Prestimulus alpha power is related to the strength of stimulus representation

Abstract

Spatial attention can modulate behavioural performance and is associated with several electrophysiological markers. In this study, we used multivariate pattern analysis in electrophysiology data to investigate the effects of covert spatial attention on the quality of stimulus processing and its underlying mechanisms. Our results show that covert spatial attention led to (i) an anticipatory alpha power desynchronization; (ii) enhanced stimuli identity information. Moreover, we found that alpha power fluctuations in anticipation of the relevant stimuli boosted and prolonged the coding of stimulus identity.

Introduction

Attention is essential to select and process sensory stimuli in the environment. One of the main difficulties in studying attentional selection in humans is assessing the quality of processing of attended and ignored stimuli. Measures such as the amplitude of electrophysiological evoked responses (i.e., N1, P1) have been used as a reflection of this processing. However, a recent study has questioned this view since the amplitude of the evoked response was not correlated with a boost in target representation (Van Ede et al., 2018). Moreover, how well the unattended stimulus is processed is particularly hard to assess, given that participants are typically asked not to respond to these events.

One possibility to address this issue is to use methods which evaluate neural processing without necessarily requiring a behavioural response. Recent studies have relied on multivariate pattern analysis (MVPA) techniques to analyse EEG/MEG responses (King & Dehaene, 2014; Stokes et al., 2013; Wolff et al., 2015). In general, these methods are based on the theoretical basis that the MEG/EEG signal reflects coupled dipoles activity in the underlying neural circuitry. Although the specific dipole activity may not be identified, their summation would result in different patterns of activity across MEG/EEG sensors (King & Dehaene, 2014; Stokes et al., 2013; Wolff et al., 2015). These MVPA methods have been increasingly used to understand the effects of attention and its underlying mechanisms. Several studies have shown that spatial attention modulates stimulus representation in working memory (Bae & Luck, 2018; Mallett & Lewis-Peacock, 2018; Wolff et al., 2017) and sensory information input (Garcia et al., 2013). Moreover, temporal attention seems to enhance relevant sensory information input, creating a temporal protection window against distractors (Van Ede et al., 2018), and boosting its representational content.

Another pre-activating mechanism commonly described in the literature of spatial attention is the modulations in the spectral characteristics of the alpha (8–16 Hz) band (Van Diepen et al., 2019). This oscillatory activity is associated with cognitive functions such as visual attention (Foxe et al., 1998), working memory (Jensen et al., 2002) and cognitive load (Wilsch et al., 2014). For example, anticipatory lateralised desynchronization of alpha power is correlated with spatial expectations of relevant upcoming stimuli in a particular hemifield (Foxe et al., 1998; Gould et al., 2011). Studies suggest that alpha oscillations can play a role in information processing by suppressing the activity of particular neural populations involved with the irrelevant stimuli feature/spatial location processing, and by selecting the inhibition release of task-related neural populations (Klimesch, 2012; Lange et al., 2013). These anticipatory states reflected by the prestimulus power of low-frequency oscillations are also related to modulations in the amplitude of sensory event-related potentials (Iemi et al., 2019; Roberts et al., 2014). The general relationship between oscillatory activity and evoked responses is still not clear, and different explanations have been proposed on how these two relate (Hanslmayr et al., 2007; Iemi et al., 2019). In the specific case of anticipatory alpha power and evoked responses, there is evidence for both positive and negative correlations. Furthermore, the mechanisms by which alpha oscillations modulate perception are also unknown. Recent studies have challenged the view that alpha power modulates perceptual precision and have suggested that it increases perceptual (Iemi et al., 2017) or decision bias (Limbach & Corballis, 2016; Samaha et al., 2017).

In the present work, we combined time-frequency and multivariate pattern analyses to investigate: (1) how covert spatial attention modulates stimulus representation; (2) whether and how different EEG markers are modulated. We adapted previous tasks that presented targets of different modalities rhythmically (Lakatos et al., 2008, Lakatos et al., 2013) to investigate whether spatial attention induces generic anticipatory mechanisms. Combining both analyses allowed us to examine whether prestimulus alpha power boosts the quality and longevity of the classifier or if there is no relationship between anticipatory markers and subsequent classification.