. Chen, Y. et al. The interaction of a new motor skill and an old one: H-reflex conditioning and locomotion in rats. J. Neurosci. 25, 6898–6906 (2005).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank J. Schuster for comments on the manuscript and assistance with data collection; H. Maas and J. Pitman for discussion and interpretation of the data and manuscript; A. Daub for writing the robot protocols; and R. Lee for feedback on experimental methods. This work was partially supported by the Foundation for Physical Therapy, Promotion of Doctoral Studies, Viva J. Erickson Scholarship (to A.S.H.), a US National Research Service Award, Pre-doctoral Fellowship (5F31NS048757-03 to A.S.H.) and a grant from the US National Institutes of Health (NINDS NS034282 to C.J.H.).

Author information

Authors and Affiliations

  1. Department of Physiology, 303 E. Chicago Avenue, Feinberg School of Medicine, Northwestern University, Chicago, 60611, Illinois, USA

    Allison S Hyngstrom, Michael D Johnson, Jack F Miller & C J Heckman

  2. Department of Physical Medicine and Rehabilitation, 303 E. Chicago Avenue, Feinberg School of Medicine, Northwestern University, Chicago, 60611, Illinois, USA

    C J Heckman

Authors
  1. Allison S Hyngstrom
    View author publications

    Search author on:PubMed Google Scholar

  2. Michael D Johnson
    View author publications

    Search author on:PubMed Google Scholar

  3. Jack F Miller
    View author publications

    Search author on:PubMed Google Scholar

  4. C J Heckman
    View author publications

    Search author on:PubMed Google Scholar

Contributions

A.S.H. and C.J.H. designed the experiments. A.S.H. collected and analyzed all data for experiments in Figures 2,3,4,5 and Supplementary Figure 1. M.D.J. and J.F.M. performed the surgical preparation and assisted with data collection for Figures 2,3,4,5 and Supplementary Figure. 1. Data interpretation and manuscript preparation were done by A.S.H. and C.J.H. with assistance from M.D.J. and J.F.M.

Corresponding author

Correspondence to C J Heckman.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

The dendritic PIC is suppressed by synaptic inhibition, but not by synaptic excitation. (PDF 46 kb)

Supplementary Methods (PDF 40 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hyngstrom, A., Johnson, M., Miller, J. et al. Intrinsic electrical properties of spinal motoneurons vary with joint angle. Nat Neurosci 10, 363–369 (2007). https://doi.org/10.1038/nn1852

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/nn1852

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing