Advertisement

Thalamo-Cortical Interactions and Synchronous Oscillations in MEG Data

  • Peter J. UhlhaasEmail author
  • Frédéric Roux
Chapter

Abstract

The thalamus has received a renewed interest in systems neuroscience because emerging evidence indicates that the thalamus may modulate cortical responses according to behavioral demands. Moreover, there is evidence to suggest that in addition to normal brain functioning, thalamic–cortical (TC) interactions are critically implicated in neuropsychiatric disorders, such as schizophrenia. In this chapter, we will discuss the possibility to examine TC interactions using magnetoencephalography (MEG), a technique that is commonly considered as too unreliable to monitor activity generated by thalamic sources. Here, we argue that if certain requirements are met, MEG can be employed to investigate TC interactions by combining advanced source reconstruction techniques and novel connectivity measures. Specifically, we summarize evidence from MEG experiments that examined alpha–gamma coupling in TC networks during resting-state recordings as well as data from a study that tested the effects of ketamine on neural oscillations in healthy volunteers. We will discuss the implication of these findings for the understanding of normal and abnormal brain functioning as well as further steps to validate and improve MEG as a noninvasive technique to probe interactions in TC circuits.

Keywords

Deep Brain Stimulation Lateral Geniculate Nucleus Transfer Entropy Alpha Oscillation Cortical Source 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Ahlfors SP et al (2010a) Sensitivity of MEG and EEG to source orientation. Brain Topogr 23:227–232CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ahlfors SP et al (2010b) Cancellation of EEG and MEG signals generated by extended and distributed sources. Hum Brain Mapp 31:140–149PubMedPubMedCentralGoogle Scholar
  3. Attal Y, Schwartz D (2013) Assessment of subcortical source localization using deep brain activity imaging model with minimum norm operators: a MEG study. PLoS One 8, e59856CrossRefPubMedPubMedCentralGoogle Scholar
  4. Attal Y et al (2007) Modeling and detecting deep brain activity with MEG & EEG. Conf Proc IEEE Eng Med Biol Soc 2007:4937–4940Google Scholar
  5. Bastos AM et al (2014) Simultaneous recordings from the primary visual cortex and lateral geniculate nucleus reveal rhythmic interactions and a cortical source for γ-band oscillations. J Neurosci 34:7639–7644CrossRefPubMedPubMedCentralGoogle Scholar
  6. Brookes MJ et al (2008) Optimising experimental design for MEG beamformer imaging. Neuroimage 39:1788–1802CrossRefPubMedGoogle Scholar
  7. Buzsáki G, Wang X-J (2012) Mechanisms of gamma oscillations. Annu Rev Neurosci 35:203–225CrossRefPubMedPubMedCentralGoogle Scholar
  8. Castelo-Branco M et al (1998) Synchronization of visual responses between the cortex, lateral geniculate nucleus, and retina in the anesthetized cat. J Neurosci 18:6395–6410PubMedGoogle Scholar
  9. Chorlian DB et al (2006) Amplitude modulation of gamma band oscillations at alpha frequency produced by photic driving. Int J Psychophysiol 61:262–278CrossRefPubMedGoogle Scholar
  10. Cohen MX et al (2009) Good vibrations: cross-frequency coupling in the human nucleus accumbens during reward processing. J Cogn Neurosci 21:875–889CrossRefPubMedGoogle Scholar
  11. Crick F (1984) Function of the thalamic reticular complex: the searchlight hypothesis. Proc Natl Acad Sci USA 81:4586–4590CrossRefPubMedPubMedCentralGoogle Scholar
  12. de Curtis M et al (1989) Excitatory amino acids mediate responses elicited in vitro by stimulation of cortical afferents to reticularis thalami neurons of the rat. Neuroscience 33:275–283CrossRefPubMedGoogle Scholar
  13. Deschênes M, Hu B (1990) Membrane resistance increase induced in thalamic neurons by stimulation of brainstem cholinergic afferents. Brain Res 513:339–342CrossRefPubMedGoogle Scholar
  14. Diester I et al (2011) An optogenetic toolbox designed for primates. Nat Neurosci 14:387–397CrossRefPubMedPubMedCentralGoogle Scholar
  15. Doesburg S et al (2016) Top-down alpha oscillatory network interactions during visuospatial attention orienting. Neuroimage 132:512–519CrossRefPubMedGoogle Scholar
  16. Dugué L et al (2011) The phase of ongoing oscillations mediates the causal relation between brain excitation and visual perception. J Neurosci 31:11889–11893CrossRefPubMedGoogle Scholar
  17. Dumas T et al (2013) MEG evidence for dynamic amygdala modulations by gaze and facial emotions. PLoS One 8, e74145CrossRefPubMedPubMedCentralGoogle Scholar
  18. Foster BL, Parvizi J (2012) Resting oscillations and cross-frequency coupling in the human posteromedial cortex. Neuroimage 60:384–391CrossRefPubMedGoogle Scholar
  19. Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474–480CrossRefPubMedGoogle Scholar
  20. Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32:209–224CrossRefPubMedGoogle Scholar
  21. Ghose GM, Freeman RD (1992) Oscillatory discharge in the visual system: does it have a functional role? J Neurophysiol 68:1558–1574PubMedGoogle Scholar
  22. Golshani P, Jones EG (1999) Synchronized paroxysmal activity in the developing thalamocortical network mediated by corticothalamic projections and “silent” synapses. J Neurosci 19:2865–2875PubMedGoogle Scholar
  23. Golshani P et al (1998) Progression of change in NMDA, non-NMDA, and metabotropic glutamate receptor function at the developing corticothalamic synapse. J Neurophysiol 80:143–154PubMedGoogle Scholar
  24. Gross J et al (2001) Dynamic imaging of coherent sources: studying neural interactions in the human brain. Proc Natl Acad Sci USA 98:694–699CrossRefPubMedPubMedCentralGoogle Scholar
  25. Guillery RW, Sherman SM (2011) Branched thalamic afferents: what are the messages that they relay to the cortex? Brain Res Rev 66:205–219CrossRefPubMedGoogle Scholar
  26. Gunduz-Bruce H (2009) The acute effects of NMDA antagonism: from the rodent to the human brain. Brain Res Rev 60:279–286CrossRefPubMedGoogle Scholar
  27. Haegens S et al (2011) α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking. Proc Natl Acad Sci USA 108:19377–19382CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hu B et al (1989) The cellular mechanism of thalamic ponto-geniculo-occipital waves. Neuroscience 31:25–35CrossRefPubMedGoogle Scholar
  29. Hung Y et al (2010) Unattended emotional faces elicit early lateralized amygdala-frontal and fusiform activations. Neuroimage 50:727–733CrossRefPubMedGoogle Scholar
  30. Hunt MJ, Kasicki S (2013) A systematic review of the effects of NMDA receptor antagonists on oscillatory activity recorded in vivo. J Psychopharmacol (Oxf Engl) 27:972–986CrossRefGoogle Scholar
  31. Jacobsen RB et al (2001) GABA(B) and NMDA receptors contribute to spindle-like oscillations in rat thalamus in vitro. J Neurophysiol 86:1365–1375PubMedGoogle Scholar
  32. Jensen O, Mazaheri A (2010) Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front Hum Neurosci 4:186CrossRefPubMedPubMedCentralGoogle Scholar
  33. Jensen O et al (2014) Temporal coding organized by coupled alpha and gamma oscillations prioritize visual processing. Trends Neurosci 37:357–369CrossRefPubMedGoogle Scholar
  34. Jones EG (2001) The thalamic matrix and thalamocortical synchrony. Trends Neurosci 24:595–601CrossRefPubMedGoogle Scholar
  35. Kao CQ, Coulter DA (1997) Physiology and pharmacology of corticothalamic stimulation-evoked responses in rat somatosensory thalamic neurons in vitro. J Neurophysiol 77:2661–2676PubMedGoogle Scholar
  36. Kirov G et al (2012) De novo CNV analysis implicates specific abnormalities of postsynaptic signalling complexes in the pathogenesis of schizophrenia. Mol Psychiatry 17:142–153CrossRefPubMedGoogle Scholar
  37. Klimesch W et al (2007) EEG alpha oscillations: the inhibition–timing hypothesis. Brain Res Rev 53:63–88CrossRefPubMedGoogle Scholar
  38. Kocsis B (2012) Differential role of NR2A and NR2B subunits in N-methyl-D-aspartate receptor antagonist-induced aberrant cortical gamma oscillations. Biol Psychiatry 71:987–995CrossRefPubMedGoogle Scholar
  39. Litvak V et al (2010) Optimized beamforming for simultaneous MEG and intracranial local field potential recordings in deep brain stimulation patients. Neuroimage 50:1578–1588CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lopes da Silva FH et al (1980) Relative contributions of intracortical and thalamo-cortical processes in the generation of alpha rhythms, revealed by partial coherence analysis. Electroencephalogr Clin Neurophysiol 50:449–456CrossRefPubMedGoogle Scholar
  41. Lorincz ML et al (2009) Temporal framing of thalamic relay-mode firing by phasic inhibition during the alpha rhythm. Neuron 63:683–696CrossRefPubMedPubMedCentralGoogle Scholar
  42. Manning JR et al (2009) Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans. J Neurosci 29:13613–13620CrossRefPubMedPubMedCentralGoogle Scholar
  43. Miller KJ (2010) Broadband spectral change: evidence for a macroscale correlate of population firing rate? J Neurosci 30:6477–6479CrossRefPubMedGoogle Scholar
  44. Miller KJ et al (2010) Dynamic modulation of local population activity by rhythm phase in human occipital cortex during a visual search task. Front Hum Neurosci 4:197CrossRefPubMedPubMedCentralGoogle Scholar
  45. Moghaddam B, Javitt D (2012) From revolution to evolution: the glutamate hypothesis of schizophrenia and its implication for treatment. Neuropsychopharmacology 37:4–15CrossRefPubMedGoogle Scholar
  46. Monaghan DT, Cotman CW (1985) Distribution of N-methyl-D-aspartate-sensitive L-[3H]glutamate-binding sites in rat brain. J Neurosci 5:2909–2919PubMedGoogle Scholar
  47. Neuenschwander S et al (2002) Feed-forward synchronization: propagation of temporal patterns along the retinothalamocortical pathway. Philos Trans R Soc Lond B Biol Sci 357:1869–1876CrossRefPubMedPubMedCentralGoogle Scholar
  48. Nolte G et al (2004) Localizing brain interactions from rhythmic EEG/MEG data. Conf Proc IEEE Eng Med Biol Soc 2:998–1001PubMedGoogle Scholar
  49. O’Donnell P, Grace AA (1998) Dysfunctions in multiple interrelated systems as the neurobiological bases of schizophrenic symptom clusters. Schizophr Bull 24:267–283CrossRefPubMedGoogle Scholar
  50. Osipova D et al (2008) Gamma power is phase-locked to posterior alpha activity. PLoS One 3, e3990CrossRefPubMedPubMedCentralGoogle Scholar
  51. Parkkonen L et al (2009) Sources of auditory brainstem responses revisited: contribution by magnetoencephalography. Hum Brain Mapp 30:1772–1782CrossRefPubMedGoogle Scholar
  52. Parnaudeau S et al (2013) Inhibition of mediodorsal thalamus disrupts thalamofrontal connectivity and cognition. Neuron 77:1151–1162CrossRefPubMedPubMedCentralGoogle Scholar
  53. Pinault D (2011) Dysfunctional thalamus-related networks in schizophrenia. Schizophr Bull 37:238–243CrossRefPubMedPubMedCentralGoogle Scholar
  54. Pinault D, Deschênes M (1992) Control of 40-Hz firing of reticular thalamic cells by neurotransmitters. Neuroscience 51:259–268CrossRefPubMedGoogle Scholar
  55. Rasch MJ et al (2008) Inferring spike trains from local field potentials. J Neurophysiol 99:1461–1476CrossRefPubMedGoogle Scholar
  56. Ribary U et al (1991) Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans. Proc Natl Acad Sci USA 88:11037–11041CrossRefPubMedPubMedCentralGoogle Scholar
  57. Roux F et al (2013) The phase of thalamic alpha activity modulates cortical gamma-band activity: evidence from resting-state MEG recordings. J Neurosci 33:17827–17835CrossRefPubMedPubMedCentralGoogle Scholar
  58. Saalmann YB (2014) Intralaminar and medial thalamic influence on cortical synchrony, information transmission and cognition. Front Syst Neurosci 8:83CrossRefPubMedPubMedCentralGoogle Scholar
  59. Saalmann YB, Kastner S (2009) Gain control in the visual thalamus during perception and cognition. Curr Opin Neurobiol 19:408–414CrossRefPubMedPubMedCentralGoogle Scholar
  60. Saalmann YB, Kastner S (2011) Cognitive and perceptual functions of the visual thalamus. Neuron 71:209–223CrossRefPubMedPubMedCentralGoogle Scholar
  61. Saalmann YB et al (2012) The pulvinar regulates information transmission between cortical areas based on attention demands. Science 337:753–756CrossRefPubMedPubMedCentralGoogle Scholar
  62. Scharfman HE et al (1990) N-methyl-D-aspartate receptors contribute to excitatory postsynaptic potentials of cat lateral geniculate neurons recorded in thalamic slices. Proc Natl Acad Sci USA 87:4548–4552CrossRefPubMedPubMedCentralGoogle Scholar
  63. Scheeringa R et al (2011) Modulation of visually evoked cortical FMRI responses by phase of ongoing occipital alpha oscillations. J Neurosci 31:3813–3820CrossRefPubMedGoogle Scholar
  64. Schmid MC et al (2012) Thalamic coordination of cortical communication. Neuron 75:551–552CrossRefPubMedGoogle Scholar
  65. Schobel SA et al (2013) Imaging patients with psychosis and a mouse model establishes a spreading pattern of hippocampal dysfunction and implicates glutamate as a driver. Neuron 78:81–93CrossRefPubMedPubMedCentralGoogle Scholar
  66. Schoffelen J-M, Gross J (2009) Source connectivity analysis with MEG and EEG. Hum Brain Mapp 30:1857–1865CrossRefPubMedGoogle Scholar
  67. Sekihara K et al (2001) Reconstructing spatio-temporal activities of neural sources using an MEG vector beamformer technique. IEEE Trans Biomed Eng 48:760–771CrossRefPubMedGoogle Scholar
  68. Sherman SM (2007) The thalamus is more than just a relay. Curr Opin Neurobiol 17:417–422CrossRefPubMedPubMedCentralGoogle Scholar
  69. Sherman SM (2012) Thalamocortical interactions. Curr Opin Neurobiol 22:575–579CrossRefPubMedPubMedCentralGoogle Scholar
  70. Sherman SM, Guillery RW (2001) Exploring the thalamus. Academic, New YorkGoogle Scholar
  71. Sherman SM, Guillery RW (2006) Exploring the thalamus and its role in cortical function. MIT, Cambridge, MAGoogle Scholar
  72. Sherman SM, Guillery RW (2011) Distinct functions for direct and transthalamic corticocortical connections. J Neurophysiol 106:1068–1077CrossRefPubMedGoogle Scholar
  73. Sherman SM, Koch C (1986) The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Exp Brain Res 63:1–20CrossRefPubMedGoogle Scholar
  74. Singer W (1994) Neurobiology. A new job for the thalamus. Nature 369:444–445CrossRefPubMedGoogle Scholar
  75. Spaak E et al (2012) Layer-specific entrainment of gamma-band neural activity by the alpha rhythm in monkey visual cortex. Curr Biol 22:2313–2318CrossRefPubMedPubMedCentralGoogle Scholar
  76. Staudigl T, Hanslmayr S (2013) Theta oscillations at encoding mediate the context-dependent nature of human episodic memory. Curr Biol 23:1101–1106CrossRefPubMedGoogle Scholar
  77. Tesche CD (1996) Non-invasive imaging of neuronal population dynamics in human thalamus. Brain Res 729:253–258CrossRefPubMedGoogle Scholar
  78. Timofeev I, Steriade M (1997) Fast (mainly 30–100 Hz) oscillations in the cat cerebellothalamic pathway and their synchronization with cortical potentials. J Physiol 504(Pt 1):153–168CrossRefPubMedPubMedCentralGoogle Scholar
  79. Toledo JB et al (2014) High beta activity in the subthalamic nucleus and freezing of gait in Parkinson’s disease. Neurobiol Dis 64:60–65CrossRefPubMedGoogle Scholar
  80. Turner JP, Salt TE (1998) Characterization of sensory and corticothalamic excitatory inputs to rat thalamocortical neurones in vitro. J Physiol 510(Pt 3):829–843CrossRefPubMedPubMedCentralGoogle Scholar
  81. Uhlhaas PJ, Singer W (2006) Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52:155–168CrossRefPubMedGoogle Scholar
  82. Urrestarazu E et al (2009) Beta activity in the subthalamic nucleus during sleep in patients with Parkinson’s disease. Mov Disord 24:254–260CrossRefPubMedGoogle Scholar
  83. Van Veen BD et al (1997) Localization of brain electrical activity via linearly constrained minimum variance spatial filtering. IEEE Trans Biomed Eng 44:867–880CrossRefPubMedGoogle Scholar
  84. Varela FJ et al (1981) Perceptual framing and cortical alpha rhythm. Neuropsychologia 19:675–686CrossRefPubMedGoogle Scholar
  85. Vicente R et al (2011) Transfer entropy—a model-free measure of effective connectivity for the neurosciences. J Comput Neurosci 30:45–67CrossRefPubMedGoogle Scholar
  86. Vijayan S, Kopell NJ (2012) Thalamic model of awake alpha oscillations and implications for stimulus processing. Proc Natl Acad Sci USA 109:18553–18558CrossRefPubMedPubMedCentralGoogle Scholar
  87. von Krosigk M et al (1993) Cellular mechanisms of a synchronized oscillation in the thalamus. Science 261:361–364CrossRefGoogle Scholar
  88. Voytek B et al (2010) Shifts in gamma phase-amplitude coupling frequency from theta to alpha over posterior cortex during visual tasks. Front Hum Neurosci 4:191CrossRefPubMedPubMedCentralGoogle Scholar
  89. Whittingstall K, Logothetis NK (2009) Frequency-band coupling in surface EEG reflects spiking activity in monkey visual cortex. Neuron 64:281–289CrossRefPubMedGoogle Scholar
  90. Wibral M et al (2011) Transfer entropy in magnetoencephalographic data: quantifying information flow in cortical and cerebellar networks. Prog Biophys Mol Biol 105:80–97CrossRefPubMedGoogle Scholar
  91. Wibral M et al (2013) Measuring information-transfer delays. PLoS One 8, e55809. doi: 10.1371/journal.pone.0055809 CrossRefPubMedPubMedCentralGoogle Scholar
  92. Woodward ND et al (2012) Thalamocortical dysconnectivity in schizophrenia. Am J Psychiatry 169:1092–1099CrossRefPubMedGoogle Scholar
  93. Wróbel A et al (2007) Two streams of attention-dependent beta activity in the striate recipient zone of cat’s lateral posterior-pulvinar complex. J Neurosci 27:2230–2240CrossRefPubMedGoogle Scholar
  94. Yanagisawa T et al (2012) Regulation of motor representation by phase-amplitude coupling in the sensorimotor cortex. J Neurosci 32:15467–15475CrossRefPubMedGoogle Scholar
  95. Yelnik J et al (1984) A Golgi analysis of the primate globus pallidus. II. Quantitative morphology and spatial orientation of dendritic arborizations. J Comp Neurol 227:200–213CrossRefPubMedGoogle Scholar
  96. Zhang Y et al (2012) NMDAR antagonist action in thalamus imposes δ oscillations on the hippocampus. J Neurophysiol 107:3181–3189CrossRefPubMedPubMedCentralGoogle Scholar
  97. Zhu Z et al (2009) The relationship between magnetic and electrophysiological responses to complex tactile stimuli. BMC Neurosci 10:4CrossRefPubMedPubMedCentralGoogle Scholar
  98. Zumer JM et al (2010) MEG in the macaque monkey and human: distinguishing cortical fields in space and time. Brain Res 1345:110–124CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Institute for Neuroscience and PsychologyGlasgow UniversityGlasgowUK
  2. 2.School of Psychology, College of Life and Environmental SciencesUniversity of BirminghamBirminghamUK
  3. 3.BCBL, Basque Center on Cognition, Brain and LanguageDonostia-San SebastianSpain

Personalised recommendations