Role of Neuronal Synchrony in the Generation of Evoked EEG/MEG Responses

Abstract

Telenczuk B, Nikulin VV, Curio G. Role of neuronal synchrony in the generation of evoked EEG/MEG responses. J Neurophysiol 104: 3557-3567, 2010. First published October 13, 2010 doi:10.1152/jn.00138.2010. Evoked EEG/MEG responses are a primary real-time measure of perceptual and cognitive activity in the human brain, but their neuronal generator mechanisms are not yet fully understood. Arguments have been put forward in favor of either "phase-reset" of ongoing oscillations or "added-energy" models. Instead of advocating for one or the other model, here we show theoretically that the differentiation between these two generation mechanisms might not be possible if based solely on macroscopic EEG/ MEG recordings. Using mathematical modeling, we show that a simultaneous phase reset of multiple oscillating neuronal (microscopic) sources contributing to EEG/MEG can produce evoked responses in agreement with both, the "added-energy" and the "phasereset" model. We observe a smooth transition between the two models by just varying the strength of synchronization between the multiple microscopic sources. Consequently, because precise knowledge about the strength of microscopic ensemble synchronization is commonly not available in noninvasive EEG/MEG studies, they cannot, in principle, differentiate between the two mechanisms for macroscopicevoked responses.

Functional and effective connectivity in subthalamic local field potential recordings of patients with Parkinson’s disease

“…The present finding of an increased functional and effective connectivity after levodopa administration is not in contrast with previous studies demonstrating a decrease of oscillatory beta power in the ON compared to OFF condition (Brown et al, 2001;Priori et al, 2004;Brown and Williams, 2005;Ray et al, 2008;Ku¨hn et al, 2009) for the following considerations: An increased amplitude of beta oscillations in the OFF condition is likely to indicate that a large number of neurons are activated simultaneously, without a considerable phase jitter (temporal delays) such that the electric fields from individual neurons can sum up to produce a large amplitude of oscillations (Telenczuk et al, 2010). This in turn indicates that the delicate structure of neuronal interactions, displaying temporal delays typical for functional communication between the neurons, is rather substituted by indiscriminable simultaneous activations of these neuronal clusters.…”

Transcranial magnetic stimulation-induced global propagation of transient phase resetting associated with directional information flow

“…Previous studies argued that such phase modulations could be either related to additive evoked responses or phase resetting (Sauseng et al, 2007; Becker et al, 2008). Moreover, it is not clear whether the macroscopic phase resetting of EEG oscillations reflects the microscopic phase resetting or additive evoked responses at the single neuron level (Telenczuk et al, 2010). Therefore, it is necessary to examine the issues by combining experimental data at different spatial scales using several indices and mathematical modeling.…”

The neuromagnetic response to spoken sentences: Co-modulation of theta band amplitude and phase

“…On the contrary, additive activity may reflect not only additional or stronger neuronal activity but also the phase alignment of multiple theta oscillations arising in somewhat different locales that contribute to the composite ongoing theta oscillation. Such phase-resetting would increase the amplitude of the theta oscillation in the post-stimulus response (on average) by reducing cancellation effects associated with phase differences among the reset oscillations (Sauseng et al, 2007; Telenczuk et al, 2010). Differentiation of the possible sources of additive activity requires information on neuronal activity at a granularity that is not, in principle, accessible in MEG/EEG data, which reflect the composite activity of large neuronal populations (Telenczuk et al, 2010).…”

“…Such phase-resetting would increase the amplitude of the theta oscillation in the post-stimulus response (on average) by reducing cancellation effects associated with phase differences among the reset oscillations (Sauseng et al, 2007; Telenczuk et al, 2010). Differentiation of the possible sources of additive activity requires information on neuronal activity at a granularity that is not, in principle, accessible in MEG/EEG data, which reflect the composite activity of large neuronal populations (Telenczuk et al, 2010). However, more fine-grained views of neuronal activity in response to auditory stimuli obtained via intra-cortical electrodes situated in the primary auditory cortex of awake macaques also found robust theta-band power enhancement in local field potential response (Chandrasekaran et al, 2010) and provided evidence that inhibitory responses to tones involve mainly phase resetting in the delta, theta, and gamma bands, while excitatory responses involve both additive and phase reset activity (O’Connell et al, 2011).…”