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.

Spontaneous muscle twitches during sleep guide spinal self-organization

Abstract

During development, information about the three-dimensional shape and mechanical properties of the body is laid down in the synaptic connectivity of sensorimotor systems through unknown adaptive mechanisms. In spinal reflex systems, this enables the fast transformation of complex sensory information into adequate correction of movements. Here we use a computer simulation to show that an unsupervised correlation-based learning mechanism, using spontaneous muscle twitches, can account for the functional adaptation of the withdrawal reflex system. We also show that tactile feedback resulting from spontaneous muscle twitches during sleep1,2,3 does indeed modify sensorimotor transformation in young rats in a predictable manner. The results indicate that these twitches, corresponding to human fetal movements4, are important in spinal self-organization.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Proposed organization of a reflex module.
Figure 2: Developmental adaptation of NWRs.
Figure 3: Simulated developmental adaptation of receptive fields for six muscles.
Figure 4: Behavioural experiments.

References

  1. Karlsson, K. A. & Blumberg, M. S. The union of the state: Myoclonic twitching is coupled with nuchal muscle atonia in infant rats. Behav. Neurosci. 116, 912–917 (2002)

    Article  Google Scholar 

  2. Blumberg, M. S. & Lucas, D. E. A developmental and component analysis of active sleep. Dev. Psychobiol. 29, 1–22 (1996)

    CAS  Article  Google Scholar 

  3. Blumberg, M. S. & Lucas, D. E. Dual mechanisms of twitching during sleep in neonatal rats. Behav. Neurosci. 108, 1196–1202 (1994)

    CAS  Article  Google Scholar 

  4. Clancy, B., Darlington, R. B. & Finlay, B. L. Translating developmental time across mammalian species. Neuroscience 105, 7–17 (2001)

    CAS  Article  Google Scholar 

  5. Pouget, A. & Snyder, L. H. Computational approaches to sensorimotor transformations. Nature Neurosci. 3 (Suppl.), 1192–1198 (2000)

    CAS  Article  Google Scholar 

  6. Schouenborg, J. & Weng, H. R. Sensorimotor transformation in a spinal motor system. Exp. Brain Res. 100, 170–174 (1994)

    CAS  Article  Google Scholar 

  7. Holmberg, H. & Schouenborg, J. Postnatal development of the nociceptive withdrawal reflexes in the rat: a behavioural and electromyographic study. J. Physiol. (Lond.) 493, 239–252 (1996)

    CAS  Article  Google Scholar 

  8. Waldenström, A., Thelin, J. & Schouenborg, J. Tactile sensory input is used for the postnatal tuning of the nociceptive withdrawal reflex system. Soc. Neurosci. Abstr. 30, 1623 (2001)

    Google Scholar 

  9. Holmberg, H. & Schouenborg, J. Developmental adaptation of withdrawal reflexes to early alteration of peripheral innervation in the rat. J. Physiol. (Lond.) 495, 399–409 (1996)

    Article  Google Scholar 

  10. Holmberg, H., Schouenborg, J., Yu, Y. B. & Weng, H. R. Developmental adaptation of rat nociceptive withdrawal reflexes after neonatal tendon transfer. J. Neurosci. 17, 2071–2078 (1997)

    CAS  Article  Google Scholar 

  11. Gardner, R. & Grossman, W. Normal motor patterns in sleep in man. Adv. Sleep Res. 2, 67–107 (1975)

    Google Scholar 

  12. Hadders-Algra, M., Nakae, Y., Van Eykern, L. A., Klip-Van den Nieuwendijk, A. W. & Prechtl, H. F. The effect of behavioural state on general movements in healthy full-term newborns. A polymyographic study. Early Hum. Dev. 35, 63–79 (1993)

    CAS  Article  Google Scholar 

  13. de Lisi, L. Su di un fenomeno motorio costante del sonno normale: Le mioclonie ipniche fisiologiche. Riv. Patol. Nerv. Ment. 29, 481–496 (1932)

    Google Scholar 

  14. Waldenström, A., Christensson, M. & Schouenborg, J. Spontaneous movements precede and overlap in time with the tuning of the nociceptive withdrawal reflex (NWR) in postnatal rats. IASP Abstr. 1558, P106 (2002)

    Google Scholar 

  15. Fitzgerald, M. & Koltzenburg, M. The functional development of descending inhibitory pathways in the dorsolateral funiculus of the newborn rat spinal cord. Brain Res. 389, 261–270 (1986)

    CAS  Article  Google Scholar 

  16. Levinsson, A., Luo, X. L., Holmberg, H. & Schouenborg, J. Developmental tuning in a spinal nociceptive system: effects of neonatal spinalization. J. Neurosci. 19, 10397–10403 (1999)

    CAS  Article  Google Scholar 

  17. Cervero, F. & Iggo, A. The substantia gelatinosa of the spinal cord: a critical review. Brain 103, 717–772 (1980)

    CAS  Article  Google Scholar 

  18. Rosenblatt, F. The perceptron: A probabilistic model for information storage and organization in the brain. Psychol. Rev. 65, 386–408 (1958)

    CAS  Article  Google Scholar 

  19. Oja, E. A simplified neuron model as a principal component analyzer. J. Math. Biol. 15, 267–273 (1982)

    MathSciNet  CAS  Article  Google Scholar 

  20. Turrigiano, G. G., Leslie, K. R., Desai, N. S., Rutherford, L. C. & Nelson, S. B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892–896 (1998)

    ADS  CAS  Article  Google Scholar 

  21. Nakatsuka, T., Ataka, T., Kumamoto, E., Tamaki, T. & Yoshimura, M. Alteration in synaptic inputs through C-afferent fibers to substantia gelatinosa neurons of the rat spinal dorsal horn during postnatal development. Neuroscience 99, 549–556 (2000)

    CAS  Article  Google Scholar 

  22. Linsker, R. From basic network principles to neural architecture: emergence of orientation columns. Proc. Natl Acad. Sci. USA 83, 8779–8783 (1986)

    ADS  CAS  Article  Google Scholar 

  23. Fregnac, Y. & Bienenstock, E. in Mechanistic Relationships between Development and Learning (eds Carew, T. J., Menzel, R. & Shatz, C. J.) 113–148 (Wiley, Berlin, 1998)

    Google Scholar 

  24. Katz, L. C. & Shatz, C. J. Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996)

    ADS  CAS  Article  Google Scholar 

  25. Nicolelis, M. A., De Oliveira, L. M., Lin, R. C. & Chapin, J. K. Active tactile exploration influences the functional maturation of the somatosensory system. J. Neurophysiol. 75, 2192–2196 (1996)

    CAS  Article  Google Scholar 

  26. Levinsson, A., Holmberg, H., Broman, J., Zhang, M. & Schouenborg, J. Spinal sensorimotor transformation: Relation between cutaneous somatotopy and a reflex network. J. Neurosci. 22, 8170–8182 (2002)

    CAS  Article  Google Scholar 

  27. Morisset, V. & Nagy, F. Nociceptive integration in the rat spinal cord: Role of non-linear membrane properties of deep dorsal horn neurons. Eur. J. Neurosci. 10, 3642–3652 (1998)

    CAS  Article  Google Scholar 

  28. Stickgold, R., Hobson, J. A., Fosse, R. & Fosse, M. Sleep, learning, and dreams: Off-line memory reprocessing. Science 294, 1052–1057 (2001)

    ADS  CAS  Article  Google Scholar 

  29. Frank, M. G., Issa, N. P. & Stryker, M. P. Sleep enhances plasticity in the developing visual cortex. Neuron 30, 275–287 (2001)

    CAS  Article  Google Scholar 

  30. Johansson, R. System Modeling and Identification (Prentice Hall, Englewood Cliffs, New Jersey, 1993)

    Google Scholar 

Download references

Acknowledgements

We thank P. Nockhammar for technical assistance and M. Garwicz for constructive comments on earlier versions of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Per Petersson.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Figure 1 (PDF 328 kb)

Supplementary Figure 2 (PDF 15 kb)

Supplementary Movie 1: Muscle Stimulation (MPG 4263 kb)

Supplementary Movie 2: Muscle Stimulation (MPG 4140 kb)

Supplementary Movie 3: Muscle Stimulation (MPG 8433 kb)

Supplementary Movie 4: Muscle Stimulation (MPG 5870 kb)

Supplementary Movie 5: Muscle Stimulation (MPG 10252 kb)

Supplementary Movie 6: Muscle Stimulation (MPG 3383 kb)

Supplementary Movie 7: Muscle Stimulation (MPG 6604 kb)

Supplementary Movie 8: Muscle Stimulation (MPG 6283 kb)

Supplementary Movie 9: Muscle Stimulation (MPG 9665 kb)

Supplementary Movie 10: Muscle Stimulation (MPG 9564 kb)

Supplementary Movie 11: Sleeping Behaviour - Litter from above (MPG 11445 kb)

Supplementary Movie 12: Sleeping Behaviour - Litter from below (MPG 9316 kb)

Supplementary Movie 12: Sleeping Behaviour - Twitch (MPG 6898 kb)

Supplementary Movie 13: Spontaneous Single Muscle Twitch - Continuous recording (MPG 15300 kb)

Supplementary Movie 14: Spontaneous Single Muscle Twitch - Extensor digitorum longus (MPG 3092 kb)

Supplementary Movie 15: Spontaneous Single Muscle Twitch - Gastrocemius (MPG 4534 kb)

Supplementary Movie 16: Spontaneous Single Muscle Twitch - Localized (MPG 2275 kb)

Supplementary Movie 17: Spontaneous Single Muscle Twitch - Peroneus longus (MPG 1792 kb)

Programme code: Functions used in simulation (DOC 19 kb)

Programme code: Functions used in simulation (DOC 19 kb)

Programme code: Functions used in simulation (XLS 28 kb)

Programme code: Functions used in simulation - Paw (BMP 0 kb)

Programme code: Functions used in simulation (DOC 19 kb)

Programme code: Simulation used in paper (DOC 43 kb)

Programme code: Movement EMG Matrices: EMG (XLS 59 kb)

Programme code: Movement EMG Matrices: EMG (XLS 60 kb)

Programme code: Movement EMG Matrices: EMG (XLS 46 kb)

Programme code: Movement EMG Matrices: EMG (XLS 60 kb)

Programme code: Movement EMG Matrices: EMG (XLS 60 kb)

Programme code: Movement EMG Matrices: EMG (XLS 60 kb)

Programme code: Movement EMG Matrices: Movement (XLS 60 kb)

Programme code: Movement EMG Matrices: Movement (XLS 60 kb)

Programme code: Movement EMG Matrices: Movement (XLS 47 kb)

Programme code: Movement EMG Matrices: Movement (XLS 60 kb)

Programme code: Movement EMG Matrices: Movement (XLS 60 kb)

Programme code: Movement EMG Matrices: Movement (XLS 60 kb)

Supplementary Information (DOC 26 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Petersson, P., Waldenström, A., Fåhraeus, C. et al. Spontaneous muscle twitches during sleep guide spinal self-organization. Nature 424, 72–75 (2003). https://doi.org/10.1038/nature01719

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01719

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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