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Edited by Robert Desimone, Massachusetts Institute of Technology, Cambridge, MA, and approved November 18, 2020 (received for review June 11, 2020)
Humans spend much of their lives engaging with their internal unrelated to an ongoing, typically externally oriented, task (8–10).
train of thoughts. Traditionally, research focused on whether or In the laboratory, subjects’ thoughts are often unrelated to the
not these thoughts are related to ongoing tasks, and has identified experimental task (9). Task-unrelated thought is also frequent in
reliable and distinct behavioral and neural correlates of task- everyday life (11), as when a student becomes distracted during a
unrelated and task-related thought. A recent theoretical frame- lecture or while driving.
work highlighted a different aspect of thinking—how it dynami- Recent theories are less task-centric and instead focus on the
cally moves between topics. However, the neural correlates of dynamics of mind wandering—that is, how internal trains of
such thought dynamics are unknown. The current study aimed thoughts unfold over time (12–17). In particular, the “dynamic
to determine the electrophysiological signatures of these dynam- framework” of spontaneous thought distinguishes three subtypes
ics by recording electroencephalogram (EEG) while participants within the train of thoughts: 1) deliberately constrained, 2) au-
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performed an attention task and periodically answered thought- tomatically constrained, and 3) freely moving thoughts (12, 14).
sampling questions about whether their thoughts were 1) task-
Constraints on the train of thoughts serve to focus internal at-
unrelated, 2) freely moving, 3) deliberately constrained, and 4)
tention on a topic for extended periods of time. For example,
automatically constrained. We examined three EEG measures across
deliberately constrained thoughts occur when a person actively
different time windows as a function of each thought type: stimulus-
directs her thoughts to goal-relevant information (e.g., when you
evoked P3 event-related potentials and non–stimulus-evoked alpha
power and variability. Parietal P3 was larger for task-related relative
contemplate your latest experiment). This type of constraint is
to task-unrelated thoughts, whereas frontal P3 was increased for implemented through cognitive control. Automatically constrained
deliberately constrained compared with unconstrained thoughts. thoughts focus on affectively or personally salient information that
Frontal electrodes showed enhanced alpha power for freely moving is difficult to disengage from (e.g., when you worry about your niece
thoughts relative to non-freely moving thoughts. Alpha-power var- who will have surgery). This type of constraint is automatic in
iability was increased for task-unrelated, freely moving, and uncon- nature and thought to operate largely outside of cognitive control.
strained thoughts. Our findings indicate distinct electrophysiological In contrast, freely moving thoughts occur when both of these
patterns associated with task-unrelated and dynamic thoughts, sug- constraints are weak, allowing the mind to wander with no over-
gesting these neural measures capture the heterogeneity of our arching purpose and direction (e.g., when your thoughts drift from a
ongoing thoughts. movie, to gardening, to dinner). Notably, the dynamic framework
thought in the context of mind wandering. This field has ex- This article is a PNAS Direct Submission.
panded at such a rapid pace that some have dubbed this the “era Published under the PNAS license.
of the wandering mind” (7). To date, the vast majority of mind- 1
To whom correspondence may be addressed. Email: julia.kam@ucalgary.ca.
wandering research has focused on the static content of individual This article contains supporting information online at https://www.pnas.org/lookup/suppl/
thoughts. In particular, mind-wandering studies have primarily doi:10.1073/pnas.2011796118/-/DCSupplemental.
focused on task-unrelated thought (8)—that is, thoughts that are Published January 18, 2021.
to which they co-occur. In accordance with the dynamic model Frontal P3 amplitudes were larger for deliberately constrained
which specifically contrasts task-unrelated thoughts with the other thoughts relative to thoughts that were not deliberately constrained
three dynamic thought types, we correlated the occurrence of task- (in the poststimulus window of 369 to 424 ms). Both of these results
unrelated thoughts with freely moving thoughts and deliberately remained significant after statistically controlling for other thought
and automatically constrained thoughts within individuals. These types, suggesting the observed patterns cannot be attributed to
intraindividual correlations were then tested at the group level other thought types. Details of these post hoc control analyses are
against 0 using the sign test, a nonparametric version of the single- reported in SI Appendix. The remaining two thought types did not
sample t test. Task-unrelated thoughts correlated positively with reveal significant conditional differences for either ERP compo-
freely moving thoughts (mean ± SE = 0.51 ± 0.05; Z = 4.29, P < nent. In addition to comparisons within each thought type, we
0.001) and automatically constrained thoughts (mean ± SE = implemented post hoc analyses to compare the ERP components
0.27 ± 0.04; Z = 4.03, P < 0.001), and negatively with deliberately between task-unrelated thought and the other three thought types.
constrained thoughts (mean ± SE = −0.26 ± 0.07; Z = −2.91,
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Details of these analyses are also reported in SI Appendix.
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P = 0.004).
Time-Frequency Power and Variability Results. In order to deter-
Behavioral Results. In order to identify the behavioral correlates
mine the neural correlates of thought types independent of
of each thought type, we examined mean accuracy, reaction time,
and reaction-time variability as a function of thought types. The
reaction time measures are shown in Fig. 2. Mean accuracy was A response time mean
high across all conditions (M = 0.95, SE = 0.012). There were no
significant differences in accuracy that survived the Bonferroni 600 * * *
correction between any of the thought types, likely due to the
ceiling effect in accuracy. 500
Mean reaction time across conditions was 500 ms (SE =
400
Time (ms)
(B) are shown separately for each thought type: A, automatically con-
relevant for the corresponding ERPs. ERP data analyses focused
strained; D, deliberately constrained; F, freely moving; NA, not automatically
on the frontal P3 and parietal P3 mean amplitude measures. We constrained; ND, not deliberately constrained; NF, not freely moving; TR,
statistically compared the mean amplitude for each ERP compo- task-related thought; TU, task-unrelated thought. Reaction-time variability
nent separately for each thought type. Parietal P3 amplitudes were was higher during task-unrelated thoughts, freely moving thoughts, and
larger for task-related thoughts compared with task-unrelated thoughts not automatically constrained. Error bars indicate SEM. *P < 0.05
thoughts (in the poststimulus time window of 367 to 432 ms). and **P < 0.0125.
1 1 1 1
0 0 0 0
-1 -1 -1 -1
-2 -2 -2 -2
-0.2 0 0.2 0.4 0.6 -0.2 0 0.2 0.4 0.6 -0.2 0 0.2 0.4 0.6 -0.2 0 0.2 0.4 0.6
Time (s) Time (s) Time (s) Time (s)
3 Pz TR 3 F 3 D 3 A
TU NF ND NA
2 2 2 2
1 1 1 1
0 0 0 0
-1 -1 -1 -1
-2 -2 -2 -2
-0.2 0 0.2 0.4 0.6 -0.2 0 0.2 0.4 0.6 -0.2 0 0.2 0.4 0.6 -0.2 0 0.2 0.4 0.6
Time (s) Time (s) Time (s) Time (s)
Fig. 3. Stimulus-evoked P3 event-related potentials. The ERP waveforms at frontal site Fz (Top) and parietal site Pz (Bottom) are shown separately for the
following thought types: (A) task-related thoughts, (B) freely moving thoughts, (C) deliberately constrained thoughts, and (D) automatically constrained
thoughts. Parietal P3 was reduced during task-unrelated thoughts, whereas frontal P3 was enhanced during deliberately constrained thoughts. Solid black
lines indicate the time points of significant conditional differences. Topographic map insets are shown for the P3 during these significant time windows. TR,
task-related; TU, task-unrelated; F, freely moving; NF, not freely moving; D, deliberately constrained; ND, not deliberately constrained; A, automatically
constrained; NA, not automatically constrained.
stimulus-evoked activity, we statistically examined spectral power alpha during task-unrelated thought using a traditional approach
in the alpha band between 600 and 1,800 ms poststimulus using with a priori electrode selection, instead of the data-driven ap-
cluster-based permutation tests. Fig. 4 shows the time-frequency proach of cluster-based permutation tests implemented on all
plots for the significant thought types, along with the alpha- electrodes. Specifically, we conducted permutation tests at the
power time series extracted from the cluster of significant elec- single-electrode level to examine conditional differences in posterior
trodes. Our analyses focused on alpha power given its role in alpha power. The aforementioned studies converged on maximal
internal attention and divergent thinking. There was a significant alpha power at midline posterior site Oz for task-unrelated thought
cluster around 1,100 to 1,350 ms over the frontal sites that relative to task-related thought (23, 25), where alpha power is also
showed greater alpha power during freely moving thoughts than maximal in our data (as shown in SI Appendix, Fig. S1). Accordingly,
during thoughts that were not freely moving (P = 0.023). This we conducted a permutation test to compare the alpha power at
effect did not survive the conservative Bonferroni correction for Oz in two time windows (600 to 1,200 and 1,200 to 1,800 ms).
multiple comparisons, but remained significant after statistically Posterior alpha power was increased during task-unrelated thought
controlling for other thought types. relative to task-related thought during the 1,200- to 1,800-ms time
There were no significant clusters over posterior sites that dif- window (P = 0.037). There were no differences in posterior alpha
ferentiated alpha power between task-related and task-unrelated during the 600- to 1,200-ms time window (P = 0.255).
thoughts. Given that enhanced posterior alpha power has been Next, we statistically examined variability in whole-brain alpha
consistently reported during internal attention (23, 25) and spon- activity across time and trials between 600 and 1,800 ms using
taneous brain activity at rest (26, 27), we implemented post hoc permutation tests. Fig. 5 illustrates alpha variability as a function of
analysis to directly test our a priori hypothesis of increased posterior thought types. All four thought types showed significant differences.
40 40
30 30
1
20 20
F
10 10 NF
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0 0
0 0.5 1 1.5 0 0.5 1 1.5 0 0.5 1 1.5
Time (ms) Time (ms) Time (ms)
Fig. 4. Stimulus-independent alpha power. Alpha power averaged across significant electrodes emerging from a cluster-based permutation test for freely
moving thought. Time-frequency representations of low-frequency power are shown (Left and Middle), with the location of the significant cluster of
electrodes and black box outlining time windows of significance. Mean alpha power (shading indicates SEM) for each condition (freely moving and not freely
moving) is displayed (Right), with the gray box highlighting the time window of significance. No significant clusters emerged for other thought types.
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increased stimulus-evoked frontal P3, relative to thought that dynamic characteristics of our thoughts may be directly reflected
lacked deliberate constraints. Our second set of results concerns in our electrophysiological measures.
stimulus-independent activity that was measured during a time In our study, task-unrelated thoughts reduced stimulus-evoked
window that is unlikely to be impacted by stimulus-evoked re- parietal P3. This is consistent with our prediction that task-
sponses. This allowed us to plausibly isolate electrophysiological unrelated thoughts would uniquely disrupt stimulus-evoked ac-
activity associated with a subject’s ongoing thoughts from task- tivity associated with task performance. This prediction flows from
relevant response. We observed that freely moving thought was the decoupling model, which proposes the attenuation of external
linked to greater intrinsic frontal alpha power than thoughts that processing is necessary for supporting task-unrelated thoughts
are not freely moving. We also observed increased variability in (33). In particular, task-unrelated thought recruits executive re-
intrinsic alpha power during task-unrelated thought, freely moving sources, which enables our disengagement from an external task
thought, and unconstrained thoughts. Taken together, our results via top–down control, resulting in the disruption of responses to
suggest that there are distinct neural signatures of task-unrelated external stimuli. Accordingly, our finding of a decreased parietal
and dynamic thoughts. P3 evoked by visual stimuli thus validates our self-reported mea-
Freely moving thought was associated with increased frontal sure of task-unrelated thought, and is consistent with previous
alpha power and alpha-power variability. Both measures were reports of a reduction in parietal P3 amplitude during task-
obtained during a time window unlikely to be impacted by external unrelated thoughts (21, 22, 34).
stimuli, which suggests that these measures reflect intrinsic activity Given that posterior alpha power has been shown to increase
associated with freely moving thoughts. Freely moving thought during cognitive states similar to task-unrelated thoughts, such as
showed increased variability in alpha power. This suggests that the attentional lapses (23), internally oriented attention (25), or rest
cognitive variability of freely moving thought parallels neural (26), we predicted an increase in posterior alpha power during
variability, particularly in the form of alpha-power fluctuations. task-unrelated thoughts. These past findings suggest that poste-
rior alpha not only reflects top–down inhibitory control of ex-
ternal inputs (35) as shown in traditional studies of selective
** ** * ** attention but also serves as an electrophysiological signature of
4 internally oriented task-unrelated thoughts. In our study, the
Alpha Power Variability
ability across the 600- to 1,800-ms time window is shown separately for each
of task-unrelated thoughts and freely moving thoughts, we ob-
thought type. Alpha-power variability was higher during task-unrelated
thoughts, freely moving thoughts, and unconstrained thoughts. TR, task-
served a number of differences between these two thought types.
related; TU, task-unrelated; F, freely moving; NF, not freely moving; D, de- For example, task-unrelated and freely moving thoughts occurred
liberately constrained; ND, not deliberately constrained; A, automatically at different rates (66 vs. 47%). Furthermore, our results revealed
constrained; NA, not automatically constrained. Error bars indicate SEM. different electrophysiological patterns between these two thought
*P < 0.05, and **P < 0.0125. types. Whereas task-unrelated thinking was primarily associated
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horizontal eye movements were recorded from electrodes above and below (8 to 14 Hz).
the right eye and two electrodes placed at the right and left outer canthi. To examine mean spectral power, we extracted alpha power across the
Data were amplified and digitized at 512 Hz. poststimulus-evoked activity window (600 to 1,800 ms) for all artifact-free
EEG data were bandpass-filtered between 1 and 50 Hz, and referenced and correct trials for each thought type. We used the cluster-based per-
offline to the average of the two mastoid electrodes. Independent compo- mutation test to determine whether alpha power differed within thought
nent analysis was used to correct for ocular and muscle artifacts. Data de- types and, if so, to depict the time course of these differences. This data-
composition was performed using the fastICA toolbox in EEGLAB, and driven approach has the advantage of not having to presume the region or
artifactual components were manually detected based on component time time window in which conditional differences may emerge. For each elec-
course, topography, and power spectral density. Electrodes with excessively trode, we averaged alpha power across trials yielding one time series per
noisy signals were interpolated from neighboring electrodes using spherical thought type. Each subject’s alpha-power time series for all electrodes were
spline interpolation (48). Continuous EEG data were segmented into 4,000- then submitted to a cluster-based permutation test to determine differences
ms epochs, beginning at 1,000 ms prior to stimulus onset. Each trial was between thought types.
visually inspected for remaining artifacts, which were removed from sub- To examine variability within participants, we focused on change over time
sequent analyses. Common average reference was then applied to the data and across trials. We extracted the relative change in alpha power across the
prior to analysis. EEG data preprocessing and analysis were performed using poststimulus-evoked activity window (600 to 1,800 ms) for all electrodes for
EEGLAB (49) and FieldTrip (50) within Matlab (MathWorks). each participant. In keeping with the cluster-based permutation tests that
considered all electrodes, we did not restrict our analyses to focal regions
EEG Data Quantification. and instead considered all electrodes. For each electrode, we assessed fluc-
ERP: Stimulus-evoked activity. For stimulus-evoked activity, we examined the tuations in spectral power over the designated time window by computing
P3 event-related potentials in a time window immediately following stim- the SD in alpha power across the time window for that electrode, yielding
ulus onset (as shown in Fig. 1). EEG signals were bandpass-filtered at 1 to 20 one variability value per trial. We then computed the SD of these values
Hz. Only artifact-free and correct trials were included in the analysis. These across trials. This variability across time and trial, averaged across electrodes,
trials were averaged separately within participants as a function of their was compared between thought types.
Automatically constrained Definition: Thoughts that are drawn to something and difficult to
disengage from, whether or not you’re actively thinking about
them.
Example: You might be thinking over and over again about a fight
you just had with your housemate.
1. M. E. Raichle et al., A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 14. Z. C. Irving, Mind-wandering is unguided attention: Accounting for the “purposeful”
676–682 (2001). wanderer. Philos. Stud. 173, 547–571 (2016).
2. H. T. Wang et al., Dimensions of experience: Exploring the heterogeneity of the 15. C. Sripada, “An exploration/exploitation tradeoff between mind wandering and task-
wandering mind. Psychol. Sci. 29, 56–71 (2018). directed thinking” in Oxford Handbook of Spontaneous Thought and Creativity,
3. M. G. Preti, T. A. Bolton, D. Van De Ville, The dynamic functional connectome: K. C. R. Fox, K. Christoff, Eds. (Oxford University Press, 2018), pp. 23–34.
State-of-the-art and perspectives. Neuroimage 160, 41–54 (2017). 16. K. Christoff, Undirected thought: Neural determinants and correlates. Brain Res.
4. J. Gonzalez-Castillo et al., The spatial structure of resting state connectivity stability 1428, 51–59 (2012).
on the scale of minutes. Front. Neurosci. 8, 138 (2014). 17. K. Christoff et al., The ethics of belief. Psychol. Bull. 4, 29–52 (2011).
5. M. L. Dixon et al., Interactions between the default network and dorsal attention 18. J. W. Y. Kam et al., Slow fluctuations in attentional control of sensory cortex. J. Cogn.
network vary across default subsystems, time, and cognitive states. Neuroimage 147, Neurosci. 23, 460–470 (2011).
632–649 (2017). 19. C. Braboszcz, A. Delorme, Lost in thoughts: Neural markers of low alertness during
6. A. Turnbull et al., The ebb and flow of attention: Between-subject variation in in- mind wandering. Neuroimage 54, 3040–3047 (2011).
trinsic connectivity and cognition associated with the dynamics of ongoing experi- 20. B. Baird, J. Smallwood, A. Lutz, J. W. Schooler, The decoupled mind: Mind-wandering
ence. Neuroimage 185, 286–299 (2019).
disrupts cortical phase-locking to perceptual events. J. Cogn. Neurosci. 26, 2596–2607
7. F. Callard, J. Smallwood, J. Golchert, D. S. Margulies, The era of the wandering mind?
(2014).
Twenty-first century research on self-generated mental activity. Front. Psychol. 4, 891
21. J. W. Y. Kam et al., Mind wandering and motor control: Off-task thinking disrupts the
(2013).
online adjustment of behavior. Front. Hum. Neurosci. 6, 329 (2012).
8. C. Mills, Q. Raffaelli, Z. C. Irving, D. Stan, K. Christoff, Is an off-task mind a freely-
22. J. Smallwood, E. Beach, J. W. Schooler, T. C. Handy, Going AWOL in the brain: Mind
moving mind? Examining the relationship between different dimensions of thought.
wandering reduces cortical analysis of external events. J. Cogn. Neurosci. 20, 458–469
Conscious. Cogn. 58, 20–33 (2018).
9. J. Smallwood, J. W. Schooler, The restless mind. Psychol. Bull. 132, 946–958 (2006). (2008).
10. J. Smallwood, J. W. Schooler, The science of mind wandering: Empirically navigating 23. R. G. O’Connell et al., Uncovering the neural signature of lapsing attention: Elec-
the stream of consciousness. Annu. Rev. Psychol. 66, 487–518 (2015). trophysiological signals predict errors up to 20 s before they occur. J. Neurosci. 29,
11. G. K. Smith, C. Mills, A. Paxton, K. Christoff, Mind-wandering rates fluctuate across 8604–8611 (2009).
Downloaded at Bolivia: PNAS Sponsored on January 21, 2021
the day: Evidence from an experience-sampling study. Cogn. Res. Princ. Implic. 3, 54 24. J. Xu, D. Friedman, J. Metcalfe, Attenuation of deep semantic processing during mind
(2018). wandering: An event-related potential study. Neuroreport 29, 380–384 (2018).
12. K. Christoff, Z. C. Irving, K. C. R. Fox, R. N. Spreng, J. R. Andrews-Hanna, Mind- 25. J. W. Y. Kam, A. K. Solbakk, T. Endestad, T. R. Meling, R. T. Knight, Lateral prefrontal
wandering as spontaneous thought: A dynamic framework. Nat. Rev. Neurosci. 17, cortex lesion impairs regulation of internally and externally directed attention.
718–731 (2016). Neuroimage 175, 91–99 (2018).
13. P. Seli et al., Mind-wandering as a natural kind: A family-resemblances view. Trends 26. H. Laufs et al., EEG-correlated fMRI of human alpha activity. Neuroimage 19,
Cogn. Sci. 22, 479–490 (2018). 1463–1476 (2003).
PSYCHOLOGICAL AND
iology 28, 240–244 (1991).
COGNITIVE SCIENCES
39. C. G. Lucas, S. Bridgers, T. L. Griffiths, A. Gopnik, When children are better (or at least 52. E. Maris, R. Oostenveld, Nonparametric statistical testing of EEG- and MEG-data.
more open-minded) learners than adults: Developmental differences in learning the J. Neurosci. Methods 164, 177–190 (2007).
forms of causal relationships. Cognition 131, 284–299 (2014). 53. J. Kam, 64-channel human scalp EEG from 24 subjects examining spontaneous
40. W. James, F. Burkhardt, F. Bowers, I. K. Skrupskelis, The Principles of Psychology thought using experience sampling. Collaborative Research in Computational Neu-
(Harvard University Press, Cambridge, MA, 1981). roscience. https://crcns.org/data-sets/methods/eeg-1. Deposited 31 December, 2020.
Downloaded at Bolivia: PNAS Sponsored on January 21, 2021