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.

  • Opinion
  • Published:

Dual function of thalamic low-vigilance state oscillations: rhythm-regulation and plasticity

Nature Reviews Neuroscience volume 19, pages 107–118 (2018)Cite this article

Subjects

Abstract

During inattentive wakefulness and non-rapid eye movement (NREM) sleep, the neocortex and thalamus cooperatively engage in rhythmic activities that are exquisitely reflected in the electroencephalogram as distinctive rhythms spanning a range of frequencies from <1 Hz slow waves to 13 Hz alpha waves. In the thalamus, these diverse activities emerge through the interaction of cell-intrinsic mechanisms and local and long-range synaptic inputs. One crucial feature, however, unifies thalamic oscillations of different frequencies: repetitive burst firing driven by voltage-dependent Ca2+ spikes. Recent evidence reveals that thalamic Ca2+ spikes are inextricably linked to global somatodendritic Ca2+ transients and are essential for several forms of thalamic plasticity. Thus, we propose herein that alongside their rhythm-regulation function, thalamic oscillations of low-vigilance states have a plasticity function that, through modifications of synaptic strength and cellular excitability in local neuronal assemblies, can shape ongoing oscillations during inattention and NREM sleep and may potentially reconfigure thalamic networks for faithful information processing during attentive wakefulness.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Cellular thalamic counterparts of electroencephalogram rhythms of relaxed wakefulness and non-rapid eye movement sleep.
Figure 2: Contribution of T-type Ca2+ channels to low-vigilance state oscillations.
Figure 3: Low-threshold spikes and action potentials in thalamic neurons.
Figure 4: Ca2+ signalling in thalamic neurons during non-rapid eye movement sleep oscillations.
Figure 5: Low-threshold Ca2+ spike-dependent plasticity in the thalamus.

Similar content being viewed by others

References

  1. Niedermeyer, E. & Lopes Da Silva, F. Electroencephalography: Basic Principles, Clinical Applications, and Related Fields (Lippincott Williams Wilkins, 2004).

    Google Scholar 

  2. Herrera, C. G. et al. Hypothalamic feedforward inhibition of thalamocortical network controls arousal and consciousness. Nat. Neurosci. 19, 290–229 (2016).

    Article  CAS  PubMed  Google Scholar 

  3. Lorincz, M. L. & Adamantidis, A. R. Monoaminergic control of brain states and sensory processing: existing knowledge and recent insights obtained with optogenetics. Prog. Neurobiol. 151, 237–253 (2017).

    Article  CAS  PubMed  Google Scholar 

  4. Leresche, N., Lightowler, S., Soltesz, I., Jassik-Gerschenfeld, D. & Crunelli, V. Low-frequency oscillatory activities intrinsic to rat and cat thalamocortical cells. J. Physiol. 441, 155–174 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Steriade, M., Nunez, A. & Amzica, F. A novel slow (&lt;1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 13, 3252–3265 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Steriade, M., Contreras, D., Curró Dossi, R. & Nuñez, A. The slow (&lt;1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J. Neurosci. 13, 3284–3299 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bal, T., von Krosigk, M. & McCormick, D. A. Synaptic and membrane mechanisms underlying synchronized oscillations in the ferret lateral geniculate nucleus in vitro. J. Physiol. 483, 641–663 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Bal, T., von Krosigk, M. & McCormick, D. A. Role of the ferret perigeniculate nucleus in the generation of synchronized oscillations in vitro. J. Physiol. 483, 665–685 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Hughes, S. W., Cope, D. W., Blethyn, K. L. & Crunelli, V. Cellular mechanisms of the slow (&lt;1 Hz) oscillation in thalamocortical neurons in vitro. Neuron 33, 947–958 (2002).

    Article  CAS  PubMed  Google Scholar 

  10. Hughes, S. W. et al. Synchronized oscillations at alpha and theta frequencies in the lateral geniculate nucleus. Neuron 42, 253–268 (2004).

    Article  CAS  PubMed  Google Scholar 

  11. Crunelli, V., Cope, D. W. & Hughes, S. W. Thalamic T-type Ca2+ channels and NREM sleep. Cell Calcium 40, 175–190 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Llinás, R. & Jahnsen, H. Electrophysiology of mammalian thalamic neurones in vitro. Nature 297, 406–408 (1982).

    Article  PubMed  Google Scholar 

  13. Deschênes, M., Paradis, M., Roy, J. P. & Steriade, M. Electrophysiology of neurons of lateral thalamic nuclei in cat: resting properties and burst discharges. J. Neurophysiol. 51, 1196–1219 (1984).

    Article  PubMed  Google Scholar 

  14. Attwell, D. & Gibb, A. Neuroenergetics and the kinetic design of excitatory synapses. Nat. Rev. Neurosci. 6, 841–849 (2005).

    Article  CAS  PubMed  Google Scholar 

  15. Berger, H. Uber das elektroenkephalogramm des menschen [German]. Arch. Psych. 87, 527–570 (1929).

    Article  Google Scholar 

  16. Hughes, S. W. & Crunelli, V. Thalamic mechanisms of EEG alpha rhythms and their pathological implications. Neuroscientist 11, 357–372 (2005).

    Article  PubMed  Google Scholar 

  17. Crunelli, V., Tóth, T. I., Cope, D. W., Blethyn, K. & Hughes, S. W. The 'window' T-type calcium current in brain dynamics of different behavioural states. J. Physiol. 562, 121–129 (2005).

    Article  CAS  PubMed  Google Scholar 

  18. Lüthi, A. Sleep spindles: where they come from, what they do. Neuroscientist 20, 243–256 (2014).

    Article  PubMed  Google Scholar 

  19. Neske, G. T. The slow oscillation in cortical and thalamic networks: mechanisms and functions. Front. Neural Circ. 9, 88 (2016).

    Google Scholar 

  20. McCormick, D. A. & Bal, T. Sleep and arousal: thalamocortical mechanisms. Ann. Rev. Neurosci. 20, 185–215 (1997).

    Article  CAS  PubMed  Google Scholar 

  21. Carracedo, L. M. et al. A neocortical delta rhythm facilitates reciprocal interlaminar interactions via nested theta rhythms. J. Neurosci. 33, 10750–10761 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lorincz, M. L. et al. A distinct class of slow (∼0.2-2 Hz) intrinsically bursting layer 5 pyramidal neurons determines UP/DOWN state dynamics in the neocortex. J. Neurosci. 35, 5442–5458 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Dossi, R. C., Nuñez, A. & Steriade, M. Electrophysiology of a slow (0.5-4 Hz) intrinsic oscillation of cat thalamocortical neurones in vivo. J. Physiol. 447, 215–234 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Timofeev, I. & Steriade, M. Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. J. Neurophysiol. 76, 4152–4168 (1996).

    Article  CAS  PubMed  Google Scholar 

  25. McCormick, D. A. & Pape, H. C. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J. Physiol. 431, 291–318 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Bal, T. & McCormick, D. A. Mechanisms of oscillatory activity in guinea-pig nucleus reticularis thalami in vitro: a mammalian pacemaker. J. Physiol. 468, 669–691 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Iber, C., Ancoli-Israel, S., Chesson, A. & S., Q. The new sleep scoring manual — the evidence behind the rules. J. Clin. Sleep Med. 3, 107 (2007).

    Article  Google Scholar 

  28. Steriade, M., Nunez, A. & Amzica, F. Intracellular analysis neocortical oscillation electroencephalogram of relations between the slow (&lt;1 Hz) and other sleep rhythms. J. Neurosci. 13, 3266–3283 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Amzica, F. & Steriade, M. Short- and long-range neuronal synchronization of the slow (&lt;1 Hz) cortical oscillation. J. Neurophysiol. 73, 20–38 (1995).

    Article  CAS  PubMed  Google Scholar 

  30. Lemieux, M., Chen, J.-Y., Lonjers, P., Bazhenov, M. & Timofeev, I. The impact of cortical deafferentation on the neocortical slow oscillation. J. Neurosci. 34, 5689–5703 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Crunelli, V., Lorincz, M. L., Errington, A. C. & Hughes, S. W. Activity of cortical and thalamic neurons during the slow (&lt;1 Hz) rhythm in the mouse in vivo. Pflug. Arch. Eur. J. Physiol. 463, 73–88 (2012).

    Article  CAS  Google Scholar 

  32. Sanchez-Vives, M. V. & McCormick, D. A. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027–1034 (2000).

    Article  CAS  PubMed  Google Scholar 

  33. Zhu, L. et al. Nucleus- and species-specific properties of the slow (&lt;1 Hz) sleep oscillation in thalamocortical neurons. Neuroscience 141, 621–636 (2006).

    Article  CAS  PubMed  Google Scholar 

  34. Blethyn, K. L., Hughes, S. W., Tóth, T. I., Cope, D. W. & Crunelli, V. Neuronal basis of the slow (&lt;1 Hz) oscillation in neurons of the nucleus reticularis thalami in vitro. J. Neurosci. 26, 2474–2486 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Cunningham, M. O. et al. Neuronal metabolism governs cortical network response state. Proc. Natl Acad. Sci. USA 103, 5597–5601 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Crunelli, V. & Hughes, S. W. The slow (&lt;1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators. Nat. Neurosci. 13, 9–17 (2010).

    Article  CAS  PubMed  Google Scholar 

  37. David, F. et al. Essential thalamic contribution to slow waves of natural sleep. J. Neurosci. 33, 19599–19610 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Le Bon-Jego, M. & Yuste, R. Persistently active, pacemaker-like neurons in neocortex. Front. Neurosci. 1, 123–129 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Dreyfus, F. M. et al. Selective T-type calcium channel block in thalamic neurons reveals channel redundancy and physiological impact of ITwindow . J. Neurosci. 30, 99–109 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Klinzing, J. G. et al. Spindle activity phase-locked to sleep slow oscillations. NeuroImage 134, 607–616 (2016).

    Article  PubMed  Google Scholar 

  41. Latchoumane, C. V., Ngo, H. V., Born, J., S. H. Thalamic spindles promote memory formation during sleep through triple phase-locking of cortical, thalamic, and hippocampal rhythms. Neuron 95, 424–435 (2017).

    Article  CAS  PubMed  Google Scholar 

  42. Morison, R. & Bassett, D. Electrical activity of the thalamus and basal ganglia in decorticate cats. J. Neurophysiol. 8, 309–314 (1945).

    Article  Google Scholar 

  43. Steriade, M., Deschênes, M., Domich, L. & Mulle, C. Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. J. Neurophysiol. 54, 1473–1497 (1985).

    Article  CAS  PubMed  Google Scholar 

  44. Steriade, M., Domich, L., Oakson, G. & Deschenes, M. The deafferented reticular thalamic nucleus generates spindle rhythmicity. J. Neurophysiol. 57, 260–273 (1987).

    Article  CAS  PubMed  Google Scholar 

  45. Contreras, D. & Steriade, M. Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm. J. Physiol. 490, 159–179 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Fuentealba, P. & Steriade, M. The reticular nucleus revisited: intrinsic and network properties of a thalamic pacemaker. Progr. Neurobiol. 75, 125–141 (2005).

    Article  CAS  Google Scholar 

  47. Destexhe, A., Contreras, D. & Steriade, M. Cortically-induced coherence of a thalamic-generated oscillation. Neuroscience 92, 427–443 (1999).

    Article  CAS  PubMed  Google Scholar 

  48. Contreras, D., Destexhe, A., Sejnowski, T. J. & Steriade, M. Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science 274, 771–774 (1996).

    Article  CAS  PubMed  Google Scholar 

  49. Bollimunta, A., Mo, J., Schroeder, C. E. & Ding, M. Neuronal mechanisms and attentional modulation of corticothalamic alpha oscillations. J. Neurosci. 31, 4935–4943 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Jensen, O., Bonnefond, M., Marshall, T. R. & Tiesinga, P. Oscillatory mechanisms of feedforward and feedback visual processing. Trends Neurosci. 38, 192–194 (2015).

    Article  CAS  PubMed  Google Scholar 

  51. Schomburg, E. W. et al. Theta phase segregation of input-specific gamma patterns in entorhinal-hippocampal networks. Neuron 84, 470–485 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Hughes, S. W. et al. Thalamic gap junctions control local neuronal synchrony and influence macroscopic oscillation amplitude during EEG alpha rhythms. Front. Psychol. 2, 193 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Lorincz, M. L., Kékesi, K. A., Juhász, G., Crunelli, V. & Hughes, S. W. Temporal framing of thalamic relay-mode firing by phasic inhibition during the alpha rhythm. Neuron 63, 683–696 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. MacFarlane, J. G., Shahal, B., Mously, C. & Moldofsky, H. Periodic K-alpha sleep EEG activity and periodic limb movements during sleep: comparisons of clinical features and sleep parameters. Sleep 19, 200–204 (1996).

    Article  CAS  PubMed  Google Scholar 

  55. Silva, L. R., Amitai, Y. & Connorst, B. W. Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science 251, 433–435 (1991).

    Article  Google Scholar 

  56. Flint, A. C. & Connors, B. W. Two types of network oscillations in neocortex mediated by distinct glutamate receptor subtypes and neuronal populations. J. Neurophysiol. 75, 951–957 (1996).

    Article  CAS  PubMed  Google Scholar 

  57. Lopes Da Silva, F. H. & Storm Van Leeuwen, W. The cortical source of the alpha rhythm. Neurosci. Lett. 6, 237–241 (1977).

    Article  CAS  PubMed  Google Scholar 

  58. Lopes da Silva, F. H., Vos, J. E., Mooibroek, J. & Van Rotterdam, A. Relative contributions of intracortical and thalamo-cortical processes in the generation of alpha rhythms, revealed by partial coherence analysis. Electroench. Clin. Neurophysiol. 50, 449–456 (1980).

    Article  CAS  Google Scholar 

  59. Buzsáki, G. Rhythms of the Brain (Oxford Univ. Press, 2006).

    Book  Google Scholar 

  60. Llinás, R. & Yarom, Y. Properties and distribution of ionic conductances generating electroresponsiveness of mammalian inferior olivary neurones in vitro. J. Physiol. 315, 569–584 (1981).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Stuart, G., Schiller, J. & Sakmann, B. Action potential initiation and propagation in rat neocortical pyramidal neurons. J. Physiol. 505, 617–632 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Crandall, S. R., Govindaiah, G. & Cox, C. L. Low-threshold Ca2+ current amplifies distal dendritic signaling in thalamic reticular neurons. J. Neurosci. 30, 15419–15429 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Destexhe, A., Neubig, M., Ulrich, D. & Huguenard, J. Dendritic low-threshold calcium currents in thalamic relay cells. J. Neurosci. 18, 3574–3588 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Errington, A. C., Renger, J. J., Uebele, V. N. & Crunelli, V. State-dependent firing determines intrinsic dendritic Ca2+ signaling in thalamocortical neurons. J. Neurosci. 30, 14843–14853 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Kovács, K., Sik, A., Ricketts, C. & Timofeev, I. Subcellular distribution of low-voltage activated T-type Ca2+ channel subunits (Cav3.1 and Cav3.3) in reticular thalamic neurons of the cat. J. Neurosci. Res. 88, 448–460 (2010).

    Article  PubMed  CAS  Google Scholar 

  66. Williams, S. R. & Stuart, G. J. Action potential backpropagation and somato-dendritic distribution of ion channels in thalamocortical neurons. J. Neurosci. 20, 1307–1317 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Zomorrodi, R., Kröger, H. & Timofeev, I. Modeling thalamocortical cell: impact of Ca2+ channel distribution and cell geometry on firing pattern. Front. Comp. Neurosci. 2, 5 (2008).

    Google Scholar 

  68. Connelly, W. M., Crunelli, V. & Errington, A. C. The global spike: conserved dendritic properties enable unique Ca2+ spike generation in low-threshold spiking neurons. J. Neurosci. 35, 15505–15522 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Major, G., Larkum, M. E. & Schiller, J. Active properties of neocortical pyramidal neuron dendrites. Ann. Rev. Neurosci. 36, 1–24 (2013).

    Article  CAS  PubMed  Google Scholar 

  70. Stuart, G., Spruston, N. & Häusser, M. Dendrites (Oxford Univ. Press, 2016).

    Book  Google Scholar 

  71. Sieber, A. R., Min, R. & Nevian, T. Non-Hebbian long-term potentiation of inhibitory synapses in the thalamus. J. Neurosci. 33, 15675–15685 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Zaman, T. et al. CaV2.3 channels are critical for oscillatory burst discharges in the reticular thalamus and absence epilepsy. Neuron 70, 95–108 (2011).

    Article  CAS  PubMed  Google Scholar 

  73. Connelly, W. M., Crunelli, V. & Errington, A. C. Variable action potential backpropagation during tonic firing and low-threshold spike bursts in thalamocortical but not thalamic reticular nucleus neurons. J. Neurosci. 37, 5319–5333 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Errington, A. C., Hughes, S. W. & Crunelli, V. Rhythmic dendritic Ca2+ oscillations in thalamocortical neurons during slow non-REM sleep-related activity in vitro. J. Physiol. 590, 3691–3700 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Cueni, L. et al. T-type Ca2+ channels, SK2 channels and SERCAs gate sleep-related oscillations in thalamic dendrites. Nat. Neurosci. 11, 683–692 (2008).

    Article  CAS  PubMed  Google Scholar 

  76. Chausson, P., Leresche, N. & Lambert, R. C. Dynamics of intrinsic dendritic calcium signaling during tonic firing of thalamic reticular neurons. PLoS ONE 8, e72275 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Perez-Reyes, E. Molecular physiology of low-voltage-activated T-type calcium channels. Physiol. Rev. 83, 117–161 (2003).

    Article  CAS  PubMed  Google Scholar 

  78. Astori, S. et al. The CaV3.3 calcium channel is the major sleep spindle pacemaker in thalamus. Proc. Natl Acad. Sci. USA 108, 13823–13828 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Swadlow, H. A. & Gusev, A. G. The impact of 'bursting' thalamic impulses at a neocortical synapse. Nat. Neurosci. 4, 402–408 (2001).

    Article  CAS  PubMed  Google Scholar 

  80. Reinagel, P., Godwin, D., Sherman, S. M. & Koch, C. Encoding of visual information by LGN bursts. J. Neurophysiol. 81, 2558–2569 (1999).

    Article  CAS  PubMed  Google Scholar 

  81. Sherman, S. M. & Guillery, R. W. Functional organization of thalamocortical relays. J. Neurophysiol. 76, 1367–1395 (1996).

    Article  CAS  PubMed  Google Scholar 

  82. Balduzzi, D. & Tononi, G. What can neurons do for their brain? Communicate selectivity with bursts. Theory Biosci. 132, 27–39 (2013).

    Article  PubMed  Google Scholar 

  83. Kepecs, A. & Lisman, J. Information encoding and computation with spikes and bursts. Network 14, 103–118 (2003).

    Article  PubMed  Google Scholar 

  84. Beierlein, M., Fall, C. P., Rinzel, J. & Yuste, R. Thalamocortical bursts trigger recurrent activity in neocortical networks: layer 4 as a frequency-dependent gate. J. Neurosci. 22, 9885–9894 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Rosanova, M. & Ulrich, D. Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train. J. Neurosci. 25, 9398–9405 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Hu, H. & Agmon, A. Differential excitation of distally versus proximally targeting cortical interneurons by unitary thalamocortical bursts. J. Neurosci. 36, 6906–6916 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Izhikevich, E. M., Desai, N. S., Walcott, E. C. & Hoppensteadt, F. C. Bursts as a unit of neural information: selective communication via resonance. Trends Neurosci. 26, 161–167 (2003).

    Article  CAS  PubMed  Google Scholar 

  88. Guido, W. & Weyand, T. Burst responses in thalamic relay cells of the awake behaving cat. J. Neurophysiol. 74, 1782–1786 (1995).

    Article  CAS  PubMed  Google Scholar 

  89. Ortuño, T., Grieve, K. L., Cao, R., Cudeiro, J. & Rivadulla, C. Bursting thalamic responses in awake monkey contribute to visual detection and are modulated by corticofugal feedback. Front. Behav. Neurosci. 8, 198 (2014).

    PubMed  PubMed Central  Google Scholar 

  90. Luscher, C. & Malenka, R. C. NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harb Perspect Biol. 4, a005710 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Kato, H. K., Watabe, A. M. & Manabe, T. Non-Hebbian synaptic plasticity induced by repetitive postsynaptic action potentials. J. Neurosci. 29, 11153–11160 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Jones, E. G. The Thalamus (Springer, 1985).

    Book  Google Scholar 

  93. Pigeat, R., Chausson, P., Dreyfus, F. M., Leresche, N. & Lambert, R. C. Sleep slow wave-related homo and heterosynaptic LTD of intrathalamic GABAAergic synapses: involvement of T-type Ca2+ channels and metabotropic glutamate receptors. J. Neurosci. 35, 64–73 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Astori, S. & Lüthi, A. Synaptic plasticity at intrathalamic connections via CaV3.3 T-type Ca2+ channels and GluN2B-containing NMDA receptors. J. Neurosci. 33, 624–630 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Hsu, C. L., Yang, H. W., Yen, C. T. & Min, M. Y. A requirement of low-threshold calcium spike for induction of spike-timing-dependent plasticity at corticothalamic synapses on relay neurons in the ventrobasal nucleus of rat thalamus. Chin. J. Physiol. 55, 380–389 (2012).

    Article  CAS  PubMed  Google Scholar 

  96. Hsu, C.-L., Yang, H.-W., Yen, C.-T. & Min, M.-Y. Comparison of synaptic transmission and plasticity between sensory and cortical synapses on relay neurons in the ventrobasal nucleus of the rat thalamus. J. Physiol. 588, 4347–4363 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Haas, J. S., Zavala, B. & Landisman, C. E. Activity-dependent long-term depression of electrical synapses. Science 334, 389–393 (2011).

    Article  CAS  PubMed  Google Scholar 

  98. Sevetson, J., Fittro, S., Heckman, E. & Haas, J. S. A calcium-dependent pathway underlies activity-dependent plasticity of electrical synapses in the thalamic reticular nucleus. J. Physiol. 595, 4417–4430 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Lee, S., Patrick, S. L., Richardson, K. A. & Connors, B. W. Two functionally distinct networks of gap junction-coupled inhibitory neurons in the thalamic reticular nucleus. J. Neurosci. 34, 13170–13182 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Lüthi, A. & McCormick, D. A. H-Current: properties of a neuronal and network pacemaker. Neuron 21, 9–12 (1998).

    Article  PubMed  Google Scholar 

  101. Lüthi, A. & McCormick, D. A. Modulation of a pacemaker current through Ca2+-induced stimulation of cAMP production. Nat. Neurosci. 2, 634–641 (1999).

    Article  PubMed  Google Scholar 

  102. Tononi, G. & Cirelli, C. Sleep and synaptic homeostasis: a hypothesis. Brain Res. Bull. 62, 143–150 (2003).

    Article  PubMed  Google Scholar 

  103. Diekelmann, S. & Born, J. The memory function of sleep. Nat. Rev. Neurosci. 11, 114–126 (2010).

    Article  CAS  PubMed  Google Scholar 

  104. Watson, B. O., Levenstein, D., Greene, J. P., Gelinas, J. N. & Buzsáki, G. Network homeostasis and state dynamics of neocortical sleep. Neuron 90, 839–852 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Liu, Z.-W., Faraguna, U., Cirelli, C., Tononi, G. & Gao, X.-B. Direct evidence for wake-related increases and sleep-related decreases in synaptic strength in rodent cortex. J. Neurosci. 30, 8671–8675 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Aton, S. J. et al. Mechanisms of sleep-dependent consolidation of cortical plasticity. Neuron 61, 454–466 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Tononi, G. & Cirelli, C. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81, 12–34 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Durkin, J. et al. Cortically coordinated NREM thalamocortical oscillations play an essential, instructive role in visual system plasticity. Proc. Natl Acad. Sci. USA 114, 10485–10490 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Acsady, L. The thalamic paradox. Nat. Neurosci. 20, 901–902 (2017).

    Article  CAS  PubMed  Google Scholar 

  110. Halassa, M. M. & Acsády, L. Thalamic inhibition: diverse sources, diverse scales. Trends Neurosci. 39, 680–693 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Halassa, M. M. et al. State-dependent architecture of thalamic reticular subnetworks. Cell 158, 808–821 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Clemente-Perez, A. et al. Distinct thalamic reticular cell types differentially modulate normal and pathological cortical rhythms. Cell Rep. 19, 2130–2142 (2017).

    Article  CAS  PubMed  Google Scholar 

  113. Wells, M. F., Wimmer, R. D., Schmitt, L. I., Feng, G. & Halassa, M. M. Thalamic reticular impairment underlies attention deficit in Ptchd1Y/- mice. Nature 532, 58–63 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Guehl, D. et al. Tremor-related activity of neurons in the 'motor' thalamus: changes in firing rate and pattern in the MPTP vervet model of parkinsonism. Eur. J. Neurosci. 17, 2388–2400 (2003).

    Article  CAS  PubMed  Google Scholar 

  115. Magnin, M., Morel, A. & Jeanmonod, D. Single-unit analysis of the pallidum, thalamus and subthalamic nucleus in parkinsonian patients. Neuroscience 96, 549–564 (2000).

    Article  CAS  PubMed  Google Scholar 

  116. von Krosigk, M., Bal, T. & McCormick, D. A. Cellular mechanisms of a synchronized oscillation in the thalamus. Science 261, 361–364 (1993).

    Article  CAS  PubMed  Google Scholar 

  117. Amzica, F. & Steriade, M. Cellular substrates and laminar profile of sleep K-complex. Neuroscience 82, 671–686 (1998).

    Article  CAS  PubMed  Google Scholar 

  118. Contreras, D. & Steriade, M. Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J. Neurosci. 15, 604–622 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank C. McCafferty, R. Bódizs and P. Halász for critical comments. The authors' work is supported by the Wellcome Trust (grant 91882 to V.C.), the European Union (grant ITN-2016/722053 to V.C.), the Hungarian Scientific Research Fund (grants NF105083, NN125601 and FK123831 to M.L.L.), the Hungarian Brain Research Program (grant KTIA_NAP_13-2-2014-0014 to M.L.L.), the Centre national de la recherche scientifique (CNRS) (grant LIA528 to V.C., N.L. and R.C.L.) and the Agence Nationale de la Recherche (grants ANR-06-Neuro-050-01 and ANR-09-MNPS-035-01 to N.L. and R.C.L.). A.C.E. is a Jane Hodge Foundation Senior Research Fellow.

Author information

Author notes

  1. Vincenzo Crunelli, Magor L. Lőrincz and William M. Connelly: V.C., M.L.L. and W.M.C. contributed equally to this work.

Authors and Affiliations

  1. Department of Physiology and Biochemistry, Malta; and the Neuroscience Division, University of Malta, Msida, School of Bioscience, Cardiff University,

    Vincenzo Crunelli

  2. and the Neuroscience Division, School of Bioscience, Cardiff University, Cardiff, UK

    Vincenzo Crunelli

  3. Department of Physiology, Research Group for Cellular and Network Neurophysiology of the Hungarian Academy of Sciences, Anatomy and Neuroscience, University of Szeged, Szeged, Hungary

    Magor L. Lőrincz

  4. Eccles Institute of Neuroscience, John Curtin School of Medical Research, Australian National University, Canberra, Australia

    William M. Connelly

  5. Lyon Neuroscience Research Center, Centre national de la recherche scientifique (CNRS) unité mixte de recherche (UMR) 5292- INSERM U1028-Université Claude Bernard, Lyon, France

    François David

  6. Vertex Pharmaceuticals, Oxford, UK

    Stuart W. Hughes

  7. Sorbonne Universités, University Pierre and Marie Curie (UPMC) Univ. Paris 06, INSERM, Centre national de la recherche scientifique (CNRS), Neurosciences Paris Seine — Institut de Biologie Paris Seine (NPS - IBPS), Paris, France

    Régis C. Lambert & Nathalie Leresche

  8. Neuroscience and Mental Health Research Institute, School of Medicine, Cardiff University, Cardiff, UK

    Adam C. Errington

Authors
  1. Vincenzo Crunelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Magor L. Lőrincz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. William M. Connelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. François David
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stuart W. Hughes
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Régis C. Lambert
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nathalie Leresche
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Adam C. Errington
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

V.C.: substantial contribution to discussion of content, writing, review, and editing of manuscript before and after submission; A.C.E.: substantial contribution to discussion of content, writing, review and editing of manuscript before submission; M.L.L.: researching data for article, substantial contribution to discussion of content, review and editing of manuscript before submission; W.M.C.: substantial contribution to discussion of content, review and editing of manuscript before submission; F.D.: substantial contribution to discussion of content, review and editing of manuscript before submission; S.W.H.: substantial contribution to discussion of content, review and editing of manuscript before submission; R.C.L.: substantial contribution to discussion of content, review and editing of manuscript before submission; N.L.: substantial contribution to discussion of content, review and editing of manuscript before submission.

Corresponding authors

Correspondence to Vincenzo Crunelli or Adam C. Errington.

Ethics declarations

Competing interests

S.W.H. is an employee of and holder of stocks in Vertex Pharmaceuticals. All other authors declare no competing financial interests.

PowerPoint slides

Glossary

Thalamocortical neurons

Glutamatergic thalamic neurons that project to the neocortex.

Nucleus reticularis thalami neurons

GABAergic neurons of the thin, laterally located thalamic nucleus that do not project to the neocortex.

Sleep spindles

Oscillatory brain activity that constitutes an electroencephalogram (EEG) hallmark of non-rapid eye movement (NREM) sleep and consists of waxing-and-waning 7–14 Hz oscillations lasting a few seconds.

First-order

A functional classification of thalamic nuclei based on their main driving input: subcortical or cortical. First-order nuclei relay a particular modality of peripheral or subcortical information to a primary cortical area.

Higher-order

A functional classification of thalamic nuclei that relay information from layer five cortical neurons to other cortical areas and act like a hub in cortico – thalamo – cortical information pathways.

Intralaminar thalamic nuclei

A collection of thalamic nuclei involved in specific cognitive and motor functions that plays a key role in the salience of stimuli of various modalities.

Cell-intrinsic mechanisms

Electrical behaviour of a neuron that results from its passive and voltage-dependent electrical properties without a contribution of the synaptic network.

UP states

On the basis of their intrinsic properties and/or the influence of the synaptic network, some neurons transition between a depolarized potential, referred to as an UP state, and a hyperpolarized DOWN state.

DOWN states

A state in which the neuronal membrane potential is hyperpolarized and transitions between this state and a depolarized UP state.

T-VGCC window current

The small depolarizing tonic current that results from the fraction of T-type calcium channels that are open in a narrow membrane potential region around −60 mV.

Electrotonic properties

The combined electrical properties of a neuron that alter the manner in which subthreshold voltage changes propagate throughout the axon and the dendritic tree.

Backpropagating action potentials

(bAPs). The transient depolarization that occurs in the dendrites as a result of the generation of an action potential in the soma or axon initial segment.

Rescale

Also known as synaptic rescaling; indicates the normalization of the strength of synaptic connections that had previously been either increased or decreased in response to (relatively long-term) changes in neuronal activity.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Crunelli, V., Lőrincz, M., Connelly, W. et al. Dual function of thalamic low-vigilance state oscillations: rhythm-regulation and plasticity. Nat Rev Neurosci 19, 107–118 (2018). https://doi.org/10.1038/nrn.2017.151

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn.2017.151

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