Juergen Fell

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Unravelling inner experiences during resting state

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Unraveling inner experiences during resting state

OPINION ARTICLE
published: 29 July 2013
doi: 10.3389/fnhum.2013.00409
Unraveling inner experiences during resting state
Juergen Fell*
Cortical Oscillations Lab, Department of Epileptology, University of Bonn, Bonn, Germany
*Correspondence: juergen.fell@ukb.uni-bonn.de
Edited by:
Shuhei Yamaguchi, Shimane University, Japan
The investigation of resting state activ-
ity has become an extremely busy topic
in neurocognitive research. A recent
pubmed search revealed more than 2000
entries for the terms “resting state” AND
“fMRI.” Several putative clinical appli-
cations have been suggested, such as the
detection of early signs of Alzheimer’s
disease (e.g., Lustig et al., 2003) or risk
of developing psychosis (e.g., Jukuri
et al., 2013). However, the usefulness
of resting state data is hampered by
the fact, that up to now only very few
investigations have tried to elucidate
the mental processes occurring during
these experiments. Without knowledge of
these processes the purely physiologically
based findings of altered activations and
functional connectivities during resting
state lack a meaningful neurocognitive
interpretation.
Today, more and more knowledge
accumulates that our minds frequently
wander during daytime activities and cre-
ate thoughts which are not directly asso-
ciated with the situation at hand (e.g.,
Schooler et al., 2011). These thoughts are,
for instance, related to autobiographical
memories, future planning, social inter-
actions, and problem-solving. By exploit-
ing the technique of so-called experience
sampling, it has been demonstrated that
such mind wandering occupies up to 50%
of our daytime experiences (Killingsworth
and Gilbert, 2010). During times when
no task performance is required, such
mind wandering is even more prevalent.
Thus, resting state activity may veridically
be described as reflecting not an idling
state, but rather a “free thinking” state
(Everding, 2003). Accordingly, the patterns
of resting state activity, such as activations
of so-called default-mode regions, are
probably strongly related to the contents
of these thoughts (e.g., Mason et al., 2007).
Individual differences in the frequency and
contents of mind wanderingmay thus cor-
respond to discrepant patterns of resting
state activity and even may lead to sys-
tematic biases, for instance, caused by age
(e.g., Maillet and Rajah, 2013) or popula-
tion (e.g., Song and Wang, 2012) related
differences.
Recent studies have moreover shed
light on the more general question, which
kinds of inner experiences are prevalent
in humans, i.e., experiences that occur in
addition to the permanent sensory mon-
itoring of the external environment (e.g.,
Heavey and Hurlburt, 2007; Hurlburt,
2011). Based on the technique of so-
called descriptive experience sampling and
investigations of several hundreds of sub-
jects, a catalog of these inner experi-
ences has been suggested (Hurlburt and
Heavey, 2006). According to these stud-
ies (e.g., Heavey and Hurlburt, 2007) the
most common forms of inner experiences
are “inner seeing” (i.e., experiencing inner
images), “feelings,” “inner speech” (con-
stituting a certain kind of expression of
thought), “unsymbolized thinking” (i.e.,
thinking which is not conveyed in words,
images or other symbols) and “sensory
awareness” (i.e., paying attention to a par-
ticular sensory aspect of the environment).
With the exception of the latter category
(sensory awareness) these inner experi-
ences again are closely related to mind
wandering.
A particularly interesting outcome of
these studies is, that the distribution of
the categories of inner experiences has
an extremely high interindividual vari-
ability across individuals (e.g., Heavey
and Hurlburt, 2007)—even though we
humans experience the external environ-
ment in a rather similar fashion. There
are, for instance, subjects, who mainly
experience inner seeing, but very rarely
inner speech, whereas for other individ-
uals the opposite is true. Accordingly,
the individual patterns of resting state
activity may strongly depend on the cat-
egories of inner experiences, which are
prevalent in a certain subject. Alterations
of a subject’s resting state patterns as
compared to an average collective sam-
ple may thus be largely determined by
her/his individual characteristics of inner
experiences. This interindividual variabil-
ity, of course, seriously impairs the clin-
ical usefulness of such data, for instance,
in the detection of early Alzheimer’s
disease.
Following on from these considera-
tions, it is of paramount importance to
access the categories and contents of inner
experiences occurring during resting state
experiments. A fundamental methodolog-
ical difficulty complicating this endeavor is
that we are typically unaware of our mind
wandering and inner experiences. In other
words, we commonly lack metaawareness
of these experiences (Schooler, 2002). This
is the case even, for instance, when sub-
jects know their mind wandering during
a sustained attention task will be sam-
pled (Christoff et al., 2009). Interestingly,
mind wandering related activations are
stronger when subjects are unaware as
compared to when they are aware of
these experiences (Christoff et al., 2009).
Accordingly, the frequency distribution of
absent versus present meta-awareness rep-
resents another individual factor deter-
mining resting state patterns.
Related to the common lack of
metaawareness for inner experiences is
the prevailing inability to remember these
experiences (research addressing this
interrelation is yet also lacking), which
makes them difficult to reconstruct by later
inquisition. Actually, it has been suggested
to inquire about inner experiences during
resting state fMRI using a post-hoc ques-
tionnaire (Delamillieure et al., 2009). This
questionnaire comprised of categories
such as “visual imagery,” “inner language,”
“somatosensory awareness,” “inner musi-
cal experiences,” and “mental processing
of numbers,” as well as several items
addressing the contents of these experi-
ences. Based on this questionnaire, for
Frontiers in Human Neuroscience www.frontiersin.org July 2013 | Volume 7 | Article 409 | 1
HUMAN NEUROSCIENCE
Fell Inner experiences during resting state
instance, functional connectivity during
resting state has been analyzed depending
on the subject’s self-reported time spent
thinking in mental images and inner lan-
guage (Doucet et al., 2012). Although this
pioneering work is to be complimented,
it remains doubtful whether subjects are
indeed able to reliably identify their inner
experiences after a temporal delay of sev-
eral minutes. Other data suggest that the
outcome of such post-hoc inquiries in sub-
jects, which are naïve to the monitoring
of inner experiences, can generally not be
trusted and, for instance, strongly depends
on the subject’s preconceptions and beliefs
concerning their inner experiences (e.g.,
Schooler, 2002; Hurlburt, 2011).
A more reliable approach to access
inner experiences during resting state
experiments may be to use reports, which
are elicited ad-hoc via probe stimuli.
Compared to self-elicited reports, i.e.,
when subjects give an account whenever
they notice the occurrence of an inner
experience, probe-elicited reports offer
two major advantages. First, because of the
elusiveness of inner experiences, it is gen-
erally less difficult to describe these expe-
riences when prompted by a probe than
to provide self-elicited reports (Hurlburt,
2011; Schooler et al., 2011). Second, the
time intervals occupied by meta-cognitive
monitoring are more clearly defined in
the probe elicited condition (basically
the times between the probes and the
responses) compared to the self-elicited
condition. Since these time intervals in a
strict sense may not be labeled as task-
free “resting state,” they may later be
excluded from the evaluation of resting
state activity.
In its simplest form, for instance,
with this approach the most common
categories (e.g., inner seeing, feeling, inner
speech, other) and contents (e.g., past,
future, about the experiment, other) of
inner experiences would be sampled.
These inquiries could be implemented, for
example, by a pair of visually prompted
subsequent questions requiring button
presses with a beep tone accompany-
ing the first question (e.g., “What kind
of inner experience did you have just
before the beep”; “What was the content
of this experience related to?”). Subjects
should be allowed to give more than
one response to each question (e.g., to
report the experiences of inner seeing
plus inner speech). Repeated pairs of
questions should be separated by ran-
domized time intervals (e.g., 50–70 s).
Of course, the suggested method can
reveal only a coarse-grained picture of
inner experiences occurring during rest-
ing state and the few probe-elicited reports
have to be extrapolated for the complete
experiment.
For several disease populations, group
differences in resting state measures com-
pared to healthy controls have been
detected, which may help to understand
the pathophysiological bases of these dis-
eases (e.g., Lustig et al., 2003; Lee et al.,
2012; Jukuri et al., 2013). It has been
pointed out, however, that these findings
are of little use in individual diagnosis,
endophenotype development, prognosis
and treatment monitoring (e.g., Anderson
et al., 2011). From a practical standpoint, a
robust classification of single-subject rest-
ing state measures with regard to control
and disease collectives would be desirable,
which, in the ideal case, could back up
clinical decisions. To accomplish this goal,
it is necessary to investigate the reliability
of such single-subject classifications and
to reduce any major variance introduced
by thus far uncontrolled factors. Since it
has been demonstrated that resting state
measures considerably depend on individ-
ual inner experiences during these exper-
iments, for instance, on the estimated
amount of time spent thinking in mental
images or inner language (Doucet et al.,
2012), taking experience sampling based
variables into accountmay have the poten-
tial to substantially enhance the validity of
such classifications.
To conclude, similar to the exploita-
tion of first-person data to elucidate
the variability of neural responses dur-
ing cognitive experiments (Lutz et al.,
2002), accessing the categories and con-
tents of inner experiences via the suggested
basic procedure may enable researchers to
explain a large amount of interindivid-
ual variance in resting state data. Hence,
this approach may have the potential to
greatly improve the usefulness of resting
state experiments for clinical purposes.
ACKNOWLEDGMENTS
The author is grateful for helpful com-
ments from Nikolai Axmacher, Leila
Chaieb, Lorena Deuker, Christian Hoppe,
Hweeling Lee, Marcin Leszczynski,
Thomas Reber, and Yilmaz Sagik.
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Received: 27 June 2013; accepted: 11 July 2013;
published online: 29 July 2013.
Citation: Fell J (2013) Unraveling inner experiences
during resting state. Front. Hum. Neurosci. 7:409. doi:
10.3389/fnhum.2013.00409
Copyright © 2013 Fell. This is an open-access
article distributed under the terms of the Creative
Commons Attribution License, which permits use,
distribution and reproduction in other forums, pro-
vided the original authors and source are credited and
subject to any copyright notices concerning any third-
party graphics etc.
Frontiers in Human Neuroscience www.frontiersin.org July 2013 | Volume 7 | Article 409 | 3


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