Skip to main content
SpringerLink
Log in

Bidirectional interaction of sleep and synaptic plasticity: A view from visual cortex

  • Review Article
  • Published:
Sleep and Biological Rhythms Aims and scope Submit manuscript

Abstract

Rapidly growing experimental evidence supports the notion that sleep plays an active role in modulating synaptic plasticity in the brain and for stabilizing various types of memory. In addition, new technologies support the view of “off-line” reprocessing of recent experience during sleep. Conversely, recent analysis of the thalamocortical circuit establishes the reciprocal observation that sleep itself is a plastic process affected by waking experience. This overview synthesizes these convergent perspectives across a variety of brain regions and species, emphasizing neuronal activity in the visual cortex. We discuss possible strategies for approaching the interaction between sleep and plasticity utilizing the developing visual pathway as a reduced model.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Miyamoto H, Hensch TK. Reciprocal interaction of sleep and synaptic plasticity. Mol. Interv. 2003; 3: 404–17.

    Article  PubMed  Google Scholar 

  2. Stickgold R. Human studies of sleep and off-line memory reprocessing. In: Maquet P, Smith C, Stickgold R, eds. Sleep and Brain Plasticity. Oxford University Press: New York, 2003; 42–63.

    Google Scholar 

  3. Karni A, Sagi D. Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. Proc. Natl. Acad. Sci. USA 1991; 88: 4966–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Schwartz S, Maquet P, Frith C. Neural correlates of perceptual learning: a functional MRI study of visual texture discrimination. Proc. Natl. Acad. Sci. USA 2002; 99: 17137–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Schoups A, Vogels R, Qian N et al. Practising orientation identification improves orientation coding in V1 neurons. Nature 2001; 412: 549–53.

    Article  CAS  PubMed  Google Scholar 

  6. Fenn KM, Nusbaum HC, Margoliash D. Consolidation during sleep of perceptual learning of spoken language. Nature 2003; 425: 614–16.

    Article  CAS  PubMed  Google Scholar 

  7. Walker MP, Brakefield T, Hobson JA et al. Dissociable stages of human memory consolidation and reconsolidation. Nature 2003; 9: 616–20.

    Article  Google Scholar 

  8. Wagner U, Gais S, Haider H et al. Sleep inspires insight. Nature 2004; 427: 352–5.

    Article  CAS  PubMed  Google Scholar 

  9. Buzsaki G. Large-scale recording of neuronal ensembles. Nat. Neurosci. 2004; 7: 446–51.

    Article  CAS  PubMed  Google Scholar 

  10. Wilson MA, McNaughton BL. Reactivation of hippocam-pal ensemble memories during sleep. Science 1994; 265: 676–9.

    Article  CAS  PubMed  Google Scholar 

  11. Kudrimoti HS, Barnes CA, McNaughton BL. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J. Neurosci. 1999; 19: 4090–101.

    CAS  PubMed  Google Scholar 

  12. Hoffman KL, McNaughton BL. Coordinated reactivation of distributed memory traces in primate neocortex. Science 2002; 297: 2070–3.

    Article  CAS  PubMed  Google Scholar 

  13. Louie K, Wilson MA. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 2001; 29: 145–56.

    Article  CAS  PubMed  Google Scholar 

  14. Ribeiro S, Gervasoni D, Soares ES et al. Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biol. 2004; 2: E24.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Brainard MS, Doupe AJ. What songbirds teach us about learning. Nature 2002; 417: 351–8.

    Article  CAS  PubMed  Google Scholar 

  16. Dave AS, Yu AC, Margoliash D. Behavioral state modulation of auditory activity in a vocal motor system. Science 1998; 282: 2250–4.

    Article  CAS  PubMed  Google Scholar 

  17. Dave AS, Margoliash D. Song replay during sleep and computational rules for sensorimotor vocal learning. Science 2000; 290: 812–16.

    Article  CAS  PubMed  Google Scholar 

  18. Deregnaucourt S, Mitra PP, Feher O et al. How sleep affects the developmental learning of bird song. Nature 2005; 433: 710–16.

    Article  CAS  PubMed  Google Scholar 

  19. Nick TA, Konishi M. Neural song preference during vocal learning in the zebra finch depends on age and state. J. Neurobiol. 2005; 62: 231–42.

    Article  PubMed  Google Scholar 

  20. Olveczky BP, Andalman AS, Fee MS. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol. 2005; 3: e153.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Datta S, Patterson EH. Activation of phasic pontine wave (P-wave): a mechanism of learning and memory processing. In: Maquet P, Smith C, Stickgold R, eds. Sleep and Brain Plasticity. Oxford University Press: New York, 2003; 135–56.

    Chapter  Google Scholar 

  22. Datta S, Mavanji V, Ulloor J et al. Activation of phasic pontine-wave generator prevents rapid eye movement sleep deprivation-induced learning impairment in the rat: a mechanism for sleep-dependent plasticity. J. Neurosci. 2004; 24: 1416–27.

    Article  CAS  PubMed  Google Scholar 

  23. Poe GR, Nitz DA, McNaughton BL et al. Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res. 2000; 855: 176–80.

    Article  CAS  PubMed  Google Scholar 

  24. McDermott CM, LaHoste GJ, Chen C et al. Sleep deprivation causes behavioral, synaptic, and membrane excitability alterations in hippocampal neurons. J. Neurosci. 2003; 23: 9687–95.

    CAS  PubMed  Google Scholar 

  25. Romcy-Pereira R, Pavlides C. Distinct modulatory effects of sleep on the maintenance of hippocampal and medial prefrontal cortex LTP. Eur. J. Neurosci. 2004; 20: 3453–62.

    Article  PubMed  Google Scholar 

  26. Cirelli C. A molecular window on sleep: changes in gene expression between sleep and wakefulness. Neuroscientist 2005; 11: 63–74.

    Article  CAS  PubMed  Google Scholar 

  27. Hensch TK. Controlling the critical period. Neurosci. Res. 2003; 47: 17–22.

    Article  PubMed  Google Scholar 

  28. Hensch TK. Critical period plasticity in local circuits. Nat. Rev. Neurosci. 2005; 6: 877–88.

    Article  CAS  PubMed  Google Scholar 

  29. Hensch TK, Fagiolini M. Excitatory-inhibitory balance and critical period plasticity in developing visual cortex. Prog. Brain Res. 2005; 147: 115–24.

    Article  CAS  PubMed  Google Scholar 

  30. Frank MG, Issa NP, Stryker MP. Sleep enhances plasticity in the developing visual cortex. Neuron 2001; 30: 275–87.

    Article  CAS  PubMed  Google Scholar 

  31. Jha SK, Jones BE, Coleman T et al. Sleep-dependent plasticity requires cortical activity. J. Neurosci. 2005; 25: 9266–74.

    Article  CAS  PubMed  Google Scholar 

  32. Shaffery JP, Sinton CM, Bissette G et al. Rapid eye movement sleep deprivation modifies expression of long-term potentiation in visual cortex of immature rats. Neuroscience 2002; 110: 431–43.

    Article  CAS  PubMed  Google Scholar 

  33. Oksenberg A, Shaffery JP, Marks GA et al. Rapid eye movement sleep deprivation in kittens amplifies LGN cell-size disparity induced by monocular deprivation. Brain Res. Dev. Brain Res. 1996; 97: 51–61.

    Article  CAS  PubMed  Google Scholar 

  34. Fagiolini M, Katagiri H, Miyamoto H et al. Separable features of visual cortical plasticity revealed by N-methyl-D-aspartate receptor 2A signaling. Proc. Natl. Acad. Sci. USA 2003; 4: 2854–9.

    Article  Google Scholar 

  35. Miyamoto H, Katagiri H, Hensch TK. Experience-dependent slow-wave sleep development. Nat. Neurosci. 2003; 6: 553–4.

    Article  CAS  PubMed  Google Scholar 

  36. Vyazovskiy V, Borbely AA, Tobler I. Unilateral vibrissae stimulation during waking induces interhemispheric EEG asymmetry during subsequent sleep in the rat. J. Sleep Res. 2000; 9: 367–71.

    Article  CAS  PubMed  Google Scholar 

  37. Iwasaki N, Karashima A, Tamakawa Y et al. Sleep EEG dynamics in rat barrel cortex associated with sensory deprivation. Neuroreport 2004; 3: 2681–4.

    Article  Google Scholar 

  38. Kattler H, Dijk DJ, Borbely AA. Effect of unilateral soma-tosensory stimulation prior to sleep on the sleep EEG in humans. J. Sleep Res. 1994; 3: 159–64.

    Article  PubMed  Google Scholar 

  39. Yasuda T, Yasuda K, Brown RA et al. State-dependent effects of light-dark cycle on somatosensory and visual cortex EEG in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005; 289: R1083–9.

    Article  CAS  PubMed  Google Scholar 

  40. Gais S, Molle M, Helms K, Born J. Learning-dependent increases in sleep spindle density. J. Neurosci. 2002; 22: 6830–4.

    CAS  PubMed  Google Scholar 

  41. Huber R, Ghilardi MF, Massimini M et al. Local sleep and learning. Nature 2004; 430: 78–81.

    Article  CAS  PubMed  Google Scholar 

  42. Bodizs R, Kis T, Lazar As et al. Prediction of general mental ability based on neural oscillation measures of sleep. J. Sleep Res. 2005; 14: 285–92.

    Article  PubMed  Google Scholar 

  43. Maret S, Franken P, Dauvilliers Y et al. Retinoic acid signaling affects cortical synchrony during sleep. Science 2005; 310: 111–13.

    Article  CAS  PubMed  Google Scholar 

  44. Steriade M, Timofeev I. Neuronal plasticity in thalamo-cortical networks during sleep and waking oscillations. Neuron 2003; 37: 563–76.

    Article  CAS  PubMed  Google Scholar 

  45. Penn AA, Riquelme PA, Feller MB et al. Competition in retinogeniculate patterning driven by spontaneous activity. Science 1998; 279: 2108–12.

    Article  CAS  PubMed  Google Scholar 

  46. Weliky M, Katz LC. Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo. Science 1999; 285: 599–604.

    Article  CAS  PubMed  Google Scholar 

  47. Chiu C, Weliky M. Relationship of correlated spontaneous activity to functional ocular dominance columns in the developing visual cortex. Neuron 2002; 35: 1123–34.

    Article  CAS  PubMed  Google Scholar 

  48. Massimini M, Huber R, Ferrarelli F et al. The sleep slow oscillation as a traveling wave. J. Neurosci. 2004; 24: 6862–70.

    Article  CAS  PubMed  Google Scholar 

  49. Fiser J, Chiu C, Weliky M. Small modulation of ongoing cortical dynamics by sensory input during natural vision. Nature 2004; 431: 573–8.

    Article  CAS  PubMed  Google Scholar 

  50. Kenet T, Bibitchkov D, Tsodyks M et al. Spontaneously emerging cortical representations of visual attributes. Nature 2003; 425: 954–6.

    Article  CAS  PubMed  Google Scholar 

  51. Sejnowski TJ, Destexhe A. Why do we sleep? Brain Res. 2000; 886: 208–23.

    Article  CAS  PubMed  Google Scholar 

  52. Zhou Q, Tao HW, Poo MM. Reversal and stabilization of synaptic modifications in a developing visual system. Science 2003; 20: 1953–7.

    Article  Google Scholar 

  53. Konishi M. The role of auditory feedback in birdsong. Ann. N. Y. Acad. Sci. 2004; 1016: 463–75.

    Article  PubMed  Google Scholar 

  54. Stickgold R, Walker MP. Memory consolidation and reconsolidation: what is the role of sleep? Trends Neurosci. 2005; 28: 408–15.

    Article  CAS  PubMed  Google Scholar 

  55. Fagiolini M, Hensch TK. Inhibitory threshold for critical-period activation in primary visual cortex. Nature 2000; 404: 183–6.

    Article  CAS  PubMed  Google Scholar 

  56. Iwai Y, Fagiolini M, Obata K et al. Rapid critical period induction by tonic inhibition in visual cortex. J. Neurosci. 2003; 23: 6695–702.

    CAS  PubMed  Google Scholar 

  57. Peigneux P, Laureys S, Fuchs S et al. Learned material content and acquisition level modulate cerebral reactivation during posttraining rapid-eye-movements sleep. Neuroimage 2003; 20: 125–34.

    Article  PubMed  Google Scholar 

  58. Martinez LM, Alonso JM. Construction of complex receptive fields in cat primary visual cortex. Neuron 2001; 32: 515–25.

    Article  CAS  PubMed  Google Scholar 

  59. Yoshimura Y, Dantzker JL, Callaway EM. Excitatory cortical neurons form fine-scale functional networks. Nature 2005; 433: 868–73.

    Article  CAS  PubMed  Google Scholar 

  60. Dragoi G, Harris KD, Buzsaki G. Place representation within hippocampal networks is modified by long-term potentiation. Neuron 2003; 39: 843–53.

    Article  CAS  PubMed  Google Scholar 

  61. Cheour M, Martynova O, Naatanen R et al. Speech sounds learned by sleeping newborns. Nature 2002; 415: 599–600.

    Article  CAS  PubMed  Google Scholar 

  62. Hennevin E. Expression and modulation of memory traces during paradoxical sleep. In: Maquet P, Smith C, Stickgold R, eds. Sleep and Brain Plasticity. Oxford University Press: New York, 2003; 101–16.

    Chapter  Google Scholar 

  63. Amedi A, Floel A, Knecht S et al. Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects. Nat. Neurosci. 2004; 7: 1266–70.

    Article  CAS  PubMed  Google Scholar 

  64. Merabet LB, Rizzo JF, Amedi A et al. What blindness can tell us about seeing again: merging neuroplasticity and neuroprostheses. Nat. Rev. Neurosci. 2005; 6: 71–7.

    Article  CAS  PubMed  Google Scholar 

  65. Angelucci A, Clasca F, Bricolo E et al. Experimentally induced retinal projections to the ferret auditory thalamus: development of clustered eye-specific patterns in a novel target. J. Neurosci. 1997; 17: 2040–55.

    CAS  PubMed  Google Scholar 

  66. Carlson M, Hubel DH, Wiesel TN. Effects of monocular exposure to oriented lines on monkey striate cortex. Brain Res. 1986; 390: 71–81.

    Article  CAS  PubMed  Google Scholar 

  67. Nakahara H, Zhang LI, Merzenich MM. Specialization of primary auditory cortex processing by sound exposure in the “critical period”. Proc. Natl. Acad. Sci. USA 2004; 101: 7170–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Salazar RF, Kayser C, Konig P. Effects of training on neuronal activity and interactions in primary and higher visual cortices in the alert cat. J. Neurosci. 2004; 24: 1627–36.

    Article  CAS  PubMed  Google Scholar 

  69. Amzica F, Neckelmann D, Steriade M. Instrumental conditioning of fast (20- to 50-Hz) oscillations in corticothalamic networks. Proc. Natl. Acad. Sci. USA 1997; 94: 1985–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Nicolelis MA. Brain-machine interfaces to restore motor function and probe neural circuits. Nat. Rev. Neurosci. 2003; 4: 417–22.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory for Neuronal Circuit Development, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama, 351-0198, Japan

    Hiroyuki Miyamoto &  Takao K. Hensch

Authors
  1. Hiroyuki Miyamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takao K. Hensch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takao K. Hensch.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miyamoto, H., Hensch, T.K. Bidirectional interaction of sleep and synaptic plasticity: A view from visual cortex. Sleep Biol. Rhythms 4, 35–43 (2006). https://doi.org/10.1111/j.1479-8425.2006.00204.x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1111/j.1479-8425.2006.00204.x

Key words

Search

Navigation