Elsevier

NeuroImage

Volume 54, Issue 4, 14 February 2011, Pages 3040-3047
NeuroImage

Lost in thoughts: Neural markers of low alertness during mind wandering

https://doi.org/10.1016/j.neuroimage.2010.10.008Get rights and content

Abstract

During concentration tasks, spontaneous attention shifts occurs towards self-centered matters. Little is known about the brain oscillatory activity underlying these mental phenomena. We recorded 128-channels electroencephalographic activity from 12 subjects performing a breath-counting task. Subjects were instructed to press a button whenever, based on their introspective experience, they realized their attention had drifted away from the task. Theta (4–7 Hz) and delta (2–3.5 Hz) EEG activity increased during mind wandering whereas alpha (9–11 Hz) and beta (15–30 Hz) decreased. A passive auditory oddball protocol was presented to the subjects to test brain-evoked responses to perceptual stimuli during mind wandering. Mismatch negativity evoked at 100 ms after oddball stimuli onset decreased during mind wandering whereas the brain-evoked responses at 200 ms after stimuli onset increased. Spectral analyses and evoked related potential results suggest decreased alertness and sensory processing during mind wandering. To our knowledge, our experiment is one of the first neuro-imaging studies that relies purely on subjects' introspective judgment, and shows that such judgment may be used to contrast different brain activity patterns.

Research Highlights

►EEG correlates of mindwandering are similar to those of low alertness level. ►Decrease sensory processing during mind wandering. ►Introspection can be used to discriminate between different brain activity patterns.

Introduction

While reading books, most people have had the experience of finding their attention drifts towards self-centered matters. After some time (ranging from seconds to minutes), the readers realize they are mind wandering and bring their attention back to their reading. Mind wandering episodes thus correspond to the emergence of task-unrelated thoughts and affects that are attracting the attention away from the task at hand (Smallwood and Schooler, 2006, Mason et al., 2007). Not surprisingly, mind wandering episodes occur in our everyday life quite often—for instance, as soon as we perform a task and start realizing we are thinking about something else while doing it. One may think that avoiding these attention shifts is only a matter of concentration and willingness to carry out a mental task. Yet, after weeks, months, or years of training in tasks involving sustained concentration–such as focused meditation practice–subjects realize that these events seem to just happen, despite purposefully trying to avoid them—see Braboszcz et al. (2010) for a review of mind wandering during meditation practice.

The experience of mind wandering thus highlights the existence of moment to moment subjectively-attested changes of attentional focus from a task to non-task related thoughts and we believe that these changes would most likely be associated with different brain activity. Although it is a common phenomenon, and although its implication for consciousness research and the study of attentional processes is critical, the brain dynamics associated with mind wandering have not yet been studied directly.

Mind wandering has been associated with lower level of alertness and vigilance (Oken et al., 2006), a mental state with limited external information processing where attention is decoupled from the environment (Smallwood and Schooler, 2006). Supporting this hypothesis, human subjects exhibited decreased performance in rare-target oddball detection tasks during mind wandering (Giambra, 1995). In addition, the amplitude of the P300 event-related potential component was reduced during mind wandering, suggesting a decrease in attentional resources directed towards stimulus processing (Smallwood et al., 2008).

Although the brain dynamics associated with mind wandering have not been studied, a number of studies have investigated the brain dynamics associated with the resting state—an awake neutral state that is not associated with any specific cognitive task and that is prone to mind wandering (Gusnard and Raichle, 2001, Mazoyer et al., 2001). Studies coupling both EEG and fMRI found that the activity in different EEG frequency bands is spontaneously fluctuating at rest and can be correlated to spontaneous fluctuations of the BOLD signal (Laufs et al., 2006, Mantini et al., 2007). These fluctuations seem to underlie two distinct modes of cerebral activity: a mode dominated by fast frequency waves (12–30 Hz, beta) that may index higher degrees of task-related attention (Ray and Cole, 1985, Laufs et al., 2006), and a mode dominated by slow 3–7 Hz theta waves oscillations that has been linked to decreased sustained task-related attention and diverse stages of transition from wake to sleep (Loomis et al., 1937, Makeig and Inlow, 1993, Klimesch, 1999, Smit et al., 2005). Based on these results, we hypothesized that task-unrelated attentional drifts–i.e. mind wandering–would be associated with decreased vigilance and increased delta and theta power.

It has also been shown that brain evoked responses to external stimuli change with the degree of vigilance or sleep stage. For example, the negative brain evoked response to the sensory detection of a sudden change in the flux of auditory perception called mismatch negativity (Naatanen et al., 2007) is reduced during the early sleep stages and drowsiness (Lang et al., 1995, Winter et al., 1995). Since the mind wandering state should be associated with decreased vigilance, we expected to observe a decrease in the mismatch negativity amplitude in the mind-wandering state compared to the breath focus state.

We designed an experiment allowing subjects to experience mind wandering in conditions we believe to be as close as possible to the way they are experiencing it in their daily life. We chose a simple concentration task–a silent breath counting task–that only requires weak cognitive involvement from the subject, a characteristic known to favor the induction of mind wandering (Giambra, 1995, Cheyne et al., 2006). Simultaneously we presented frequent and rare pure-frequency auditory stimuli that subjects were instructed to ignore, and we used these stimuli to assess the evoked electrophysiological activity during the mind wandering and breath concentration states.

Section snippets

Participants

Sixteen volunteers from the laboratory staff and local universities (8 females and 8 males; age 19–36 years old, mean: 27 and standard deviation 5) gave written consent to participate to the experiment. Participants stated that they were not taking any substances or medications that could potentially affect their concentration nor having histories of major psychological disorders or any auditory deficiencies. Before starting the experiment, all participants read the instructions and had the

EEG activity time-locked to meta-consciousness events

The time frequency analysis of EEG data time-locked to meta-consciousness event–button press shows a significant influence of the subject's attentional state at all frequency bands from 2 to 25 Hz (Fig. 1). The most pronounced state-associated change on the EEG spectral activity occurs in the theta band (4–7 Hz) where absolute spectral power is significantly higher in the mind wandering state compared to the breath focus state. This effect is observed at all electrode sites and is larger over

Discussion

Our study aimed at characterizing the neural correlates of spontaneous and task-unrelated mental activity (i.e. mind wandering) and its effect on sensory processing. Compared to a breath-focus mental state, we have shown that mind wandering is characterized by a power amplitude increase in the theta frequency band and a power amplitude decrease in the alpha and beta frequency bands. We also showed that, during mind wandering, standard auditory stimuli induce a higher power in the theta and

Acknowledgments

This project was supported by a small grant from the Mind and Life foundation and by a PhD fellowship from the French CNRS governmental organization. We also wish to thank Dr. Emmanuel Barbeau for his suggestions on the manuscript.

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