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.

  • Letter
  • Published:

Early motor activity drives spindle bursts in the developing somatosensory cortex

Abstract

Sensorimotor coordination emerges early in development. The maturation period is characterized by the establishment of somatotopic cortical maps1,2, the emergence of long-range cortical connections3, heightened experience-dependent plasticity4,5,6,7 and spontaneous uncoordinated skeletal movement8,9. How these various processes cooperate to allow the somatosensory system to form a three-dimensional representation of the body is not known. In the visual system, interactions between spontaneous network patterns and afferent activity have been suggested to be vital for normal development10,11. Although several intrinsic cortical patterns of correlated neuronal activity have been described in developing somatosensory cortex in vitro12,13,14, the in vivo patterns in the critical developmental period and the influence of physiological sensory inputs on these patterns remain unknown. We report here that in the intact somatosensory cortex of the newborn rat in vivo, spatially confined spindle bursts represent the first and only organized network pattern. The localized spindles are selectively triggered in a somatotopic manner by spontaneous muscle twitches8,9, motor patterns analogous to human fetal movements15,16. We suggest that the interaction between movement-triggered sensory feedback signals and self-organized spindle oscillations shapes the formation of cortical connections required for sensorimotor coordination.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Movement-triggered spindle bursts in S1 of the newborn rat.
Figure 2: Synaptic correlates of S1 spindle bursts.
Figure 3: Cortical spindles are spatially confined.
Figure 4: Spindles can occur in the absence of sensory inputs.

Similar content being viewed by others

References

  1. Killackey, H. P., Rhoades, R. W. & Bennettclarke, C. A. The formation of a cortical somatotopic map. Trends Neurosci. 18, 402–407 (1995)

    Article  CAS  Google Scholar 

  2. Armstrong-James, M. A. Spontaneous and evoked single unit activity in 7-day rat cerebral cortex. J. Physiol. (Lond.) 208, 10P–11P (1970)

    CAS  Google Scholar 

  3. Lopez-Bendito, G. & Molnar, Z. Thalamocortical development: How are we going to get there? Nature Rev. Neurosci. 4, 276–289 (2003)

    Article  CAS  Google Scholar 

  4. Fox, K. A critical period for experience-dependent synaptic plasticity in rat barrel cortex. J. Neurosci. 12, 1826–1838 (1992)

    Article  CAS  Google Scholar 

  5. Fox, K. Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience 111, 799–814 (2002)

    Article  CAS  Google Scholar 

  6. Feldman, D. E., Nicoll, R. A. & Malenka, R. C. Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses. J. Neurobiol. 41, 92–101 (1999)

    Article  CAS  Google Scholar 

  7. Jain, N., Diener, P. S., Coq, J. O. & Kaas, J. H. Patterned activity via spinal dorsal quadrant inputs is necessary for the formation of organized somatosensory maps. J. Neurosci. 23, 10321–10330 (2003)

    Article  CAS  Google Scholar 

  8. Gramsbergen, A., Schwartze, P. & Prechtl, H. F. The postnatal development of behavioral states in the rat. Dev. Psychobiol. 3, 267–280 (1970)

    Article  CAS  Google Scholar 

  9. Petersson, P., Waldenstrom, A., Fahraeus, C. & Schouenborg, J. Spontaneous muscle twitches during sleep guide spinal self-organization. Nature 424, 72–75 (2003)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  11. Katz, L. C. & Crowley, J. C. Development of cortical circuits: lessons from ocular dominance columns. Nature Rev. Neurosci. 3, 34–42 (2002)

    Article  CAS  Google Scholar 

  12. Yuste, R., Peinado, A. & Katz, L. C. Neuronal domains in developing neocortex. Science 257, 665–669 (1992)

    Article  ADS  CAS  Google Scholar 

  13. Yuste, R., Nelson, D. A., Rubin, W. W. & Katz, L. C. Neuronal domains in developing neocortex: mechanisms of coactivation. Neuron 14, 7–17 (1995)

    Article  CAS  Google Scholar 

  14. Garaschuk, O., Linn, J., Eilers, J. & Konnerth, A. Large-scale oscillatory calcium waves in the immature cortex. Nature Neurosci. 3, 452–459 (2000)

    Article  CAS  Google Scholar 

  15. de Vries, J. I., Visser, G. H. & Prechtl, H. F. The emergence of fetal behaviour. I. Qualitative aspects. Early Hum. Dev. 7, 301–322 (1982)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  17. Steriade, M. Impact of network activities on neuronal properties in corticothalamic systems. J. Neurophysiol. 86, 1–39 (2001)

    Article  CAS  Google Scholar 

  18. Kidd, F. L. & Isaac, J. T. Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature 400, 569–573 (1999)

    Article  ADS  CAS  Google Scholar 

  19. Ben Ari, Y. Developing networks play a similar melody. Trends Neurosci. 24, 353–360 (2001)

    Article  CAS  Google Scholar 

  20. Ben-Ari, Y., Khazipov, R., Leinekugel, X., Caillard, O. & Gaiarsa, J. L. GABA-A, NMDA and AMPA receptors: a developmentally regulated ‘menage a trois’. Trends Neurosci. 20, 523–529 (1997)

    Article  CAS  Google Scholar 

  21. Steriade, M., McCormick, D. A. & Sejnowski, T. J. Thalamocortical oscillations in the sleeping and aroused brain. Science 262, 679–685 (1993)

    Article  ADS  CAS  Google Scholar 

  22. Destexhe, A. & Sejnowski, T. Thalamocortical Assemblies: How Ion Channels, Single Neurons and Large-Scale Networks Organize Sleep Oscillations (Oxford Univ. Press, New York, 2001)

    Google Scholar 

  23. Chatrian, G. E., Petersen, M. C. & Lazarte, J. A. The blocking of the rolandic wicket rhythm and some central changes related to movement. Electroencephalogr. Clin. Neurophysiol. 11(Suppl.), 497–510 (1959)

    Article  CAS  Google Scholar 

  24. O'Donovan, M. J. The origin of spontaneous activity in developing networks of the vertebrate nervous system. Curr. Opin. Neurobiol. 9, 94–104 (1999)

    Article  CAS  Google Scholar 

  25. Bureau, I., Shepherd, G. M. G. & Svoboda, K. Precise development of functional and anatomical columns in the neocortex. Neuron 42, 789–801 (2004)

    Article  CAS  Google Scholar 

  26. Dreyfus-Brisac, C. & Larroche, J. C. Discontinuous electroencephalograms in the premature newborn and at term. Electro-anatomo-clinical correlations [in French]. Rev. Electroencephalogr. Neurophysiol. Clin. 1, 95–99 (1971)

    Article  CAS  Google Scholar 

  27. Leinekugel, X. et al. Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296, 2049–2052 (2002)

    Article  ADS  CAS  Google Scholar 

  28. Margrie, T. W., Brecht, M. & Sakmann, B. In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflugers Arch. 444, 491–498 (2002)

    Article  CAS  Google Scholar 

  29. Karlsson, K. A. & Blumberg, M. S. Hippocampal theta in the newborn rat is revealed under conditions that promote REM sleep. J. Neurosci. 23, 1114–1118 (2003)

    Article  CAS  Google Scholar 

  30. Bragin, A. et al. Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 15, 47–60 (1995)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank T. Pankevych for helping with histological reconstruction, R. Cossart, D. Robbe, S. Montgomery and M. Zugaro for constructive comments. Supported by grants from the National Institutes of Health (G.B. and G.L.H.) and INSERM (R.K. and Y.B.-A.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to György Buzsáki.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Methods

This section provides detailed information about the methods used in experimental procedures in the paper. (PDF 47 kb)

Supplementary Figures S1–S6

This section contains Supplementary Figures S1–S6. Fig. S1 illustrates the persistence of spindle bursts under urethane anesthesia. Fig. S2 depicts the participation of thalamic VPL neurons in S1 spindle-bursts. Fig. S3 shows the slow spread of spindle activity across S1 cortex. Fig. S4 is a representation of body map in S1 cortex. Fig. S5 is a comparison of the latencies of movement-triggered sharp potentials and skin stimulation-evoked potentials. Fig. S6 is the properties of evoked S1 bursts under anesthesia. (PDF 1601 kb)

Supplementary Table

The Table contains quantitative data of the intracellular experiments, the parameters of spontaneous synaptic currents in neonatal rat S1 neurons. (PDF 27 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Khazipov, R., Sirota, A., Leinekugel, X. et al. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432, 758–761 (2004). https://doi.org/10.1038/nature03132

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03132

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