Theta EEG oscillatory activity and auditory change detection

Abstract

The mismatch negativity is an electrophysiological marker of auditory change detection in the event-related brain potential and has been proposed to reflect an automatic comparison process between an incoming stimulus and the representation of prior items in a sequence. There is evidence for two main functional subcomponents comprising the MMN, generated by temporal and frontal brain areas, respectively. Using data obtained in an MMN paradigm, we performed time–frequency analysis to reveal the changes in oscillatory neural activity in the theta band. The results suggest that the frontal component of the MMN is brought about by an increase in theta power for the deviant trials and, possibly, by an additional contribution of theta phase alignment. By contrast, the temporal component of the MMN, best seen in recordings from mastoid electrodes, is generated by phase resetting of theta rhythm with no concomitant power modulation. Thus, frontal and temporal MMN components do not only differ with regard to their functional significance but also appear to be generated by distinct neurophysiological mechanisms.

Introduction

Delineating the neural basis of cognitive processes for a deeper understanding of the role of the brain's oscillatory activity is important. Indeed, several experimental results have pointed to a key role of neural oscillations. These include intracerebral electroencephalographical (iEEG) studies of the hippocampus in the rat (O'Keefe and Recce, 1993, Huxter et al., 2003) and cortical structures in monkeys (Fries et al., 2001) and humans (Rizzuto et al., 2003, Siapas et al., 2005, Shah et al., 2004). In normal human participants, non-invasive scalp EEG and MEG (magnetoencephalography) (e.g., Makeig et al., 2002, Düzel et al., 2005) have also been examined with regard to oscillatory activity. On the basis of such data, it has been suggested that modulations of oscillatory neural activity may underlie cognitive processes (Ward, 2003, Buzsáki and Draguhn, 2004, Buzsaki and Chrobak, 2005).

Also, a growing body of experimental evidence supports the view that EEG oscillations underlie event-related potential (ERP) generation (Sayers et al., 1974, Basar, 1999, Brandt et al., 1991, Makeig et al., 2002, Fuentemilla et al., 2006). Stimulus- or task-related brain responses interact trial-by-trial with EEG background activity in a non-stochastic manner, which leads to an ERP when individual trials are averaged (Penny et al., 2002, Kruglikov and Schiff, 2003, Makeig et al., 2004a). It has been demonstrated that these time-locked interactions manifest themselves in modulations of spectral power and/or phase-resetting of EEG rhythms (Makeig et al., 2002, David et al., 2005, Fuentemilla et al., 2006, Hanslmayr et al., 2007).

For example, test stimuli that need to be compared with other recently presented items lead to phase-resetting of theta (4–8 Hz) oscillations both, in animals (Adey and Walter, 1963, Givens, 1996) and humans (Klimesch, 1999, Rizzuto et al., 2003). Thus, these findings suggest that processing of memory-related stimulus events involves a phase reset or shift of ongoing oscillations (Rizzuto et al., 2003).

In the auditory domain, one of the most basic operations is the detection of sudden changes against a background of uniform stimuli. This operation, which may occur outside the focus of attention, requires a comparison of the deviant stimulus with a template derived from the previous stimulus series, i.e. a very basic memory process. The detection of a mismatch between the incoming deviant stimulus and the template is reflected in the averaged event-related potential (ERP) by the so-called mismatch negativity (MMN; Näätänen et al., 2001). MMN has been shown to be elicited by simple (e.g. duration, pitch) mismatches but also occurs for deviations in complex repetitive sound patterns (Näätänen and Winkler, 1999, Picton et al., 2000).

While there is strong evidence that brain oscillations underlie the generation of ERP components (Makeig et al., 2002, Gruber et al., 2005, Fuentemilla et al., 2006), their contributions to the MMN have not been properly studied. In the present work, we therefore analyzed the oscillatory basis of the MMN by using trial-by-trial time–frequency techniques. Given the reported involvement of theta phase-resetting in memory processes, we hypothesized that the MMN is similarly brought about – at least in part – by phase-resetting of the EEG theta rhythm.

In the present work, spectral phase-resetting and power modulation were measured through the Inter-Trial Coherence (ITC) and the Event-Related Spectral Perturbation (ERSP) modulation indices, respectively (Makeig et al., 2002). ITC and ERSP measures associated to MMN were studied through the differences between responses to deviant sounds and responses to repetitive standard sounds in an auditory paradigm comprising two different stimulus classes: trains of three consecutive identical tones preceded by long silent intervals (30 s) served as standard stimuli and trains of three sounds with a duration deviant in the third position served as deviant stimuli (P = 0.5). The long silent intertrain interval excludes the influence of the neighbouring stimuli trains. An MMN was expected for the third sound of deviant trains compared to the third sound of standard trains.