Review
New insights into rhythmic brain activity from TMS–EEG studies

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There is renewed interest in the functional role of oscillatory brain activity in specific frequency bands, investigated in humans through electroencephalography (EEG) and magnetoencephalography (MEG) recordings. In parallel, there is a growing body of research on non-invasive direct stimulation of the human brain via repetitive (rhythmic) transcranial magnetic stimulation (TMS), and on those frequencies that have the strongest behavioural impact. There is, therefore, great potential in combining these two lines of research to foster knowledge on brain rhythms, in addition to potential therapeutic applications of rhythmic brain stimulation. Here, we review findings from this rapidly evolving field linking intrinsic brain oscillations to distinct sensory, motor and cognitive operations. The findings emphasize that brain rhythms are causally implicated in cognitive functions.

Section snippets

Basic organizing principles of brain rhythms: a brief introduction

Rhythmic activity is a fundamental property of neural elements and is organized in complex patterns depending on the state of the brain (e.g. sleep or awake) and on the task that is currently being executed. It can be recorded non-invasively from the scalp of human participants by electroencephalography (EEG) or magnetoencephalography (MEG) and many of the oscillatory components of EEG and MEG signals have been attributed a role in a variety of brain operations, including aspects of perception,

Analogies between EEG-, MEG- and TMS-research on rhythmic brain activity: added value of combining these techniques

There is renewed interest in ongoing oscillatory brain activity in the absence of any stimulus input or motor output as an index of the internal state of the brain, and linked to it, the extent to which features of this ongoing activity have predictive power for subsequent sensory experience or cognitive processes (e.g. see Ref. [13]). This interest in how the internal state of the brain shapes forthcoming perception and cognition transpires many fields in neuroscience (for a recent review see

Do specific frequencies reflect specific functions? α-oscillations and the regulation of cortical excitability versus inhibition

Recent EEG and MEG research has identified posterior α-oscillations, recorded before a visual event, as a predictor of the perceptual fate of the stimulus 8, 15, 16, 17. More specifically, the amplitude of α-oscillations over occipito-parietal sites is inversely related to perception of the forthcoming visual event 8, 15, 16, 17 (Figure 1a) with enhancement of α-power being observed under conditions requiring suppression of task-irrelevant visual information 32, 33, 34, 35. Based on these

Topography of brain-rhythms: are α-oscillations intrinsic to specific brain regions?

If specific frequencies have specific functions, they should show some degree of topographic specificity. Over the scalp, the cerebral α-rhythm is predominant over posterior and rolandic sites (over rolandic sites alongside β-oscillations). It is modulated by sensory input or motor output and therefore thought to reflect the spontaneous rhythm of sensory and sensory-motor areas. In line with this view, it has been found to originate in calcarine, occipito-parietal and somatosensory cortex 45, 46

Embedding in the cortical network: cortico-cortical interactions in the modulation of α-activity

If the α-rhythm reflects oscillations of neuronal elements close to signal input- and output-stages as reviewed earlier, it should be adjustable through top-down control from higher-order areas involved in attention and movement control and thus depend on the integrity of these areas. Here, the combined TMS–EEG approach has provided new information by virtue of TMS over higher-order areas and the study of EEG-changes at remote, anatomically connected sites (akin to analogous TMS-studies on

Rhythmic activity: epiphenomenal or causal manifestations of brain function?

Do brain rhythms have a causal functional role or merely represent epiphenomenal manifestations of the processes underlying perception, cognition and action? Historically, the α-rhythm was considered to reflect a cortical idling state, and its prominent suppression during visual and motor tasks [45] a valuable (but epiphenomenal) manifestation of cortical activation. Today, there is a growing body of evidence for α-enhancement beyond baseline (idling) levels, speaking against this

Rhythmic entrainment: the interest of biasing function in desired directions

Could the previously mentioned findings lead to new implementations of rhythmic TMS as a tool in therapy and neurorehabilitation? Several investigations indeed indicate that interacting with cortical activity, by means of rhythmic transcranial stimulation, can positively influence cognitive performance of patients affected by disorders such as aphasia, unilateral neglect or dementia [72]. The modification of cortical activity for an adequate period of time through the use of rhythmic

Concluding remarks

We have reviewed the evolving field of TMS–EEG research from which new insights into brain rhythms emerge. We have shown that the TMS–EEG combination is particularly promising and well suited to address several open questions on the generation and functional role of brain oscillations. This field has provided so far novel information mostly on the α-rhythm, namely on its role in perceptually relevant tuning of occipito-parietal areas, on its origin of generation in sensory-motor regions and

Acknowledgements

We thank Joachim Gross, Jan-Mathijs Schoffelen and three anonymous reviewers for comments, and Stefano Bonezzi for preparing Figure I in Box 1.

Glossary

Electroencephalography (EEG) and magnetoencephalography (MEG)
non-invasive electrophysiological recording techniques that sample ongoing electrical brain activity, which oscillates at various frequencies, through electrodes or sensors placed over the whole scalp.
Frequency bands used to classify brain oscillations
δ: delta (0.5–4Hz), θ: theta (4–8Hz), α: alpha (8–14Hz), β: beta (14–30Hz), γ: gamma (30–100Hz), fast (100–200Hz) and ultra fast (200–600Hz).
Transcranial magnetic stimulation (TMS) or

References (75)

  • T. Ergenoglu

    Alpha rhythm of the EEG modulates visual detection performance in humans

    Brain Res. Cogn. Brain Res.

    (2004)
  • M. Kobayashi et al.

    Transcranial magnetic stimulation in neurology

    Lancet Neurol.

    (2003)
  • A. Antal

    Comparatively weak after-effects of transcranial alternating current stimulation (tACS) on cortical excitability in humans

    Brain Stimulation

    (2008)
  • R. Kanai

    Frequency dependent electrical stimulation of visual cortex

    Curr. Biol.

    (2008)
  • P. Sauseng

    Spontaneous locally restricted EEG alpha activity determines cortical excitability in the motor cortex

    Neuropsychologia

    (2009)
  • G. Fuggetta

    Modulation of cortical oscillatory activities induced by varying single-pulse transcranial magnetic stimulation intensity over the left primary motor area: a combined EEG and TMS study

    Neuroimage

    (2005)
  • T.A. Rihs

    A bias for posterior alpha-band power suppression versus enhancement during shifting versus maintenance of spatial attention

    Neuroimage

    (2009)
  • J.F. Lepage

    EEG and neuronavigated single-pulse TMS in the study of the observation/execution matching system: are both techniques measuring the same process?

    J. Neurosci. Methods

    (2008)
  • M. Siegel

    Neuronal synchronization along the dorsal visual pathway reflects the focus of spatial attention

    Neuron

    (2008)
  • N. Yamagishi

    Attentional changes in pre-stimulus oscillatory activity within early visual cortex are predictive of human visual performance

    Brain Res.

    (2008)
  • M. Ploner

    Oscillatory activity reflects the excitability of the human somatosensory system

    Neuroimage

    (2006)
  • J.A. Pineda

    The functional significance of mu rhythms: translating “seeing” and “hearing” into “doing”

    Brain Res. Brain Res. Rev.

    (2005)
  • R. Hari

    Magnetoencephalographic cortical rhythms

    Int. J. Psychophysiol.

    (1997)
  • I. Manshanden

    Source localization of MEG sleep spindles and the relation to sources of alpha band rhythms

    Clin. Neurophysiol.

    (2002)
  • M. Steriade

    Basic mechanisms of cerebral rhythmic activities

    Electroencephalogr. Clin. Neurophysiol.

    (1990)
  • L.H. Strens

    The effects of subthreshold 1 Hz repetitive TMS on cortico-cortical and interhemispheric coherence

    Clin. Neurophysiol.

    (2002)
  • G. Thut

    Differential effects of low-frequency rTMS at the occipital pole on visual-induced alpha desynchronization and visual-evoked potentials

    Neuroimage

    (2003)
  • H. Jing et al.

    Observation of EEG coherence after repetitive transcranial magnetic stimulation

    Clin. Neurophysiol.

    (2000)
  • I. Griskova

    The effects of 10 Hz repetitive transcranial magnetic stimulation on resting EEG power spectrum in healthy subjects

    Neurosci. Lett.

    (2007)
  • W.H. Chen

    Low-frequency rTMS over lateral premotor cortex induces lasting changes in regional activation and functional coupling of cortical motor areas

    Clin. Neurophysiol.

    (2003)
  • M.F. Rushworth

    The left parietal and premotor cortices: motor attention and selection

    Neuroimage

    (2003)
  • D.J. Schutter

    High frequency repetitive transcranial magnetic over the medial cerebellum induces a shift in the prefrontal electroencephalography gamma spectrum: a pilot study in humans

    Neurosci. Lett.

    (2003)
  • W. Klimesch

    EEG alpha oscillations: the inhibition-timing hypothesis

    Brain Res. Rev.

    (2007)
  • D.J. Mitchell

    Frontal-midline theta from the perspective of hippocampal “theta”

    Prog. Neurobiol.

    (2008)
  • G.G. Knyazev

    Motivation, emotion, and their inhibitory control mirrored in brain oscillations

    Neurosci. Biobehav. Rev.

    (2007)
  • C. Miniussi

    Efficacy of repetitive transcranial magnetic stimulation/transcranial direct current stimulation in cognitive neurorehabilitation

    Brain Stimulation

    (2008)
  • G. Buzsáki

    Neuronal oscillations in cortical networks

    Science

    (2004)

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