Temporal dynamics of access to consciousness in the attentional blink

Abstract

Presentation of two targets in close temporal succession often results in an impairment of conscious perception for the second stimulus. Previous studies have identified several electrophysiological correlates for this so-called ‘attentional blink’. Components of the event-related potential (ERP) such as the N2 and the P3, but also oscillatory brain signals have been shown to distinguish between detected and missed stimuli, and thus, conscious perception. Here we investigate oscillatory responses that specifically relate to conscious stimulus processing together with potential ERP predictors. Our results show that successful target detection is associated with enhanced coherence in the low beta frequency range, but a decrease in alpha coherence before and during target presentation. In addition, we find an inverse relation between the P3 amplitudes associated with the first and second target. We conclude that the resources allocated to first and second target processing are directly mirrored by the P3 component and, moreover, that brain states before and during stimulus presentation, as reflected by oscillatory brain activity, strongly determine the access to consciousness. Thus, becoming aware of a stimulus seems to depend on the dynamic interaction between a number of widely distributed neural processes, rather than on the modulation of one single process or component.

Introduction

A central question in current neuroscience research involves the neural correlates of conscious perception (Engel and Singer, 2001, Ward, 2003). Although the concept itself is under heavy debate, researchers seem to agree that conscious perception of visual stimuli is a rather quick, fleeting phenomenon. Therefore, measures of electromagnetic brain activity with high temporal resolution have been proven useful in the scientific study of consciousness (Tallon-Baudry et al., 1997, Rodriguez et al., 1999, Koivisto and Revonsuo, 2003, Kranczioch et al., 2003, Eimer and Mazza, 2005, Sergent et al., 2005).

The brain mechanisms controlling whether physically identical information sometimes does and sometimes does not reach awareness remain poorly understood. In the case of the attentional blink (AB) paradigm, where two temporally close targets need to be processed, the second target often goes undetected. It has been suggested that this differentiation is due to a competition between neural processes devoted to the processing of the two targets reflected in the N2 and P3 waves of the event-related potential (ERP, Sergent et al., 2005). In line with this suggestion the amplitude of the P3 component evoked by the first target was found to be related to the size of the AB, that is the number of second targets that cannot be reported (McArthur et al., 1999, Shapiro et al., 2006). The P3 evoked by the second target on the other hand was shown to be reduced, if not absent, for undetected as compared to detected stimuli (Rolke et al., 2001, Kranczioch et al., 2003). Since detected task-relevant stimuli nearly always generate a P3 response, a prediction that can be drawn from these studies is that the competition for resources should be directly reflected in an interaction between first target and second target P3 amplitudes.

Recent theoretical (Fell et al., 2002, Dehaene et al., 2003) and empirical work has highlighted the role of synchronous oscillatory brain activity in the AB: differences between detected and undetected targets in long-range neural synchrony in the beta (Gross et al., 2004) and gamma (Nakatani et al., 2005) frequency ranges have been found to emerge even before target stimulus presentation. Although the functional role of different frequencies remains a matter of discussion, these findings clearly indicate that the state of oscillatory brain activity before and during stimulus presentation has an important influence on whether the second target in the AB paradigm is consciously perceived or not.

Here we tested the assumption of resource competition in the AB by analysing both ERPs and oscillatory brain activity. We predicted that brain states before and during stimulus presentation, as reflected by oscillatory brain activity, should determine the detection of a second target stimulus in the AB interval. Furthermore, the resources allocated to the first and second target processing should be directly mirrored by the P3 component, that is, the successful temporal management of resources should be reflected in larger P3 amplitudes for detected target stimuli.