Magnetoencephalography pp 429-449 | Cite as
Thalamocortical Network Dynamics: A Framework for Typical/Atypical Cortical Oscillations and Connectivity
Abstract
Recently there has been increased interest in understanding the brain’s functional connectivity within local and long-range networks. While structural and functional connectivity at the cortical level has received considerable attention, the structure and functional dynamics of thalamo-cortical interactions are as yet insufficiently integrated with our knowledge of large-scale connectivity and regional function. An important question, yet to be answered in detail, is how typical cognitive functions and their alterations in neuro-psychiatric pathologies are temporally generated across the entire brain space (thalamo-cortical, cortico-cortical, cortico-thalamic) based on intact or altered brain structure and function. We review MEG and related EEG research in the context of multimodal imaging findings, focusing on thalamo-cortical dynamics and their role in functional connectivity across cortico-cortical, and cortico-thalamic circuits, including oscillatory synchronization within and across the various frequency bands underlying cognition. We then further explore the cognitive consequences of various disruptions of thalamo-cortical and cortico-cortical dynamics, including slowing and selective loss of functional network dynamics in particular brain networks related to disabilities or pathologies. We present an overview of current findings and their conceptual implications for how brain imaging technologies can further contribute to a better understanding of the brain’s structural, functional and temporal connectivity dynamics and their relationship to typical and atypical cognition and consciousness.
Keywords
Thalamo-cortical Cortico-cortical Cortico-thalamic Synchronization Functional connectivity dynamics Alpha Theta Gamma Cognition Consciousness Cognitive deficit Neurology Psychiatry Traumatic brain injuryNotes
Acknowledgements
Preparation of this chapter was facilitated by funding from the Canadian BC Leading Edge Endowment Fund (BC LEEF) to UR, the Canadian Foundation for Innovation (CFI) and related Operating Funds for the Behavioral and Cognitive Neuroscience Institute (BCNI) to UR, from the Natural Sciences and Engineering Research Council (NSERC) of Canada to LMW and from the Hospital for Sick Children Centre for Brain and Behavior, the Ontario Brain Institute to SMD.
References
- Alkire MT, Hudetz AG, Tononi G (2008) Consciousness and anesthesia. Science 322:876–880Google Scholar
- Babloyantz A (1991) Self-organization, emerging properties and learning. Plenum Press, New YorkGoogle Scholar
- Banerjee S, Snyder AC, Molholm S, Foxe JJ (2011) Oscillatory alpha-band mechanisms and the deployment of spatial attention to anticipated auditory and visual target locations: supramodal or sensory-specific control mechanisms? J Neurosci 31:9923–9932Google Scholar
- Barth DS, MacDonald KD (1996) Thalamic modulation of high-frequency oscillating potentials in auditory cortex. Nature 383:78–81Google Scholar
- Benasich AA, Tallal P (2002) Infant discrimination of rapid auditory cues predicts later language impairment. Behav Brain Res 136:31–49Google Scholar
- Benasich AA, Fitch RH (2012) Developmental dyslexia. Paul H Brooks Publishing Co, Baltimore, USAGoogle Scholar
- Boly M, Garrido MI, Gosseries O, Bruno MA, Boveroux P, Schnakers C, et al (2011) Preserved feedforward but impaired top-down processes in the vegetative state. Science 332:858–862Google Scholar
- Castaigne P, Lhermitte F, Buge A, Escourolle P, Derouisne C, Der Agopian P et al (1980) Paramedian thalamic and midbrain infarcts: clinical and neuropathological study. Ann Neurol 10:127–214Google Scholar
- Crick F, Koch C (1990) Some reflections on visual awareness. Cold Spring Harbor Sympos Quant Biol 55:953–962Google Scholar
- DeVolder AG, Goffinet AM, Bol A, Michel C, de Barsy T, Laterre C (1990) Brain glucose metabolism in postanoxic stroke. Arch Neurol 47:197–204Google Scholar
- Doesburg SM, Roggeveen AB, Kitajo K, Ward LM (2008) Large-scale gamma-band phase synchronization and selective attention. Cereb Cortex 18:386–396Google Scholar
- Doesburg SM, Green JJ, McDonald JJ, Ward LM (2009) Rhythms of consciousness: binocular rivalry reveals large-scale oscillatory network dynamics mediating visual perception. PLoS ONE 4:e6142Google Scholar
- Doesburg SM, Herdman AT, Ribary U, Cheung T, Moiseev A, Weinberg H, Liotti M, Weeks D, Grunau RE (2010) Long-range synchronization and local desynchronization of alpha oscillations during visual short-term memory retention in children. Exp Brain Res 4:719–727Google Scholar
- Doesburg SM, Ribary U, Herdman AT, Miller SP, Poskitt KJ, Moiseev A, Whitfield MF, Synnes A, Grunau RE (2011a) Altered long-range alpha-band synchronization during visual short-term memory retention in children born very preterm. Neuroimage 54:2330–2339Google Scholar
- Doesburg S, Ribary U, Herdman AT, Moiseev A, Cheung T, Miller SP, Poskitt KJ, Weinberg H, Whitfield MF, Synnes A, Grunau RE (2011b) Magnetoencephalography reveals slowing of resting peak oscillatory frequency in children born very preterm. J Paediatr Res 70:171–176Google Scholar
- Doesburg SM, Green JJ, McDonald JJ, Ward LM (2012) Theta modulation of inter-regional gamma synchronization during auditory attention control. Brain Res 1431:77–85Google Scholar
- Façon E, Steriade M, Wertheim N (1958) Hypersomnie prolongée engendrée par les lésions bilatérales du système activateur médial. Le syndrome thrombotique de la bifurcation du tronc basilaire. Rev Neurol (Paris) 98:117–133Google Scholar
- Fair DA, Bathula D, Mills KL, Costa Dias TG, Blythe MS, Zhang D et al (2010) Maturing thalamocortical functional connectivity across development. Front Syst Neurosci 4:1–10Google Scholar
- Fell J et al (2002) Suppression of EEG gamma activity may cause the attentional blink. Conscious Cogn 11:114–122Google Scholar
- Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291:1506–1507Google Scholar
- Fries P (2005) A mechanism for cognitive dynamics: Neuronal communication through neuronal coherence. Trends Cog Sci 9:474–480Google Scholar
- Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Ann Rev Neurosci 32:209–224Google Scholar
- Gabrieli JDE (2009) Dyslexia: a new synergy between education and cognitive neuroscience. Science 325:280–283Google Scholar
- Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci USA 86:1698–1702Google Scholar
- Gray CM (1999) The temporal correlation hypothesis of visual feature integration: Still alive and well. Neuron 24:31–47Google Scholar
- Green JJ, Doesburg SM, Ward LM, McDonald JJ (2011) Electrical neuroimaging of voluntary audiospatial attention: evidence for a supramodal attention control network. J Neurosci 31:3560–3564Google Scholar
- Griesmayr B, Gruber WR, Klimesch W, Sauseng P (2010) Human frontal midline theta and its synchronization to gamma during a verbal delayed match to sample task. Neurobiol Learn Mem 93:208–215Google Scholar
- Guillery RW, Sherman SM (2002) The thalamus as a monitor of motor outputs. Phil Trans R Soc Lond 357:1809–1821Google Scholar
- Hanslmayer S, Gross J, Klimesch W, Shapiro KL (2011) The role of alpha oscillations in temporal attention. Brain Res Rev 67:331–343Google Scholar
- Hari R, Salmelin R (1997) Human cortical oscillations: a neuromagnetic view through the skull. Trends Neurosci 20:44–49Google Scholar
- Heim S, Eulitz C, Kaufmann J, Fuchter I, Pantev C, Lamprecht-Dinnesen A et al (2000) Atypical organisation of the auditory cortex in dyslexia as revealed by MEG. Neuropsychologia 38:1749–1759Google Scholar
- Helenius P, Uutela K, Hari R (1999) Auditory stream segregation in dyslexic adults. Brain 122:907–913Google Scholar
- Huang MX, Nichols S, Robb A, Angeles A, Drake A, Holland M, Asmussen S, D’Andrea J, Chun W, Levy M, Cui L, Song T, Baker DG, Hammer P, McLay R, Theilmann RJ, Coimbra R, Diwakar M, Boyd C, Neff J, Liu TT, Webb-Murphy J, Farinpour R, Cheung C, Harrington DL, Heister D, Lee RR (2012) An automatic MEG low-frequency source imaging approach for detecting injuries in mild and moderate TBI patients with blast and non-blast causes. Neuroimage 61:1067Google Scholar
- Jahnsen H, Llinás RR (1984) Electro-physiological properties of guinea-pig thalamic neurones: An in vitro study. J Physiol 349:205–226Google Scholar
- Jeanmonod D, Magnin M, Morel A (1996) Low-threshold calcium spike bursts in the human thalamus: common physiopathology for sensory, motor and limbic positive symptoms. Brain 119:363–375Google Scholar
- Jeanmonod D, Magnin M, Morel A, Siegemund M, Cancro R, Lanz M, Llinás R, Ribary U, Kronberg E, Schulman JJ, Zonenshayn M (2001) Thalamocortical dysrhythmia II: clinical and surgical aspects. Thal Rel Syst 1:245–254Google Scholar
- Jensen O, Vanni S (2002) A new method to identify multiple sources of oscillatory activity. NeuroImage 15:568–574Google Scholar
- Jensen O, Kaiser J, Lachaux JP (2007) Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci 30:317–324Google Scholar
- Jensen O, Mazaheri A (2010) Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front Hum Neurosci 4:1–8Google Scholar
- Jerbi K, Ossandón T, Hamamé CM, Senova S, Dalal SS et al (2009) Task-related gamma-band dynamics from an intracerebral perspective: review and implications for surface EEG and MEG. Hum Brain Mapp 30:1758–1771Google Scholar
- John ER, Prichep LS, Friedman J, Easton P (1988) Neurometrics: Computer assisted differential diagnosis of brain dysfunctions. Science 293:162–169Google Scholar
- Joliot M, Ribary U, Llinás R (1994) Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding. Proc Natl Acad Sci USA 91:11748–11751Google Scholar
- Jones EG (2001) The thalamic matrix and thalamocortical synchrony. Trends Neurosci 24:595–601Google Scholar
- Jones EG (2002) Thalamic circuitry and thalamocortical synchrony. Phil Trans R Soc Lond 357:1659–1673Google Scholar
- Jones EG (2009) Synchrony in the interconnected circuitry of the thalamus and cerebral cortex. In: ND Schiff, S Laureys (eds) Disorders of Consciousness, vol 1157. Annals of the New York Academy of Sciences, New York, pp 10–23Google Scholar
- Kahana MJ, Seelig D, Madsen JR (2001) Theta returns. Curr Opin Neurobiol 11:739–744Google Scholar
- Klimesch W, Sauseng P, Hanslmayr S (2007) EEG alpha oscillations: the inhibition timing hypothesis. Brian Res Rev 53:63–88Google Scholar
- Laureys S, Goldman S, Phillips C, Van Bogaert P, Aerts J, Luxen A et al (1999) Impaired effective cortical connectivity in vegetative state: preliminary investigation using PET. Neuroimage 9:377–382Google Scholar
- Laureys S, Owen AM, Schiff N (2004) Brain function in coma, vegetative state, and related disorders. Lancet Neurol 3:537–546Google Scholar
- Laureys S (2005) Death, unconsciousness and the brain. Nat Rev Neurosci 6:899–909Google Scholar
- Lee G, Byram A, Stables C, Mizgalewicz A, Ribary U, Owen AM, Illes J (2012) A framework for assessing the clinical actionability of functional neuroimaging for disorders of consciousness. Int Neuroethics SocGoogle Scholar
- Levy DE, Sidtis JJ, Rottenberg DA, Jarden JO, Strother SC, Dhawan V et al (1987) Differences in cerebral blood flow and glucose utilization in vegetative versus locked-in patients. Ann Neurol 22:673–682Google Scholar
- Llinás R, Grace AA, Yarom Y (1991) In vitro neurons in mammalian cortical layer 4 exhibit intrinsic activity in the 10 to 50 Hz frequency range. Proc Natl Acad Sci USA 88:897–901Google Scholar
- Llinás R (1993) Is dyslexia a dyschronia? Ann NY Acad Sci 682:48–56Google Scholar
- Llinás R, Ribary U (1993) Coherent 40-Hz oscillation characterizes dream state in humans. Proc Natl Acad Sci USA 90:2078–2081Google Scholar
- Llinás R, Ribary U, Joliot M, Wang XJ (1994) Content and context in temporal thalamocortical binding. In: Buzsaki G, Llinás R, Singer W, Berthoz A, Christen Y (eds) Temporal coding in the brain. Springer, Heidelberg, pp 251–272Google Scholar
- Llinás R, Ribary U, Tallal P (1998a) Dyschronic language-based learning disability. In: VonEuler C, Lundberg I, Llinás R (eds) Basic mechanisms in cognition and language. Elsevier, New York, pp 101–108Google Scholar
- Llinás R, Ribary U, Contreras D, Pedroarena C (1998b) The neuronal basis for consciousness. Phil Trans R Soc Lond 353:1841–1849Google Scholar
- Llinás R, Ribary U, Jeanmonod D, Kronberg E, Mitra PP. (1999) Thalamo-cortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci USA 96:15222–15227Google Scholar
- Llinás R, Ribary U, Jeanmonod D, Cancro R, Kronberg E, Schulman JJ, Zonenshayn M, Magnin M, Morel A, Siegemund M (2001) Thalamocortical dysrhythmia I: functional and imaging aspects. Thal Rel Syst 1:237–244Google Scholar
- Llinás RR, Leznik E, Urbano FJ (2002) Temporal binding via cortical coincidence detection of specific and nonspecific thalamocortical inputs: a voltage-dependent dye-imaging study in mouse brain slices. Proc Natl Acad Sci USA 99:449–454Google Scholar
- Lou HC, Joensson M, Biermann-Ruben K, Schnitzler A, Ostergaard L, Kjaer TW, Gross J (2011) Recurrent activity in higher order, modality non-specific brain regions: A granger causality analysis of autobiographic memory retrieval. PLoS ONE 6:e22286Google Scholar
- Madler C, Keller I, Schwender D, Poeppel E (1991) Sensory information processing during general anaesthesia: effect of isoflurane on auditory evoked neuronal oscillations. Brit J Anaesthes 66:81–87Google Scholar
- Merzenich MM, Jenkins WM, Johnston P, Schreiner C, Miller SL, Tallal P (1996) Temporal processing deficits of language-learning impaired children ameliorated by training. Science 271:77–81Google Scholar
- Miller G (2010) Neuroscientists grapple with their field’s big questions. Science 330:164Google Scholar
- Mumford D (1991) On the computational architecture of the neocortex. The role of the thalamo-cortical loop. Biol Cyber 65:135–145Google Scholar
- Nagarajan S, Mahncke H, Salz T, Tallal P, Roberts T, Merzenich MM (1999) Cortical auditory signal processing in poor readers. Proc Natl Acad Sci USA 96:6483–6488Google Scholar
- Osipova D, Takashima A, Oostenveld R, Fernandez G, Maris E, Jensen O (2006) Theta and gamma oscillations predict encoding and retrieval of declarative memory. J Neurosci 26:7523–7531Google Scholar
- Owen AM, Hampshire A, Grahn JA, Stenton R, Dajani S, Burns AS et al (2010) Putting brain training to the test. Nature 465:775–778Google Scholar
- Palva JM, Monto S, Kulashekhar S, Palva S (2010) Neural synchrony reveals working memory networks and predicts individual memory capacity. Proc Natl Acad Sci USA 107:7580–7585Google Scholar
- Palva S, Palva JM (2007) New vistas for alpha-frequency band oscillations. Trends Neurosci 30:150–158Google Scholar
- Pantev C, Makeig S, Hoke M, Galambos R, Hampson S, Gallen C (1991) Human auditory evoked gamma-band magnetic fields. Proc Natl Acad Sci USA 88:8996–9000Google Scholar
- Pfurtscheller G, Schwarz G, Pfurtscheller B (1983) Computer assisted analysis of EEG, evoked potentials, EEG reactivity and heart rate variability in comatose patients. Elektroenzephalogr Elektromyogr Verwandte Geb 14:66–73Google Scholar
- Pfurtscheller G, Neuper C (1994) Event-related synchronization of mu rhythm in the EEG over the cortical hand area in man. Neurosci Lett 174:93–96Google Scholar
- Pfurtscheller G, Stancak A, Neuper C (1996) Event-related synchronization (ERS) in the alpha-band—an electrophysiological correlate of cortical idling: a review. Int J Psychophysiol 24:39–46Google Scholar
- Plum F, Schiff N, Ribary U, Llinás R (1998) Coordinated expression in chronically unconscious persons. Phil Trans R Soc Lond 353:1929–1933Google Scholar
- Purpura KP, Schiff ND (1997) The thalamic intralaminar nuclei: role in visual awareness. Neuroscientist 3:8–14Google Scholar
- Rennie CJ, Robinson PA, Wright JJ (2002) Unified neurophysiological model of EEG spectra and evoked potentials. Biol Cyber 86:457–471MATHGoogle Scholar
- Ribary U, Llinás R, Kluger A, Suk J, Ferris SH (1989) Neuropathological dynamics of magnetic, auditory, steady-state responses in Alzheimer’s disease. In: Williamson SJ, Hoke M, Stroink G, Kotani M (eds) Advances in biomagnetism. Plenum Press, New York, pp 311–314Google Scholar
- Ribary U, Ioannides AA, Singh KD, Hasson R, Bolton JPR, Lado F, Mogilner A, Llinás R (1991) Magnetic field tomography (MFT) of coherent thalamo-cortical 40-Hz oscillations in humans. Proc Natl Acad Sci USA 88:11037–11041Google Scholar
- Ribary U, Cappell J, Mogilner A, Hund M, Kronberg E, Llinás R (1999) Functional imaging of plastic changes in the human brain. Adv Neurol 81:49–56Google Scholar
- Ribary U, Joliot M, Miller SL, Kronberg E, Cappell J, Tallal P, Llinás R (2000) Cognitive temporal binding and its relation to 40 Hz activity in humans: alteration during dyslexia. In: Aine C, Okada Y, Stroink G, Swithenby S, Wood CC (eds) Biomag96. Springer, Berlin, pp 971–974Google Scholar
- Ribary U (2005) Dynamics of thalamo-cortical network oscillations and human perception. Progr Brain Res 150:127–142Google Scholar
- Ribary U, Ward LM (2014) Synchronization and functional connectivity dynamics across TC-CC-CT networks: Implications for clinical symptoms and consciousness. In: Mishara A (ed) Phenomenological neuropsychiatry: bridging the clinic with clinical neuroscience, SpringerGoogle Scholar
- Rudolf J, Ghaemi M, Haupt WF, Szelies B, Heiss WD (1999) Cerebral glucose metabolism in acute and persistent vegetative state. J Neurosurg Anesthesiol 11:17–24Google Scholar
- Salmelin R, Service E, Kiesila P, Uutela K, Salonen O (1996) Impaired visual word processing in dyslexia revealed with magnetoencephalography. Ann Neurol 40:157–162Google Scholar
- Salmelin R (2007) Clinical neurophysiology of language: the MEG approach. Clin Neurophysiol 118:237–254Google Scholar
- Sarnthein J, Morel A, von Stein A, Jeanmonod D (2003) Thalamic theta field potentials and EEG: high thalamocortical coherence in patients with neurogenic pain, epilepsy and movement disorders. Thal Rel Syst 2:231–238Google Scholar
- Sarnthein J, Jeanmonod D (2007) High thalamocortical coherence in patients with Parkinson’s disease. J Neurosci 27:124–131Google Scholar
- Sarnthein J, Jeanmonod D (2008) High thalamocortical coherence in patients with neurogenic pain. NeuroImage 39:1910–1917Google Scholar
- Sauseng P, Klimesch W, Doppelmayr M, Hanslmayr S, Schabus M, Gruber WR (2004) Theta coupling in the human electroencephalogram during a working memory task. Neurosci Lett 354:123–126Google Scholar
- Sauseng P, Klimesch W, Gruber WR, Birbaumer N (2008) Cross-frequency phase synchronization: a brain mechanism of memory matching and attention. Neuroimage 40:308–317Google Scholar
- Sauseng P, Griesmayr B, Freunberger R, Klimesch W (2010) Control mechanisms in working memory: a possible function of EEG theta oscillations. Neurosci Biobehav Rev 34:739–744Google Scholar
- Schiff ND, Ribary U, Plum F, Llinás R (1999) Words without mind. J. Cog. Neurosci. 11:650–656Google Scholar
- Schiff ND, Ribary U, Moreno DR, Beattie B, Kronberg E, Blasberg R, Giacino J, McCagg C, Fins JJ, Llinas R, Plum F (2002) Residual cerebral activity and behavioural fragments can remain in the persistently vegetative brain. Brain 125:1210–1234Google Scholar
- Schiff ND, Giacimo JT, Kalmar K, Victor JD, Baker K, Gerber M et al (2007) Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 448:600–603Google Scholar
- Schnitzler A, Gross J (2005) Normal and pathological oscillatory communication in the brain. Nat Rev Neurosci 6:285–296Google Scholar
- Schulman JJ, Ramirez RR, Zonenshayn M, Ribary U, Llinás R (2005) Thalamocortical dysrhythmia syndrome: MEG imaging of neuropathic pain. Thal Rel Syst 3:33–39Google Scholar
- Schulman JJ, Cancro R, Lowe S, Lu F, Walton KD, Llinás RR (2011) Imaging of thalamocortical dysrhythmia in neuropsychiatry. Front Hum Neurosci 5:1–11Google Scholar
- Sherman SM, Guillery RW (2006) Exploring the thalamus and its role in cortical function. MIT Press, Cambridge, MAGoogle Scholar
- Simos PG, Breier JI, Fletcher JM, Bergman E, Papanicolaou AC (2000) Cerebral mechanisms involved in word reading in dyslexic children: a magnetic source imaging approach. Cereb Cortex 10:809–816Google Scholar
- Snyder AC, Foxe JJ (2010) Anticipatory attentional suppression of visual features indexed by oscillatory alpha-band power increases: a high-density electrical mapping study. J Neurosci 30:4024–4032Google Scholar
- Sporns O, Tononi G, Kötter R (2005) The human connectome: a structural description of the human brain. PLoS Comput Biol 1:e42Google Scholar
- Steriade M, Llinas RR (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68:649–742Google Scholar
- Steriade M, Curro Dossi R, Pare D, Oakson G (1991) Fast oscillations (20–40 Hz) in thalamocortical systems and their potentiation by mesopontine cholinergic nuclei in the cat. Proc Natl Acad Sci USA 88:4396–4400Google Scholar
- Steriade M (1993) Central core modulation of spontaneous oscillations and sensory transmission in thalamocortical systems. Curr Opin Neurobiol 3:619–625Google Scholar
- Steriade M, Curró Dossi R, Contreras D (1993a) Electrophysiological properties of intralaminar thalamocortical cells discharging rhythmic ~40 Hz spike-bursts at ~1000 Hz during waking and rapid-eye movement sleep. Neurosci 56:1–9Google Scholar
- Steriade M, McCormick DA, Sejnowski TJ (1993b) Thalamocortical oscillations in the sleeping and aroused brain. Science 262:679–685Google Scholar
- Steriade M, Amzica F (1996) Intracortical and corticothalamic coherency of fast spontaneous oscillations. Proc Natl Acad Sci USA 93:2533–2538Google Scholar
- Supp et al (2007) Directed cortical information flow during human object recognition: analyzing induced EEG gamma-band responses in brain’s source space. PLoS ONE 2:e684Google Scholar
- Tallal P, Miller S, Fitch RH (1993) Neurobiological basis of speech: a case for the preeminence of temporal processing. Ann NY Acad Sci 682:27–47Google Scholar
- Tallal P, Miller SL, Bedi G, Byma G, Wang X, Nagarajan SS, Schreiner C, Jenkins WM, Merzenich MM (1996) Language comprehension in language-learning impaired children improved with acoustically modified speech. Science 271:81–84Google Scholar
- Tallal P (2004) Improving language and literacy is a matter of time. Nat Rev Neurosci 5:721–728Google Scholar
- Tallon-Baudry C, Bertrand O, Peronnet F, Pernier J (1998) Induced γ-band activity during the delay of a visual short-term memory task in humans. J Neurosci 18:4244–4254Google Scholar
- Tallon-Baudry C, Bertrand O (1999) Oscillatory gamma activity in humans and its role in object representation. Trends Cogn Sci 3:151–162Google Scholar
- Timmermann L, Gross J, Butz M, Kircheis G, Haussinger D, Schnitzler A (2003) Mini-asterixis in hepatic encephalopathy induced by pathologic thalamo-motor-cortical coupling. Neurology 61:689–692Google Scholar
- Tomassino C, Grana C, Lucignani G, Torri G, Ferrucio F (1995) Regional metabolism of comatose and vegetative state patients. J Neurosurg Anesthesiol 7:109–116Google Scholar
- Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration. Nature Rev Neurosci 2:229–239Google Scholar
- Victor JD, Drover JD, Conte MM, Schiff ND (2011) Mean-field modeling of thalamocortical dynamics, and a model-driven approach to EEG analysis. Proc Natl Acad Sci USA 108:15631–15638Google Scholar
- Volkmann J, Joliot M, Mogilner A, Ioannides AA, Lado F, Fazzini E, Ribary U, Llinás RR (1996) Central motor loop oscillations in Parkinsonian resting tremor revealed by magnetoencephalography. Neurology 46:1359–1370Google Scholar
- Wang HP, Spencer D, Fellous JM, Sejnowski TJ (2010) Synchrony of thalamocortical inputs maximizes cortical reliability. Science 328:106–109Google Scholar
- Ward LM (2003) Synchronous neural oscillations and cognitive processes. Trends Cog Sci 17:553–559Google Scholar
- Ward LM (2011) The thalamic dynamic core theory of conscious experience. Consc Cogn 20:464–486Google Scholar
- Wright JJ, Robinson PA, Rennie CJ, Gordon E, Bourke PD, Chapman CL et al (2001) Toward an integrated continuum model of cerebral dynamics: the cerebral rhythms, synchronous oscillation and cortical stability. BioSystems 63:71–88Google Scholar