Impact Factor 3.566

The Frontiers in Neuroscience journal series is the 1st most cited in Neurosciences

Frontiers Commentary ARTICLE

Front. Neurosci., 01 May 2009 | https://doi.org/10.3389/neuro.01.011.2009

Cross-frequency coupling in parieto-frontal oscillatory networks during motor imagery revealed by magnetoencephalography

1
INSERM U821, Brain Dynamics and Cognition, Lyon, France
2
University Lyon 1, Lyon, France
A commentary on
Interactions between posterior gamma and frontal alpha/beta oscillations during imagined actions
by Floris P. de Lange, Ole Jensen, Markus Bauer and Ivan Toni
Movement execution is the end-product of multiple intricate neural processes including action selection and planning. Although the neural dynamics involved in such internal processes are generally investigated during the build-up to movement execution, the study of motor imagery provides an alternative window on the large-scale cortical dynamics mediating formation of motor plans. Indeed, motor imagery is associated with oscillatory power modulations widely distributed in sensorimotor cortical networks (Pfurtscheller and Neuper, 1997 ). However, the functional role of such oscillations and the putative inter-regional coupling within and across multiple frequency bands are still unresolved issues.
The study by de Lange et al. (2008) addresses these timely questions by using whole-head magnetoencephalography (MEG) to investigate oscillatory brain dynamics in subjects performing a motor imagery task. The participants were required to judge the handedness of drawings of a left hand or a right hand presented at various angles. Such a task elicits internal simulations of rotating one’s own hands. With frequency domain analysis and MEG source estimation, the authors evaluate modulations of various rhythmic components induced by the hand motor imagery task demands. While task-related suppressions in oscillatory power were found in the alpha (8–12 Hz) and beta (16–24 Hz) bands over occipito-parietal and precentral areas, significant increases in gamma-range (50–80 Hz) power were revealed over occipitoparietal cortex. Interestingly, when compared to right-hand motor imagery, left hand imagery was associated with stronger suppressions in contralateral motor areas. A further significant novelty of the study is the usage of cross-frequency amplitude correlation to specifically investigate oscillatory interactions between posterior parietal and frontal regions during formation of a motor plan. The authors therefore provide evidence for a significant long-range anti-correlation between parietal gamma power and frontal beta power at specific periods during mental simulation of action.
Viewed in the broader context of the previous work, the findings are of particular significance. Firstly, because the findings provide novel insights into the local and long-range oscillatory dynamics within the parieto-frontal network during motor imagery, and secondly, because of the important questions raised by the findings for future research. Acknowledging the fact that behavior arises from the integrative action of large-scale brain networks (Varela et al., 2001 ), earlier electrophysiological studies have assessed long-range interactions between distant structures of the human brain during different experimental paradigms by using various measures of coupling (e.g., Hummel and Gerloff, 2006 ; Jerbi et al., 2007 ; Lachaux et al., 1999 ; Schoffelen and Gross, 2009 ; Sehatpour et al., 2008 ; von Stein et al., 2000 ). These studies suggest that coupling between distinct neural structures at certain frequencies might provide an efficient mechanism for inter-regional communication in the brain (Fries, 2005 ). A growing body of research in recent years extends this view by pointing to cross-frequency coupling as a further putative mechanism mediating complex hierarchies of integrated neural ensembles at various scales (Jensen and Colgin, 2007 ). The study by de Lange et al. (2008) provides evidence for cross-frequency inter-areal amplitude coupling adding to a list of reported inter-frequency relations such as cross-frequency phase synchrony (Palva et al., 2005 ) or nested oscillations. The latter findings are observed as a locking between amplitude fluctuation of faster oscillations and the phase of slower oscillations, and have been observed during active tasks as well as in spontaneous brain activity (Bruns and Eckhorn, 2004 ; Canolty et al., 2006 ; Lakatos et al., 2008 ; Monto et al., 2008 ; Mormann et al., 2005 ; Osipova et al., 2008 ; Schack et al., 2002 ). Finally, in order to better understand the functional role of these mechanisms, future studies will have to monitor the putative relationship between interaction measures and behavioral performance. Investigating the alteration of cross-frequency coupling in pathology will also enhance the shift from descriptions of correlations to causal inference.

References

Bruns, A., and Eckhorn, R. (2004). Task-related coupling from high- to low-frequency signals among visual cortical areas in human subdural recordings. Int. J. Psychophysiol. 51, 97–116.
Canolty, R. T., Edwards, E., Dalal, S. S., Soltani, M., Nagarajan, S. S., Kirsch, H. E., Berger, M. S., Barbaro, N. M., and Knight, R. T. (2006). High gamma power is phase-locked to theta oscillations in human neocortex. Science 313, 1626–1628.
de Lange, F. P., Jensen, O., Bauer, M., and Toni, I. (2008). Interactions between posterior gamma and frontal alpha/beta oscillations during imagined actions. Front. Hum. Neurosci. 2, 7.
Fries, P. (2005). A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 9, 474–480.
Hummel, F. C., and Gerloff, C. (2006). Interregional long-range and short-range synchrony: a basis for complex sensorimotor processing. Prog. Brain Res. 159, 223–236.
Jensen, O., and Colgin, L. L. (2007). Cross-frequency coupling between neuronal oscillations. Trends Cogn. Sci. 11, 267–269.
Jerbi, K., Lachaux, J. P., N’Diaye, K., Pantazis, D., Leahy, R. M., Garnero, L., and Baillet, S. (2007). Coherent neural representation of hand speed in humans revealed by MEG imaging. Proc. Natl. Acad. Sci. U.S.A. 104, 7676–7681.
Lachaux, J. P., Rodriguez, E., Martinerie, J., and Varela, F. J. (1999). Measuring phase synchrony in brain signals. Hum. Brain Mapp. 8, 194–208.
Lakatos, P., Karmos, G., Mehta, A. D., Ulbert, I., and Schroeder, C. E. (2008). Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320, 110–113.
Monto, S., Palva, S., Voipio, J., and Palva, J. M. (2008). Very slow EEG fluctuations predict the dynamics of stimulus detection and oscillation amplitudes in humans. J. Neurosci. 28, 8268–8272.
Mormann, F., Fell, J., Axmacher, N., Weber, B., Lehnertz, K., Elger, C. E., and Fernández, G. (2005). Phase/amplitude reset and theta-gamma interaction in the human medial temporal lobe during a continuous word recognition memory task. Hippocampus 15, 890–900.
Osipova, D., Hermes, D., and Jensen, O. (2008). Gamma power is phase-locked to posterior alpha activity. PLoS ONE 3, e3990.
Palva, J. M., Palva, S., and Kaila, K. (2005). Phase synchrony among neuronal oscillations in the human cortex. J. Neurosci. 25, 3962–3972.
Pfurtscheller, G., and Neuper, C. (1997). Motor imagery activates primary sensorimotor area in humans. Neurosci. Lett. 239, 65–68.
Schack, B., Vath, N., Petsche, H., Geissler, H. G., and Möller, E. (2002). Phase-coupling of theta-gamma EEG rhythms during short-term memory processing. Int. J. Psychophysiol. 44, 143–163.
Schoffelen, J. M., and Gross, J. (2009). Source connectivity analysis with MEG and EEG. Hum Brain Mapp. (in press).
Sehatpour, P., Molholm, S., Schwartz, T. H., Mahoney, J R., Mehta, A. D., Javitt, D. C., Stanton, P. K., and Foxe, J. J. (2008). A human intracranial study of long-range oscillatory coherence across a frontal-occipital-hippocampal brain network during visual object processing. Proc. Natl. Acad. Sci. U.S.A. 105, 4399–4404.
Varela, F., Lachaux, J. P., Rodriguez, E., and Martinerie, J. (2001). The brainweb: phase synchronization and large-scale integration. Nat. Rev. Neurosci. 2, 229–239.
von Stein, A., Chiang, C., and König, P. (2000). Top-down processing mediated by interareal synchronization. Proc. Natl. Acad. Sci. U.S.A. 97, 14748–14753.
Citation:
Jerbi K and Bertrand O (2009). Cross-frequency coupling in parieto-frontal oscillatory networks during motor imagery revealed by magnetoencephalography. Front. Neurosci. 3,1: 3-4. doi: 10.3389/neuro.01.011.2009
Received:
03 March 2009;
 Published online:
01 May 2009.
Copyright:
© 2009 Jerbi and Bertrand. This is an open-access publication subject to an exclusive license agreement between the authors and the Frontiers Research Foundation, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.
*Correspondence:
Karim Jerbi, INSERM U821, Brain Dynamics and Cognition, Lyon, France; University Lyon 1, Lyon, France; e-mail: jerbi@lyon.inserm.fr