Alpha activity reflects individual abilities to adapt to the environment

Abstract

Recent findings suggest that oscillatory alpha activity (7–13 Hz) is associated with functional inhibition of sensory regions by filtering incoming information. Accordingly the alpha power in visual regions varies in anticipation of upcoming, predictable stimuli which has consequences for visual processing and subsequent behavior. In covert spatial attention studies it has been demonstrated that performance correlates with the adaptation of alpha power in response to explicit spatial cueing. However it remains unknown whether such an adaptation also occurs in response to implicit statistical properties of a task. In a covert attention switching paradigm, we here show evidence that individuals differ on how they adapt to implicit statistical properties of the task. Subjects whose behavioral performance reflects the implicit change in switch trial likelihood show strong adjustment of anticipatory alpha power lateralization. Most importantly, the stronger the behavioral adjustment to the switch trial likelihood was, the stronger the adjustment of anticipatory posterior alpha lateralization. We conclude that anticipatory spatial attention is reflected in the distribution of posterior alpha band power which is predictive of individual detection performance in response to the implicit statistical properties of the task.

Introduction

When driving down a long and lonesome road, you can probably attend to the road while also talking to your passenger. As you head towards a crowded crossing, you will gradually focus your attention to the traffic and eventually stop talking to your passenger. After having passed the crossing you can allow yourself to again attend to your passenger.

This example illustrates our ability to gradually adjust our attentional resources according to the surrounding. This process is likely to be associated with a gradual engagement and disengagement of brain regions processing respectively relevant or irrelevant for the task at hand. We hypothesize that this redistribution of resources is partly reflected by a differential adjustment of neural oscillations in various brain regions. Recent findings suggest that oscillatory alpha activity (7–13 Hz) plays a role in the distribution of attention resources by functional inhibition of sensory regions. This allows for filtering incoming information (reviewed in Bonnefond and Jensen, 2012, Foxe and Snyder, 2011, Jensen and Mazaheri, 2010, Jensen et al., 2012, Klimesch, 1999, Klimesch, 2012). The main idea is that alpha activity increases in sensory regions associated with suppression of task-irrelevant information, while alpha activity decreases in regions processing the task-relevant information. For instance, recent studies on visual covert attention have demonstrated that alpha power decreases in the parieto-occipital regions contralateral to the anticipated stimuli whereas alpha activity increases relatively in ipsilateral parieto-occipital regions (Worden et al., 2000). In a visuo-spatial detection task, Thut et al. (2006) demonstrated that the degree of prestimulus hemispheric alpha lateralization correlated with faster target detections. Kelly et al. (2009) and Händel et al. (2011) showed that the strength of prestimulus alpha lateralization is predictive of target discriminability. These studies indicate that hemispheric alpha lateralization correlates with enhanced performance in spatial attention tasks. Finally, Romei et al. (2010) demonstrated that TMS can be applied to entrain alpha oscillations over the parietal cortex ipsi-lateral to the attended direction. Since this entrainment had positive consequences for performance in a spatial attention task, one can argue for a causal inhibitory role of the alpha oscillations.

Two recent studies provided strong evidence for alpha power being under top-down control by demonstrating that prestimulus hemispheric alpha lateralization is influenced by explicit manipulation of the reliability of the spatial cue (i.e. a cue indicating the visual hemifield to covertly attend to). Haegens et al. (2011) conducted a spatial somatosensory discrimination task in which subjects were explicitly informed about the cue reliability. They found that the reliability of the cue correlated with the prestimulus alpha power lateralization in sensorimotor regions. A related study was performed by Gould et al. (2011) in the visual domain. They found a linear increase in alpha lateralization in visual regions with cue reliability. Furthermore, subjects with a stronger alpha power decrease contralateral to the cue also showed a stronger behavioral cueing effect as reflected in faster reaction times. These two studies show that alpha power in both visual and somatosensory regions is modulated by expectations about the likelihood of external events.

In these paradigms attention biasing was manipulated using explicit cues. In real life, however, attention biasing is often modulated by statistical properties of events in the environment. The aim of our current study was to assess whether biases in the allocation of attention due to statistical properties in the environment are reflected in anticipatory alpha-band lateralization. In a visual covert attention paradigm subjects were instructed to detect a stream of targets occurring in one hemifield. However, they had to switch attention to the unattended hemifield when a stimulus change occurred in the unattended side. The likelihood of an attention-switch-stimulus (indicating an attention switch trial) increased with the number of trials following the previous switch; however, the subjects were not explicitly informed about this statistical property. We assessed the individual change in alpha lateralization and switch-trial detection rate with switch-trial likelihood. Our study provides evidence that subjects who adapted their behavior (i.e. switch trial detection rate) according to the statistical properties of the task (switch-trial likelihood) also were the ones who adjusted their hemispheric alpha lateralization accordingly.