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Unified principles of thalamo-cortical processing: the neural switch

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Abstract

It has been reported that cross-frequency interactions may play an important role in local processing within thalamus and neocortex, as well as information transfer between subcortical and cortico-cortical brain regions. Strong commonalities in rhythmic network properties have been observed across recording techniques and task demands, but strong neuroscientific theories to situate such observations within a unified framework with direct relevance to explain neuropathologies remain scarce. Based on a comprehensive review of animal and human literature, we probe and introduce a neurophysiological framework to explain how coordinated cross-frequency and interregional oscillatory cortical dynamics underlie typical and atypical brain activation, and the formation of distributed functional ensembles supporting cortical networks underpinning perception and cognition. We propose that local regional activation by an external stimulus via a sensory pathway entails (1) attenuated alpha (8–14 Hz) and increased theta (4–8 Hz) and gamma (30–50 Hz) oscillatory activity, and (2) increased interactions among theta and gamma rhythms. These local dynamics also mediate the integration of activated neural populations into large-scale functional assemblies through neuronal synchronization. This comprehensive perspective into the animal and human literature indicates a further thinking beyond synchrony and connectivity and the readiness for more hypothesis-driven research and modeling toward unified principles of thalamo-cortical processing. We further introduced such a possible framework: “The ATG switch”. We also discussed evidence that alpha–theta–gamma dynamics emerging from thalamocortical interactions may be implicated and disrupted in numerous neurological and neuropsychiatric conditions.

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References

  1. Varela F, Lachaux JP, Rodriguez E, Martinerie J. The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci. 2001;2(4):229–39.

    Article  Google Scholar 

  2. Ward LM. Synchronous neural oscillations and cognitive processes. Trends Cog Sci. 2003;7:553–9.

    Article  Google Scholar 

  3. Ribary U. Dynamics of thalamo-cortical network oscillations and human perception. Prog Brain Res. 2005;150:127–42.

    Article  Google Scholar 

  4. Uhlhaas PJ, Pipa G, Lima B, Melloni L, Neuenschwander S, Nikolić D, Singer W. Neural synchrony in cortical networks: history, concept and current status. Front Int Neurosci. 2009;3(17):1–19.

    Google Scholar 

  5. Canolty RT, Ganguly K, Kennerly SW, Cadieu CF, Koepsell K, Wallis JD, Carmena JM. Oscillatory phase coupling coordinates anatomically dispersed functional cell assemblies. Proc Natl Acad Sci USA. 2010;107:17356.

    Article  Google Scholar 

  6. Llinás R, Ribary U, Jeanmonod D, Kronberg E, Mitra PP. Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci USA. 1999;96:15222–7.

    Article  Google Scholar 

  7. Mazaheri A, Picton TW. EEG spectral dynamics during discrimination of auditory and visual targets. Cogn Brain Res. 2005;24:81–96.

    Article  Google Scholar 

  8. Sauseng P, Klimesch W, Gruber WR, Birbaumer N. Cross-frequency phase synchronization: a brain mechanism of memory matching and attention. Neuroimage. 2008;40:308–17.

    Article  Google Scholar 

  9. Doesburg SM, Green JJ, McDonald JJ, Ward LM. Rhythms of consciousness: binocular rivalry reveals large-scale oscillatory network dynamics mediating visual perception. PLoS ONE. 2009;4(7):e6142.

    Article  Google Scholar 

  10. Holz EM, Glennon M, Prendergast K, Sauseng P. Theta–gamma phase synchronization during memory matching in visual working memory. Neuroimage. 2010;67:331–43.

    Google Scholar 

  11. Palva JM, Palva S. Discovering oscillatory interaction networks with M/EEG: challenges and breakthroughs. TICS. 2012;16:219–30.

    Google Scholar 

  12. Doesburg SM, Green JJ, McDonald JJ, Ward LM. Theta modulation of inter-regional gamma synchronization during auditory attention control. Brain Res. 2012;1431:77–85.

    Article  Google Scholar 

  13. Kirschner A, Kam JWY, Handy TC, Ward LM. Differential synchronization in default and task-specific networks of the human brain. Front Hum Neurosci. 2012;6:139.

    Article  Google Scholar 

  14. Burgess AP. Towards a unified understanding of event-related changes in the EEG: the firefly model of synchronization through cross frequency phase modulation. PLoS ONE. 2012;7(9):e45630. doi:10.1371/journal.pone.0045630.

    Article  Google Scholar 

  15. FitzGerald THB, Valentin A, Selway R, Richardson MP. Cross-frequency coupling within and between the human thalamus and neocortex. Front Hum Neurosci. 2013;7:1–13.

    Article  Google Scholar 

  16. Doesburg SM, Ward LM, Ribary U. The alpha–theta–gamma (ATG) switch: toward unified principles of cortical processing. Curr Trends Neurol. 2015;9:1–12.

    Google Scholar 

  17. Von Stein A, Sarnthein J. Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. Int J Psychophsiol. 2000;38:301–13.

    Article  Google Scholar 

  18. Klimesch W, Sauseng P, Hanslmayr S. EEG alpha oscillations: the inhibition timing hypothesis. Brian Res Rev. 2007;53:63–88.

    Article  Google Scholar 

  19. Pfurtscheller G, Stancak A, Neuper C. Event-related synchronization (ERS) in the alpha-band—an electrophysiological correlate of cortical idling: a review. Int J Psychophysiol. 1996;24:39–46.

    Article  Google Scholar 

  20. Rihs TA, Michel CM, Thut G. Mechanisms of selective inhibition in visual spatial attention are indexed by α-band EEG synchronization. Eur J Neurosci. 2007;25:603–10.

    Article  Google Scholar 

  21. Hanslmayer S, Gross J, Klimesch W, Shapiro KL. The role of alpha oscillations in temporal attention. Brain Res Rev. 2011;67:331–43.

    Article  Google Scholar 

  22. Haegens S, Nácher V, Luna R, Romo R, Jensen O. α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking. Proc Natl Acad Sci USA. 2011;108:19377–82.

    Article  Google Scholar 

  23. Palva JM, Monto S, Kulashekhar S, Palva S. Neuronal synchrony reveals working memory networks and predicts individual memory capacity. Proc Natl Acad Sci USA. 2010;107:7580–5.

    Article  Google Scholar 

  24. Doesburg SM, Ribary U, Herdman AT, Miller SP, Poskitt KJ, Moiseev A, Whitfield MF, Synnes A, Grunau RE. Altered long-range alpha-band synchronization during visual short-term memory retention in children born very preterm. Neuroimage. 2011;54:2330–9.

    Article  Google Scholar 

  25. Jensen O, Mazaheri A. Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front Hum Neurosci. 2010;4:1–8.

    Article  Google Scholar 

  26. Jensen O, Kaiser J, Lachaux JP. Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci. 2007;30:317–24.

    Article  Google Scholar 

  27. Ribary U, Ioannides AA, Singh KD, Hasson R, Bolton JPR, Lado F, Mogilner A, Llinas R. Magnetic field tomography (MFT) of coherent thalamo-cortical 40-Hz oscillations in humans. Proc Natl Acad Sci USA. 1991;88:11037–41.

    Article  Google Scholar 

  28. Tallon-Baudry C, Bertrand O, Peronnet F, Pernier J. Induced g-band activity during the delay of a visual short-term memory task in humans. J Neurosci. 1998;18:4244–54.

    Google Scholar 

  29. Fell J, Klaver P, Elger CE, Fernández G. Suppression of EEG gamma activity may cause the attentional blink. Conscious Cogn. 2002;11:114–22.

    Article  Google Scholar 

  30. Fries P. Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci. 2009;32:209–24.

    Article  Google Scholar 

  31. Kahana MJ, Seelig D, Madsen JR. Theta returns. Curr Opin Neurobiol. 2001;11:739–44.

    Article  Google Scholar 

  32. Sauseng P, Griesmayr B, Freunberger R, Klimesch W. Control mechanisms in working memory: a possible function of EEG theta oscillations. Neurosci Biobehav Rev. 2010;34:739–44.

    Article  Google Scholar 

  33. Caplan JB, Madsen JR, Schulze-Bonhage A, Aschenbrenner-Scheibe R, Newman EL, Kahana MJ. Human theta oscillations related to sensorimotor integration and spatial learning. J Neurosci. 2003;23:4726–36.

    Google Scholar 

  34. Osipova D, Takashima A, Oostenveld R, Fernandez G, Maris E, Jensen O. Theta and gamma oscillations predict encoding and retrieval of declarative memory. J Neurosci. 2006;26:7523–31.

    Article  Google Scholar 

  35. Ribary U, Doesburg SM, Ward LM. Thalamocortical network dynamics: a framework for typical/atypical cortical oscillations and connectivity. In: Supek S, Aine CJ, editors. Magnetoencephalography—from signals to dynamic cortical networks. Heidelberg: Springer; 2014. p. 429–50.

    Google Scholar 

  36. Llinas R, Ribary U, Joliot M, Wang XJ. Content and context in temporal thalamocortical binding. In: Buzsaki G, Llinas R, Singer W, Berthoz A, Christen Y, editors. Temporal coding in the brain. Heidelberg: Springer; 1994. p. 251–72.

    Chapter  Google Scholar 

  37. Llinás R, Ribary U. Coherent 40-Hz oscillation characterizes dream state in humans. Proc Natl Acad Sci USA. 1993;90:2078–81.

    Article  Google Scholar 

  38. Jones EG. The thalamic matrix and thalamocortical synchrony. Trends Neurosci. 2001;24:595–601.

    Article  Google Scholar 

  39. Llinás R, Ribary U, Contreras D, Pedroarena C. The neuronal basis for consciousness. Philos Trans R Soc Lond. 1998;353:1841–9.

    Article  Google Scholar 

  40. Ward LM. The thalamic dynamic core theory of conscious experience. Conscious Cogn. 2011;20:464–86.

    Article  Google Scholar 

  41. Buzsáki G, Chrobak JJ. Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neurobiol. 1995;5:504.

    Article  Google Scholar 

  42. Melzer S, Michael M, Caputi A, Eliava M, Fuchs EC, Whittington MA, Monyer H. Long-range–projecting GABAergic neurons modulate inhibition in hippocampus and entorhinal cortex. Science. 2012;335:1506–10.

    Article  Google Scholar 

  43. Zilles K, Amunts K. Segregation and wiring in the brain. Science. 2012;335:1582–4.

    Article  Google Scholar 

  44. Proske JH, Jeanmonod D, Verschure PFMJ. A computational model of thalamocortical dysrhythmia. Eur J Neurosci. 2011;. doi:10.1111/j.1460-9568.2010.07588.x.

    Google Scholar 

  45. Jeanmonod D, Magnin M, Morel A. Low-threshold calcium spike bursts in the human thalamus: common physiopathology for sensory, motor and limbic positive symptoms. Brain. 1996;119:363–75.

    Article  Google Scholar 

  46. Sarnthein J, Jeanmonod D. High thalamocortical coherence in patients with Parkinson’s disease. J Neurosci. 2007;27:124–31.

    Article  Google Scholar 

  47. Sarnthein J, Jeanmonod D. High thalamocortical coherence in patients with neurogenic pain. NeuroImage. 2008;39:1910–7.

    Article  Google Scholar 

  48. De Ridder D, Vanneste S, Langguth B, Llinas R. Thalamocortical dysrhythmia: a theoretical update in tinnitus. Front Neurol. 2015;6:124.

    Article  Google Scholar 

  49. Lashley KS. The problem of serial order in behavior. In: Jeffress LA, editor. Cerebral mechanisms in behavior. New York: Wiley; 1951.

    Google Scholar 

  50. Ward LM. Dynamical cognitive science. Cambridge: MIT Press; 2002.

    Google Scholar 

  51. Roux F, Uhlhaas PJ. Working memory and neural oscillations: alpha–gamma versus theta–gamma codes for distinct WM information? Trends Cog Sci. 2014;18:16–25.

    Article  Google Scholar 

  52. Jensen O, Gips B, Bergmann TO, Bonnefond M. Temporal coding organized by coupled alpha and gamma oscillations prioritize visual processing. Trends Neurosci. 2014;37:357–69.

    Article  Google Scholar 

  53. Spaak E, Bonnefond M, Maier A, Leopold DA, Jensen O. Layer-specific entrainment of gamma-band neural activity by the alpha rhythm in monkey visual cortex. Curr Biol. 2012;22:2313–8.

    Article  Google Scholar 

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Acknowledgements

This work was facilitated by funding from the BC Leading Edge Endowment Fund (BC LEEF) to UR, the Canadian Foundation for Innovation (CFI, CFI-IOF) relating to the Behavioral and Cognitive Neuroscience Institute (BCNI) to UR; from the Canadian Institutes of Health Research (CIHR: MOP-136935) and the Natural Sciences and Engineering Research Council (NSERC) of Canada (RGPIN-435659) to SMD; and from NSERC (A9958) to LMW. We thank Drs. Mazaheri, Picton, Burgess and Canolty for their generous permission to use modified parts of figures from their papers [5, 7, 14].

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Ribary, U., Doesburg, S.M. & Ward, L.M. Unified principles of thalamo-cortical processing: the neural switch. Biomed. Eng. Lett. 7, 229–235 (2017). https://doi.org/10.1007/s13534-017-0033-4

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  • DOI: https://doi.org/10.1007/s13534-017-0033-4

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