Elsevier

NeuroImage

Volume 49, Issue 3, 1 February 2010, Pages 2238-2247
NeuroImage

Single-trial coupling of the gamma-band response and the corresponding BOLD signal

https://doi.org/10.1016/j.neuroimage.2009.10.058Get rights and content

Abstract

Oscillations in the gamma-band frequency range have been described to be more closely connected to hemodynamic changes as assessed with functional magnetic resonance imaging (fMRI) than other aspects of neuronal activity. In addition, gamma-band oscillations have attracted much interest during the last few years since they are thought to play a crucial role in many aspects of brain function related to perception and cognition. It was the aim of the present simultaneous EEG-fMRI study to identify brain regions specifically involved in the generation of the auditory gamma-band response (GBR) using single-trial coupling of EEG and fMRI. Ten healthy subjects participated in this study. Three different runs of an auditory choice reaction task with increasing difficulty were performed. Brain activity was recorded simultaneously with high density EEG (61 channels) and fMRI (1.5 T). BOLD correlates of the GBR have been predicted using the single-trial amplitude of the GBR.

Reaction times (p < 0.001), error rates (p < 0.05) and self-ratings of task difficulty and effort demands (p < 0.001) were related to the level of difficulty in the task. In addition, we found a significant influence of task difficulty on the amplitude of the GBR at Cz (p < 0.05). Using single-trial coupling of EEG and fMRI GBR-specific activations were found only in the auditory cortex, the thalamus and the anterior cingulate cortex (ACC) in the most difficult run. Single-trial coupling might be a useful method in order to increase our knowledge about the functional neuroanatomy of “neural ensembles” coupled by 40 Hz oscillations.

Introduction

Functional magnetic resonance imaging (fMRI) based on hemodynamic changes as assessed by the BOLD (blood oxygenation level dependent) signal is widely used today to indirectly investigate the neuronal activity of the brain. While the precise relationship between neuronal activity and the BOLD signal is not yet fully understood, several lines of evidence support an especially close coupling between high frequency oscillations in the gamma-band frequency range (> 30 Hz) and hemodynamic changes that can be assessed using the BOLD signal. The BOLD signal was shown to be most closely related to local field potentials in the gamma-band range using invasive measurements in animals (Logothetis et al., 2001). Corresponding evidence was also provided by studies in men demonstrating a closer relationship of the BOLD signal and gamma-band oscillations than between the BOLD signal and event-related-potentials (ERP) (Foucher et al., 2003). Accordingly, theoretical models were developed predicting that a shift in the frequency profile of the EEG to high frequency components should be correlated with an increase in the BOLD signal (Kilner et al., 2005).

Neuronal oscillations in the gamma-band frequency range have attracted much interest because they were suggested to play an important role in the linking of neurons into cell assemblies that code information in the brain (Singer, 1999). Experimental data obtained both in animals and in humans suggest that gamma-band oscillations are involved in perception and cognition (Herrmann et al., 2004a, Ribary, 2005). For example, several authors have described the early evoked gamma-band response (GBR) to be involved in attention (Tiitinen et al., 1993, Debener et al., 2003). Furthermore, an effect of task difficulty on the GBR amplitude was described (Mulert et al., 2007).

It is an important question, which neuronal substrates are responsible for the gamma-band oscillations measured on the scalp. The auditory GBR is at least partially generated in the auditory cortex (Pantev et al., 1991, Schadow et al., 2009) as a result of thalamo-cortical interactions (Ribary et al., 1991). However, since in cognitive tasks such as those mentioned above, it is well known that additional brain regions are involved, e.g. in the frontal lobe, one might wonder whether some of these regions might contribute as electrical generators to the GBR measured on the scalp or being functionally coupled by gamma-band oscillations. Using EEG source analysis, generators of the GBR in both the auditory cortex and the anterior cingulate cortex (ACC) have been described in more difficult conditions of a cognitive task (Mulert et al., 2007). However, EEG-based source imaging suffers from a limited spatial resolution in comparison to imaging techniques such as fMRI. In addition, it is difficult to investigate the role of sub-cortical structures such as the thalamus using scalp-EEG, although the thalamus is assumed to play a major role in the generation of brain rhythms (Steriade, 2006).

Recently, the integration of EEG and simultaneous fMRI was successfully introduced in order to combine the high temporal resolution of the EEG and the high spatial resolution of the fMRI (Ives et al., 1993, Lemieux et al., 1999, Goldman et al., 2000, Mulert et al., 2002b, Moosmann et al., 2003; for a review, see Ritter and Villringer, 2006, Mulert et al., 2008a). In particular, using single-trial coupling of EEG and fMRI, specific BOLD correlates of distinct neurophysiological components were demonstrated including the CNV (Nagai et al., 2004), N100 (Mulert et al., 2008b), P300 (Eichele et al., 2005, Benar et al., 2007) and ERN (Debener et al., 2005). Accordingly, it was the aim of the present study to use single-trial variations of the evoked gamma-band response to predict the GBR-related BOLD signal. We hypothesized to find GBR-related BOLD changes in brain regions that were described earlier using EEG source imaging during a difficult cognitive task (auditory cortex, ACC). In addition, we assumed to find GBR-related BOLD changes in the thalamus.

Section snippets

Subjects

Ten healthy subjects (4 men, 6 women, mean age = 22.8 years, range = 19–30 years, 9 right-hander, 1 left-hander) with no history of neurological and psychiatric disturbances or reduced hearing were recruited from an academic environment and participated in the study after giving their written informed consent. The research protocol was approved by the Ethics Committee for Human Experiments at the Ludwig-Maximilian University, Munich, Germany.

Paradigm

We used three different difficulty levels of an auditory

Reaction times

There was a significant condition effect for reaction times [F(2,18) = 34.7, p < 0.001] with longer reaction times in the more difficult runs. In the post hoc t-test analysis, reaction times were longer in DC than in IC [t(9) = 5.5, p < 0.001] and in EC [t(9) = 7.7, p < 0.001]. In addition, reaction times were longer in IC than in EC [t(9) = 3.75, p = 0.005], see Table 1.

Error rates

Error rates were very low in EC (0.5 %), higher in IC (3.4 %) and highest in DC (9.1 %). A significant condition effect was present [F

Discussion

This simultaneous EEG-fMRI study was intended to investigate the functional neuroanatomy of the auditory gamma-band response (GBR) using single-trial coupling of EEG and fMRI. We assumed both the auditory cortex and the thalamus to be involved in the generation of the GBR and aimed to clarify earlier reports of an involvement of the ACC. In accordance to our hypothesis, we found GBR-specific fMRI activations in the auditory cortex and the thalamus. In addition, we could also demonstrate

Acknowledgment

Part of this work was prepared in the context of Philip Hepp's dissertation at the Faculty of Medicine, Ludwig-Maximilians-University, Munich.

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