The resting state questionnaire: An introspective questionnaire for evaluation of inner experience...

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Brain Research Bulletin 81 (2010) 565–573 Contents lists available at ScienceDirect Brain Research Bulletin journal homepage: www.elsevier.com/locate/brainresbull Research report The resting state questionnaire: An introspective questionnaire for evaluation of inner experience during the conscious resting state Pascal Delamillieure a,b,, Gaëlle Doucet a , Bernard Mazoyer a,c , Marie-Renée Turbelin a,b , Nicolas Delcroix a , Emmanuel Mellet a , Laure Zago a , Fabrice Crivello a , Laurent Petit a , Nathalie Tzourio-Mazoyer a , Marc Joliot a a Centre d’Imagerie-Neurosciences et Applications aux Pathologies, UMR6232 CNRS, CEA, Universités de Caen et Paris Descartes, GIP-Cyceron, Bd Henri Becquerel, BP5229, 14074 Caen, France b Département Hospitalo-Universitaire de Psychiatrie, Centre Hospitalier et Universitaire de Caen, 14033 Caen cedex, France c Institut Universitaire de France et Centre Hospitalier et Universitaire de Caen, 14033 Caen cedex, France article info Article history: Received 7 October 2009 Received in revised form 27 November 2009 Accepted 29 November 2009 Available online 7 December 2009 Keywords: Consciousness Resting state Brain default mode Introspection Visual mental imagery Inner speech abstract We designed a semi-structured questionnaire for the introspective evaluation of inner experience of participants undergoing functional magnetic resonance imaging (fMRI) in the resting state. This resting state questionnaire (ReSQ) consists of 62 items organized by five main types of mental activity: visual mental imagery (IMAG); inner language (LANG), split into two subtypes, inner speech (SPEE) and auditory mental imagery (AUDI); somatosensory awareness (SOMA); inner musical experience (MUSI); and mental manipulation of numbers (NUMB). For IMAG and LANG, additional questions estimated association of such activities with ongoing learning, retrospective memories, or prospective thoughts. Using a 0–100% scale, the participant quantitatively rated the proportion of time spent in each mental activity during the resting state fMRI acquisition. A total of 180 healthy volunteers completed the ReSQ immediately after being scanned with fMRI while at rest. Of these, 66% exhibited dominance of a type of mental activity at rest (IMAG: 35%; LANG: 17%; SOMA: 7%; MUSI: 6%; NUMB: 1%). A majority of participants reported either retrospective memories (82%) or prospective thoughts (78%), with 58% of participants reporting both in at least one type of mental activity. Thoughts related to ongoing learning were low (37% of participants). The present results are consistent with those of previous studies investigating inner experience in a natural environment. In conclusion, we provide a robust and easy-to-implement tool for the exploration of mental activities during rest of healthy participants undergoing fMRI. This tool relies on normative data acquired from a 180-participant sample balanced for sex and handedness. © 2009 Elsevier Inc. All rights reserved. 1. Introduction A significant part of our wakeful brain activity is self-directed rather than goal-directed, consisting of periods of uncontrolled stream of thoughts, recollection of past episodes of our life, analysis of current inner sensations, thinking about problems, or planning for the future. This particular mind state, also referred to as “random episodic silent thinking” (REST) [1], “default mode” [34], or “con- scious rest” [4,28], has received increased attention in recent years because the corresponding brain state is both a physiological base- Corresponding author at: Centre d’Imagerie-Neurosciences et Applications aux Pathologies, UMR6232 CNRS, CEA, Universités de Caen et Paris Descartes, GIP- Cyceron, Bd Henri Becquerel, BP5229, 14074 Caen, France. Tel.: +33 0 2 31 47 01 10; fax: +33 0 2 31 47 02 22. E-mail address: [email protected] (P. Delamillieure). line [34] and a state of high neural activity and energy metabolism [38]. Several investigators have identified a large-scale cortical net- work with activity that appears to be maximal during REST and reduced during goal-directed cognitive tasks [4,28,30,31,37]. This network seems to support, at least in part, self-oriented activi- ties [1,4,7,12,19,28]. Modulation in brain default mode network activity due to life events, such as development [15,16], learning [27], aging [2,13], and neuropsychiatric diseases [36,39,43], has also been studied with the underlying hypothesis that the asso- ciated behavioral/cognitive changes or deficits may be related to such modulation. A major concern in all neuroimaging experiments addressing the resting state is the assessment of the participant’s mental con- tent while being imaged. First, the researcher must ensure that the participant has adequately followed instructions. Second, although some investigators have made efforts to perform online evalua- tion of the participant’s mental content while in the resting state 0361-9230/$ – see front matter © 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.brainresbull.2009.11.014

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Brain Research Bulletin 81 (2010) 565–573

Contents lists available at ScienceDirect

Brain Research Bulletin

journa l homepage: www.e lsev ier .com/ locate /bra inresbul l

esearch report

he resting state questionnaire: An introspective questionnaire for evaluation ofnner experience during the conscious resting state

ascal Delamillieurea,b,∗, Gaëlle Douceta, Bernard Mazoyera,c, Marie-Renée Turbelina,b, Nicolas Delcroixa,mmanuel Melleta, Laure Zagoa, Fabrice Crivelloa, Laurent Petit a, Nathalie Tzourio-Mazoyera, Marc Joliota

Centre d’Imagerie-Neurosciences et Applications aux Pathologies, UMR6232 CNRS, CEA, Universités de Caen et Paris Descartes, GIP-Cyceron,d Henri Becquerel, BP5229, 14074 Caen, FranceDépartement Hospitalo-Universitaire de Psychiatrie, Centre Hospitalier et Universitaire de Caen, 14033 Caen cedex, FranceInstitut Universitaire de France et Centre Hospitalier et Universitaire de Caen, 14033 Caen cedex, France

r t i c l e i n f o

rticle history:eceived 7 October 2009eceived in revised form7 November 2009ccepted 29 November 2009vailable online 7 December 2009

eywords:onsciousnessesting staterain default mode

a b s t r a c t

We designed a semi-structured questionnaire for the introspective evaluation of inner experience ofparticipants undergoing functional magnetic resonance imaging (fMRI) in the resting state. This restingstate questionnaire (ReSQ) consists of 62 items organized by five main types of mental activity: visualmental imagery (IMAG); inner language (LANG), split into two subtypes, inner speech (SPEE) and auditorymental imagery (AUDI); somatosensory awareness (SOMA); inner musical experience (MUSI); and mentalmanipulation of numbers (NUMB). For IMAG and LANG, additional questions estimated association ofsuch activities with ongoing learning, retrospective memories, or prospective thoughts. Using a 0–100%scale, the participant quantitatively rated the proportion of time spent in each mental activity during theresting state fMRI acquisition. A total of 180 healthy volunteers completed the ReSQ immediately afterbeing scanned with fMRI while at rest. Of these, 66% exhibited dominance of a type of mental activity at

ntrospectionisual mental imagery

nner speech

rest (IMAG: 35%; LANG: 17%; SOMA: 7%; MUSI: 6%; NUMB: 1%). A majority of participants reported eitherretrospective memories (82%) or prospective thoughts (78%), with 58% of participants reporting both inat least one type of mental activity. Thoughts related to ongoing learning were low (37% of participants).The present results are consistent with those of previous studies investigating inner experience in anatural environment. In conclusion, we provide a robust and easy-to-implement tool for the explorationof mental activities during rest of healthy participants undergoing fMRI. This tool relies on normative

-part

data acquired from a 180

. Introduction

A significant part of our wakeful brain activity is self-directedather than goal-directed, consisting of periods of uncontrolledtream of thoughts, recollection of past episodes of our life, analysis

f current inner sensations, thinking about problems, or planningor the future. This particular mind state, also referred to as “randompisodic silent thinking” (REST) [1], “default mode” [34], or “con-cious rest” [4,28], has received increased attention in recent yearsecause the corresponding brain state is both a physiological base-

∗ Corresponding author at: Centre d’Imagerie-Neurosciences et Applications auxathologies, UMR6232 CNRS, CEA, Universités de Caen et Paris Descartes, GIP-yceron, Bd Henri Becquerel, BP5229, 14074 Caen, France.el.: +33 0 2 31 47 01 10; fax: +33 0 2 31 47 02 22.

E-mail address: [email protected] (P. Delamillieure).

361-9230/$ – see front matter © 2009 Elsevier Inc. All rights reserved.oi:10.1016/j.brainresbull.2009.11.014

icipant sample balanced for sex and handedness.© 2009 Elsevier Inc. All rights reserved.

line [34] and a state of high neural activity and energy metabolism[38].

Several investigators have identified a large-scale cortical net-work with activity that appears to be maximal during REST andreduced during goal-directed cognitive tasks [4,28,30,31,37]. Thisnetwork seems to support, at least in part, self-oriented activi-ties [1,4,7,12,19,28]. Modulation in brain default mode networkactivity due to life events, such as development [15,16], learning[27], aging [2,13], and neuropsychiatric diseases [36,39,43], hasalso been studied with the underlying hypothesis that the asso-ciated behavioral/cognitive changes or deficits may be related tosuch modulation.

A major concern in all neuroimaging experiments addressing

the resting state is the assessment of the participant’s mental con-tent while being imaged. First, the researcher must ensure that theparticipant has adequately followed instructions. Second, althoughsome investigators have made efforts to perform online evalua-tion of the participant’s mental content while in the resting state

566 P. Delamillieure et al. / Brain Research Bulletin 81 (2010) 565–573

Table 1Nature of mental activities.

Mental activities Description Example

Visual mental imagery (IMAG) Seeing something in thought Seeing the new car bought this morning

Inner language (LANG):Inner Speech (SPEE) Thinking in words with your own voice

without overt productionSaying to oneself mentally, “I’ve got to buy the bread.”

Auditory mental imagery (AUDI) Imagining or recalling words, phrases,or sentences

Recalling conversation between self and a friend

Somatosensory awareness (SOMA) Paying attention to a particular sensoryaspect of the body

Being aware of breathing or cardiac rhythms

Inner musical experience (MUSI) Experiencing a melody and/or a Listening to music with or without lyrics

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rhythm in thoughtMental processing of numbers (NUMB) Arithmetic processing, c

estimation of the time toexam

8,31], avoiding interaction with the participant being scanned isecommended to prevent switching between a free mode and aoal-directed mode. As a consequence, assessment of participantental content during a functional magnetic resonance imaging

fMRI) study must rely on a posteriori introspective evaluation.We previously attempted to complete such an introspective

ost-fMRI evaluation in a group of participants who were scannedt rest with positron emission tomography (PET) [28]. This eval-ation was qualitative, however, and restricted to having thearticipants indicate whether their mental content during the rest-

ng state consisted mainly of mental imagery or inner language.owever, the conscious resting state is a mind state during whicharious types of thought, not necessarily limited to language andmagery, alternate. Here we report on a new questionnaire, theesting state questionnaire (ReSQ) that we designed to obtain auantitative and detailed evaluation of the mental content duringhe resting state. A total of 180 healthy adults, including women and

en and right- and left-handers, completed this questionnaire, andnglish and French versions are available upon request.

. Methods

.1. Participants and experimental context

The present study included 180 young (26.0 ± 6.6 years, mean ± SD), healthyolunteers. The participants had no history of any psychiatric, neurological or med-cal conditions. The sample was balanced for sex (91 women) and handedness (90eft-handers). All participants gave their informed written consent, and the localthical committee (CPP de Basse-Normandie, France) approved the study. Partici-ant handedness was assessed using the Edinburgh Handedness Inventory [33], andducational level was based on the number of school years starting at primary schoolEL, number of years at school and university) until the time of the examination.

The participants performed an 8-min resting state task during fMRI. This acqui-ition was preceded by a 15-min structural brain acquisition period during whichhe participants realized no task. Immediately prior to the fMRI acquisition, thearticipants were instructed to “keep their eyes closed, to relax, to refrain fromoving, to stay awake, and to let their thoughts come and go.” Within the 10 min

ollowing fMRI completion, participants started to complete the ReSQ. Filling out theuestionnaire lasted about 10 min under supervision of a psychologist or physicianreviously trained at the task and applying a standardized procedure. Participantsere told that fMRI scanning would be followed by a debriefing session but wereot informed about the nature of the post-experimental questionnaire.

.2. ReSQ structure and content

ReSQ has been designed as a semi-structured questionnaire for the introspectivevaluation of inner experience of participants undergoing fMRI while in the restingtate. ReSQ consists of 12 quotations and 62 items organized into five types (seeppendixBSupplementary information) or phases, as follows.

.2.1. Phase 1: task instruction–related questionsThe questionnaire started with three questions related to the correct realization

f the resting state task in the magnet. Participants were asked about being able toeep their eyes closed, to refrain from moving, and to stay alert during fMRI scanning.

g,nd of the

Thinking of numbers, calculating, or counting

2.2.2. Phase 2: profile of the mental activity (first quotation)Each participant was asked to give the proportion of time spent during the 8-

min fMRI exam on each of the following mental activities (Table 1): visual mentalimagery (IMAG), inner language (LANG), somatosensory awareness (SOMA), innermusical experience (MUSI), and mental manipulation of numbers (NUMB).

IMAG [25] is classically defined as “having thoughts in the shape of images,”such as picturing your new car in your mind. LANG covers two subtypes of activity:inner speech (SPEE) and auditory mental imagery (AUDI). Inner speech correspondsto imagined speech (talking to oneself with one’s voice) without overt produc-tion. During AUDI, the participants imagine or recall words, phrases, or sentencesas generated by an imagined voice [29], such as the recall of a radio broadcast.SOMA corresponds to feeling body sensations. MUSI experience can be describedas experiencing a melody and/or a rhythm in thought. Finally, mental processing ofnumbers corresponds to thinking of numbers, calculating (arithmetic processing),or counting.

Each participant rated the proportion of time spent in each activity during the8-min fMRI exam on a 0–100% scale so that the total score for the five types ofactivity had to equal 100%. This rating system allows definition of a “profile” ofeach participant’s mental activity at rest. Additionally, each participant was askedto report the ratio of inner speech and auditory mental imagery corresponding tothe language mental content.

2.2.3. Phase 3: individual itemsImmediately after quoting these proportions, the participant was asked to

describe the content of each type of mental activity. To do so, the experimenterfollowed a pre-defined decision tree questionnaire, unbeknownst to the participant.

For the IMAG, SPEE, and AUDI, the decision trees were similar and built touncover whether the thoughts were related to ongoing learning activities, memoryreminiscences, or prospective thoughts (thoughts about the future, such as plan-ning). At each leaf of the decision tree, the participant was asked if the reportedthought conveyed an emotional charge (positive/negative).

SOMA was investigated for the occurrence of outer or inner perceptions. Forouter perceptions, the participant was asked about thermoception (sensation of heator cold) and nociception (pain), whereas for the inner perceptions, participants wereasked about senses that were normally perceived within the body (e.g., heartbeatand breathing detection).

When reporting MUSI, the participant was asked if the experimental contexthad induced it (rhythmic noise of the fMRI sequence) or if it was independentlygenerated.

NUMB activity was documented in terms of level of complexity: count-ing/enumeration, simple calculation (addition/subtraction), or complex calculation(multiplication, division, . . .). In the case of counting, the participant was asked ifthe purpose was related to estimating the time (to the end of the exam).

Beyond these main items, each of the five mental activities was describedthrough more specific questions, covering the quality (e.g., “Were the mental imagesin color?”) and the nature of the thoughts (e.g., “Was the inner speech related toobject/place/people?”). These specific questions were included for further hypoth-esis testing in relation to functional data.

2.2.4. Phase 4: synthesis of the mental activityEach participant was asked if some thoughts recurred through the course of the

experiment and if any of these themes were related to ongoing learning.

2.2.5. Phase 5: profile of the mental activity (second quotation)Immediately upon ReSQ completion, this second quotation was included to

check whether the proportion of each mental activity would be modified in theparticipant’s report. The participant was asked to quote again the time spent duringthe 8-min fMRI exam on each of the five mental activities (as in phase 2).

P. Delamillieure et al. / Brain Research Bulletin 81 (2010) 565–573 567

Table 2Population description.

N Handednessa score ± SD Age years ± SD Educational level Yrs ± SD

Women, RH 47 92 ± 15 25.6 ± 4.8 15.8 ± 2.6Women, LH 44 −65 ± 36 24.9 ± 6.0 14.7 ± 2.6

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.3. ReSQ analysis

All data were rendered anonymous and stored in a database through a specifi-ally designed web-oriented interface. Plots and descriptive analyses were carriedut using JMP 7.0.2 (2007, SAS Institute Inc.).

.3.1. Descriptive statistics

.3.1.1. Task instruction-related questions. Occurrences and proportions of partic-pants reporting eye opening/drowsiness and movements were computed on the

hole sample (N = 180 participants).

.3.1.2. Profile and dominant mode of mental activity. First, a repeated-measuresNOVA was performed to compare the results from the first and the second quota-

ions for the proportion of time spent in each mental activity. This ANOVA did nothow any significant main effect of quotation repetition (p = 0.99). The mean abso-ute difference between quotations was 9%, with 14 participants having changedheir quotation by more than 10%. More precisely, one participant modified onenswer from 60% (maximal modification), two participants from 30%, four from0%, and seven from 15%. Each participant’s individual “profile” of mental activitiest rest was thus calculated as the mean of the responses to the two quotations. Usinghe rule proposed by Heavey and Hurlburt [20], participant profiles were then clas-ified according to the dominant mental activity mode. A participant was defineds dominant in a mental activity if more than 50% of the time focused on this activ-ty, with less than 50% on any of the others. Those participants who did not show aominant mode were aggregated into a non-dominant class.

For each mental activity occurrence, the proportion and the average of the timepent were computed. Additionally, we calculated the proportion of participants asfunction of the time spent in the mental activity (separated into six classes: no

ime spent, from 0% excluded to 20% included, from 20% excluded to 40% included,tc.).

.3.1.3. Individual items of the questionnaire. For each item of each type of mentalctivity, we report the occurrence (n, number of participants having answered tohe item) and the proportion ratio related to the number of participants who hadxperienced the type of mental activity (N).

We also calculated the occurrence and proportion of memory reminiscences,rospective thoughts, and ongoing learning (designated as mental processes) across

MAG, SPEE, and AUDI. Part of the data related to the SOMA, MUSI and NUMB mentalctivities are given in the result section: the occurrence of inner musical experi-nce initiated by fMRI noise (MUSI), the occurrence of simple arithmetic operationsnd counting (NUMB) and the occurrence of attention to heartbeat, breath, heatr cold sensation, and pain (SOMA). Results all the items of the ReSQ are given asppendixBSupplementary materials.

.3.1.4. Composite scores. Composite scores were created for items that were askedore than once, with the rule that the composite item is set to one if at least one of

he constituent items was answered positively. Such composite items were built for

ental processes (memory reminiscences, prospective thoughts, ongoing learning)

cross the mental activities (IMAG, SPEE, and AUDI).A global composite score of emotional charge was formulated on the basis of

ll of the emotional-related items in the IMAG, SPEE, and AUDI mental activities.omposite scores for the occurrence of emotion in each mental process (memoryeminiscences, prospective thoughts, ongoing learning) and each mental activity

able 3ental activity description: occurrence and proportion, the average time spent during

ominance. IMAG: visual mental imagery; LANG: inner language; SOMA: somatosensory a

Mental activity Number of participantsreporting the activity (% of 180)

Averagactivity

IMAG 171 (95) 40 ± 22LANG 167 (93) 30 ± 19SOMA 170 (94) 19 ± 16MUSI 92 (51) 23 ± 17NUMB 62 (34) 12 ± 10

a Excluding participants not reporting the activity.b Percentage of the 8 min of the experiment spent in one type of mental activity.

28.1 ± 7.0 16.0 ± 3.025.7 ± 7.9 14.0 ± 2.3

(IMAG, SPEE, and AUDI) were also computed. These scores were calculated regard-less of emotional valence.

2.3.2. Testing the effect of sex, age, educational level, and handedness2.3.2.1. Dominant mode. For each IMAG-dominant group, LANG-dominant group,and the non-dominant group, we performed ANOVA to test sex and handednesseffects and used regressions to test educational level and age effects.

2.3.2.2. Composite scores. For each mental process (memory reminiscences,prospective thoughts, ongoing learning) and global emotional valence compositescores, we performed ANCOVA with a global linear model (binomial error) to testsex, handedness, age, and educational level effects. When a significant effect wasfound at the p = 0.05 level, post-hoc t-tests were computed for each mental activity(IMAG, SPEE, and AUDI).

2.3.3. Specific testingRestricting the analysis to participants showing exclusively memory reminis-

cences or prospective thoughts, Chi square tests were used to check whether bothprocesses were preferentially associated with a particular mental activity (IMAG,SPEE, and AUDI).

3. Results

3.1. Participants

Table 2 shows handedness, age, and educational level for thesample. The sample average handedness scores were 88.6 ± 18.0(N = 90, mean ± SD) for the right-handers and −61.4 ± 38.6 (N = 90)for the left-handers. The sample mean age was 26.0 ± 6.6 years(N = 180, range = [18.1–51.3] years) without sex or handednesseffect (ANOVA). The mean educational level of the participantswas 15 ± 3 years (mean ± SD, range = [11–20] years), indicating anaverage of 3 years at a university, with left-handers having a signif-icantly lower educational level than right-handers (14.3 ± 2.4 yearsversus 15.9 ± 2.8 years, mean ± SD, p = 0.0001).

3.2. Descriptive statistics

3.2.1. Task instruction-related questionsA total of 84% (n = 152) of participants did not open their eyes

while the remaining participants reported an occasional blink. Of

the participants, 57% (n = 102) did not move, and the remainderreported small finger movements. For wakefulness, 86% (n = 154)of participants said they maintained a good level of arousal whilethe remainder reported occasional periods of drowsiness (30 s onaverage).

the experiment, and the occurrence and proportion of participants showing awareness; MUSI: inner musical experience; NUMB: mental processing of numbers.

e time spent in the reporteda %2 ± SD

Number of participants reporting atleast 50%b of the mental activity (%)

63 (35)31 (17)

12 (7)11 (6)1 (<1)

568 P. Delamillieure et al. / Brain Research Bulletin 81 (2010) 565–573

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ig. 1. Participant profile of mental activity classified according to the dominantercentage of the 8-min experiment spent in one activity. The lower right graph sh

nner language; SOMA: somatosensory awareness; MUSI: inner musical experience

.2.2. Profile and dominant mode of mental activityTable 3 presents a descriptive analysis of each mental activity

uotation. Among the 180 participants, IMAG, LANG, and SOMAere the most frequent (above 90%).

The classification of individual profiles showed that 66% of thearticipants (n = 118) exhibited a dominant mode of activity (Fig. 1).mong them, 35% reported IMAG as their dominant activity, fol-

owed by 17% LANG, 7% SOMA, 6% MUSI, and less than 1% NUMB.ig. 2 shows each dominant category mean profile. Among theemaining 62 participants, 13% (n = 23) had dual-mode profiles, 18%n = 33) a triple-mode profile, and 3% (n = 6) a flat profile consist-ng of 20% of the time spent in each of the five mental activities.

(above or equal to 50% of one mental activity). The ordinate corresponds to thearticipant profiles without a dominant mode. IMAG: visual mental imagery; LANG:B: mental processing of numbers.

Whether in the dual or triple-mode, IMAG and LANG were mostfrequent: 8% (n = 8) for the IMAG/LANG dual-mode profile and 12%(n = 22) for IMAG/LANG/another modality triple-mode profile.

The analysis of the time devoted to each mental activity (Fig. 3)confirmed the supremacy of both IMAG and LANG mental activities,which exhibited a maximal proportion in the 20–40% range (% ofthe 8 min of the acquisition) as opposed to the 0–20% range for the

SOMA.

The sub-partition analysis of the LANG mental activity demon-strated that SPEE was dominant over AUDI (Fig. 4). Note that 62participants reported only SPEE, while no participant reported onlyAUDI. On average, 78% of the time the participants devoted to LANG

P. Delamillieure et al. / Brain Research Bulletin 81 (2010) 565–573 569

Fig. 2. Average category profiles. Dominant IMAG activity (35% of participants, red),dominant LANG activity (17% of participants, cyan), dominant SOMA activity (7% ofparticipants, magenta), dominant MUSI activity (6% of participants, green), dom-inant NUMB (less than 1% of participants, brown), no dominant activity (34% ofpsct

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Fig. 4. Proportion of participants as a function of the time spent in inner speech(SPEE) and auditory mental imagery (AUDI) among the 167 participants having

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articipants, black). IMAG: visual mental imagery; LANG: inner language; SOMA:omatosensory awareness; MUSI: inner musical experience; NUMB: mental pro-essing of numbers. (For interpretation of the references to color in this figure legend,he reader is referred to the web version of the article.).

as spent in SPEE (SD = 25, N = 167) and only 22% in AUDI (SD = 25,= 167).

.2.3. Composite scoresAs Table 4 shows, the proportion of ongoing learning was lower

37%, n = 67) than memory reminiscences (82%, n = 148) or prospec-

ig. 3. Proportion of participants related to the time spent in each cognitive activity. Tharticipant in the specific cognitive activity. Error bar = 95% confidence interval.

reported some inner language (LANG). The abscissa range is from 0 (no time) to100 (all the time of LANG) spent by the participant in the specific cognitive activity.SPEE: inner speech; AUDI: auditory mental imagery.

tive thoughts (78%, n = 141). A total of 58% of participants (n = 105)reported both memory and prospective thoughts in at least onetype of activity.

Positive or negative emotions were reported at least oncein 78% of the participants (n = 141) with a higher propor-

tion for IMAG 74% (n = 125, N = 171) than for LANG, i.e.,62% for SPEE (n = 103, N = 167) and 61% for AUDI (n = 64,N = 105). The proportion for memory reminiscences with emo-tions (68%, n = 100, N = 148) was higher than those of prospective

e abscissa range is from 0 (no time) to 100 (8 min) with a bin of 20% spent by the

570 P. Delamillieure et al. / Brain Research Bulletin 81 (2010) 565–573

Table 4Proportion of the memory, prospective thought, ongoing learning for the visual mental imagery (IMAG, second column), inner speech (SPEE, third column), and auditorymental imagery (AUDI, fourth column). The composite score proportions for the three mental activities are shown in the fifth column. N: number of participants reportingthe mental activity.

IMAG (N = 171) %a SPEE (N = 167) %a AUDI (N = 105) %1 Composite score %b

Memory reminiscences 77 62 69 82Prospective thought 67 70 34 78Ongoing learning 27 28 15 37

a Percent of N.b Percent of 180 participants.

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ig. 5. Proportion of participants reporting only memory reminiscences (gray) or onlntervals).

houghts (52%, n = 74, N = 141) and ongoing learning (36%, n = 24,= 67).

.2.4. Individual items of the questionnaire

.2.4.1. Visual mental imagery, inner speech, auditory mentalmagery. Table 4 presents proportions for memory reminiscence,rospective thought, and ongoing learning occurrences. Memoryeminiscences and prospective thoughts were found in a major-ty of participants (above 60%) except for prospective thoughts inUDI (34%). Ongoing learning was found at an equivalent low level

n each mental activity (below 30%).

.2.4.2. Somatosensory awareness. Among the 170 participantseporting somatosensory awareness, the interoceptive sensationsoncerned preferentially attention to breathing (71%, n = 120,= 170) versus attention to heartbeat (26%, n = 44, N = 170). For the

xteroceptive sensations, 68% of the participants reported hot/coldensation (n = 116, N = 170) and 24% reported pain (n = 40, N = 170).

.2.4.3. Inner musical experience. A total of 92 participants reportedhis activity, and 50% of them (n = 46, N = 92) described it as inducedy the fMRI noise.

.2.4.4. Mental processing of numbers. Most of the 62 participantseporting this activity performed simple arithmetic operations32%, n = 20, N = 62) or counting (56%, n = 35, N = 62). For the count-ng activity, a majority reported using it for time estimation.

.3. Testing the effect of sex, age educational level, andandedness

.3.1. Dominant modeAssignment to the IMAG-dominant, LANG-dominant, or non-

ominant group showed no effect of sex (p = 0.18), age (p = 0.85),

ducational level (p = 0.10), or handedness (p = 0.46).

.3.2. Composite scoresWe observed a significant effect of educational level on

he occurrence of prospective thoughts (p = 0.0001). Prospective

pective thoughts (dark). (*p < 0.05; ***p < 0.0001; error bar shows the 95% confidence

thoughts were more frequent in people with higher educationallevels. Post-hoc t-tests showed a similar effect for each of the men-tal activities (IMAG: p < 0.01; SPEE: p < 0.001; AUDI: p < 0.004).

We observed both a sex effect (p = 0.045, male > female) and anage effect (p = 0.047, negative effect) on the occurrence of ongoinglearning. Men reported more mental activity related to ongoinglearning than women, while older participants reported less thanyounger participants. Post-hoc t-tests showed that in both cases,the IMAG mental activity reached significance (sex: p < 0.01; age:p < 0.02).

No such effects were observed with memory reminiscences oremotional valence.

3.4. Specific testing

Occurrence of memory reminiscences was higher when com-pared to prospective thoughts in both visual (IMAG, p < 0.05) andauditory (AUDI, p < 0.0001) mental imageries (Fig. 5). Occurrence ofprospective thoughts and memory reminiscences did not differ forSPEE.

4. Discussion

The development of neuroimaging techniques that allow corre-lation of subjective experience with a neuroanatomical substratehas triggered a new interest in the study of the neural bases ofinner experience, a phenomenon long considered to be beyond thereach of scientific investigations [20]. Consciousness access is thephenomenon by which information is accessible to the mind forreport. We can therefore access our thinking (we can introspect)and we can report accurately about our introspections [23,24].

Inner thoughts can be assessed by retrospective measures likethought listings or questionnaires [17] such as the one we devel-oped. Two non-retrospective methods for examination of thinking

have been proposed: the think-aloud [14] and the descriptive expe-rience sampling (DES) [22] methods. These methods have notyet been used in the context of cognitive neuroimaging. Anothermethod based on the triggered recall of ongoing thoughts has beenapplied during fMRI experiments [30]; however, the quantity of

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ecorded information was minimal and perturbation of the free-houghts state could not be controlled.

Here, we have elaborated the first introspective questionnaireo explore the mental activity of participants during the restingtate of an fMRI experiment. The aim was to create a tool to assessarticipant inner experience, one that is easy to use in practice.

The present questionnaire has its roots in a previous study of theonscious resting state in men [28] in which participants (N = 41)ere asked to describe the nature of their mental activities after

ET scanning. At the time, the experimental procedure consistedainly of an unstructured recall session with the participants. The

eed to refine the description of the mental activities required aore structured version of such a session. This structure leads to

educed inter-experimenter variability and thus permits applica-ion to a large number of participants with many experimenters.ur goal was also to provide a tool for the neuroimaging commu-ity, so filtering out experimenter interpretation was thus essential.he retrospective nature of this evaluation implies that the recallf some possibly forgotten mental activities (due to both the lengthf the experiment and the delay between the experiment and theuestionnaire) could be prompted in the participant. In this sense,he parallelism of our results with results provided by a more eco-ogical study, e.g., unstructured and randomly distributed duringhe day [20], can give an indication of the validity of our question-aire (see below). In addition to evaluating the possible impact ofhe questionnaire (such as the induction of false memory reminis-ences) on the participant’s report of mental activity, we comparedhe quantification of the mental activities at the beginning andt the end of the questionnaire. The results demonstrate that thisotential bias is minimal.

This tool, built as a decision tree, requires minimal practice forhe experimenter. The questions are straightforward, and partici-ants did not experience difficulties in understanding them. Theescription of each activity was built partly from the observedctivities in the 2001 study [28], such as memories, and partlyrom the literature addressing the resting state [6], such as prospec-ion and self-projection. The ongoing learning activity was includedecause of the possible modulation of the resting state activity dueo a prior cognitive state [42] or prior cognitive training [27]. A setf questions was added to explore the precision and vividness ofhe thoughts up to the emotional valence.

.1. Comparison to natural evaluation of inner thoughts

Our results are in agreement with the literature concerning thebservation of the inner experience of small samples of individu-ls outside the context of fMRI conditions [20]. As a matter of fact,e found that 66% of the participants exhibited a dominant mode

f thoughts during rest, and Heavey and Hurlburt [20] reported aomparable picture in which 73% of participants engaged in a singleype of activity. For three of the dominant activities addressed inoth studies, the time spent in each activity reported by Heavey andurlburt [20] matches our own measures. In their study, the partic-

pants reported inner seeing, inner speech, and sensory awarenessith occurrences of 34%, 26%, and 22%, respectively, whereas for

MAG, LANG, and SOMA, we reported occurrences of 40%, 30%,nd 19%, respectively. Note that our definition of LANG includesoth SPEE and AUDI, the latter a non-dominant phenomenon des-

gnated as inner hearing in the DES [22]. Our results showed thatPEE is the major constituent of language mental activity and thato participant reported only AUDI. One difference between our

esults and those of Heavey and Hurlburt [22] concerns the propor-ion of participants reporting mental activities. They observed that7%, 83%, and 70% of participants were engaged in the equivalentf IMAG, LANG, and SOMA, respectively [20], while our propor-ions are higher (95%, 93%, and 94% of participants, respectively),

h Bulletin 81 (2010) 565–573 571

especially for SOMA. Such differences can likely be ascribed tomethodology differences. In Heavey and Hurlburt’s study, a reportof a mental activity occupying less than 10% of the time was notpossible. Using the same threshold (considering only participantsreporting a mental activity above 10%), we found similar results totheirs with, respectively, 92%, 86%, and 75% for IMAG, LANG, andSOMA.

The two other dominant activities reported by Heaveyand Hurlburt—“unsymbolized thinking” and “feeling”—were notincluded in the present questionnaire. In the Heavey and Hurlburtstudy [20], method reports occurred randomly during the day andconsisted of snapshots of mental activities that were not neces-sarily structured, such as those on the fringe of consciousness [3].We can postulate that the length of our experiment and the delaybetween the experiment and the questionnaire precluded report ofsemi-conscious brief activities.

The “feeling,” defined as affective experiences in the DES [22],bears some similarity to our definition of “emotion.” While Heaveyand Hurlburt [22] described it as a phenomenon (corresponding toour mental activity), in our questionnaire, it was given in relation tomental processes. Only through the composite score of emotionalvalence we can compare the proportion of emotion between ourstudy and that of Heavey and Hurlburt’s. These proportions weresimilar (83%, Heavey and Hurlburt, 78% present study), confirmingthe importance of affect in the generation of inner thoughts.

The greater occurrence and time spent in IMAG over othermental activities confirms our previous results [28] and those ofHeavey and Hurlburt [20]. However, its classification as a dominantmodality emphasized this prevalence, as we show that the propor-tion of participants predominantly engaged in this activity reachedmore than twice the proportion of participants engaged in a pre-dominantly language-related activity. Moreover, images reportedmost of the time by these participants were vivid and colored (seeAppendixBSupplementary materials), as previously observed byKosslyn et al. [26] and Mellet et al. [32]. This activity seems thus tobe a core of mental processing during rest. Its predominance couldbe related to its early organization in the course of development, asinner mental imagery ability is likely to be operational before innerlanguage-related activity.

As for language mental activity, participants spent more timein SPEE than in AUDI. This result is in line with those of the DES[20,22] in which this latter activity, designated “inner hearing,” wasnot considered as a dominant feature. According to Baars [3], overtspeech takes up about one-tenth of our daily awake time, whereasinner speech appears to go on all the time (e.g., we talk to ourselvesduring dreams). In fact, we devote most of our spontaneous innerspeech to actual preoccupations [3].

SOMA was also a frequent report of the participants. However,this activity was rarely the dominant feature of the mental activ-ity. This result is consistent with that of Tracy et al. [41], whohypothesized that throughout periods of wakefulness, participantsare inundated with sensory signals originating both internally andexternally. Indeed, in their study, they noted that “the subjectspaid constant attention to internal pain, visceral or somatic signals(aches, temperature, heartbeat, breathing, . . .)”. These authors sug-gested that this type of attention may be critical to early detectionand early intervention of significant health risks (e.g., heart attack)[41].

MUSI was reported by 92 participants; half of them reportedthat such thoughts were related to the noise of the MRI machines.Their musical thoughts were thus externally driven, and this activ-

ity was at least partly context dependent and cannot be generalized.Seashore (1919) (in Brodsky et al. [5]) proposed the idea that amusical mind is characterized by its ability to “think in music,” andBrodsky et al. [5] commented that it seems likely that this abilityis particularly linked to expertise in music. In the DES [22], music

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xperience without lyrics was not included in the 16 basic phenom-na, and “lyric” was categorized as inner hearing, a non-dominanthenomenon [22]. Finally, it has been proposed that during audi-ory and music imagery, the inner voice supplies a kinesthetictimulus that acts as raw material via some association [5]. In ourample, only five of the 11 MUSI-dominant participants reportedractice in music, with a diverse degree of skills (none were profes-ional musicians). Further work is certainly needed to investigatehe specificity of music mental activity.

Concerning the 62 participants who reported mental processingf numbers, it is worth noticing that a majority relied on this typef activity for time estimation. As in the musical experience, thisctivity can thus be partly ascribed to an external cause, the require-ent to stay immobile for a substantial length of time. NUMB was

ot reported in the DES [22].According to Heavey and Hurlburt [20], differences in partici-

ant reporting style cannot explain the differences in frequenciesf report of each mental activity (i.e., our proportion of timepent); we confirm this observation with our similar proportionssing a different method and in a totally different environment.he characteristics of inner experience are probably related tohe characteristics of the personality and the functioning of thearticipants [20]. Note that such hypotheses constitute the basisf Neuro-Linguistic Programming, a model of interpersonal com-unication concerned with the relationship between successful

atterns of behavior and the subjective experiences (patterns ofhought) underlying them, with vision, audition, and kinesthesiaonsidered as the thinking subsets of our senses and constitutinghe building blocks of thoughts [40].

.2. Added knowledge to the mental content during the restingtate

We observed that the participants reported that their sponta-eous streams of thought was largely self-involved, i.e., dwellingn significant past events and attending to plans for the future. Iteems likely that the mode of mental activity depends on the per-onality of the participants and on their current concerns. Thesebservations are consistent with models proposed by Buckner andaroll [6] and Baars [3]. We have already reported observing theccurrence of memory reminiscences in both SPEE and IMAG [28],ut the present study adds knowledge concerning the prospectivehoughts that appeared at an equivalent level in the sample. Fur-hermore, we observed that 58% of the participants reported both

emory reminiscences and prospective thoughts in at least one ofhe mental activities. This result is highly consistent with the facthat imagining the future and remembering the past depend on

uch of the same neural machinery [35].Conway et al. [10] proposed that visual mental imagery has sev-

ral different functions: first, it is a sort of “language” of goals; andecond, it is a type of mental representation specialized for rep-esenting information about goals relating to the future or goalsnfluencing the past. When an image or a set of images is in mind,mportant goal information becomes available and may influenceurrent processing. Compared to sentences, image descriptions areore likely to take a form that resembles personal memories, to

escribe a specific event, including more personal involvement, ando describe sensation [21]. It has been argued that autobiographicalpisodic memories are largely stored in the form of images, includ-ng associated emotions [11]. In line with those theories, we foundpredominance of memories compared to prospection in the visual

ental imagery.The AUDI modality showed the same preferential support for

emories (compared to planning) as the IMAG modality. How-ver, occurrence and time spent in this mental modality were belowhose for IMAG and SPEE. Such an outcome is in line with the work

h Bulletin 81 (2010) 565–573

of Greenberg and Rubin [18], who found that auditory imagerywas not associated with global autobiographical amnesia, its roleremaining to be elucidated.

SPEE is used for instructional, preparatory, affective purposes,and planning [9]. Indeed, during SPEE, the occurrence of prospec-tive thoughts was above the occurrence of retrospective memories,though this comparison did not reach a significant threshold. Inter-estingly, our study reveals a positive effect of educational level onthe occurrence of prospective thoughts. Because our sample of edu-cational level is uniform and between 11 and 20 years, this resultapplies only for a post-graduate population. To our knowledge,there is no current comparable reference in the literature, and thispoint thus requires further investigation.

To summarize, our results show an association between thepresence of mental activity of visual imagery type and episodicmemory [18] and suggest that inner speech could be more special-ized for prospective thoughts. Concerning emotional introspection,Holmes et al. [21] showed that mental imagery is more likely toelicit emotion than verbal processing; indeed, our results showedsuch a tendency. We also found a larger proportion of emotion asso-ciated with memory reminiscences than with either prospectivethoughts or ongoing learning. Other authors have observed thesephenomena through a facilitated relationship between imageryand emotion [26] or a tendency to recall highly emotional events(moments of particular self relevance) as images rather thanverbally [10]. As a matter of fact, using mental imagery in psy-chotherapy provides an effective route to access and modifyemotion that is superior to verbal processing.

5. Conclusions and perspectives

We conclude that ReSQ is a robust and easy tool for explo-ration of the mental activities of healthy participants during theresting state of an fMRI experiment. The results are consistentwith those from studies investigating inner experience under nat-ural conditions. These behavioral data add some evidence to theself-referential memory and planning activity nature of the rest-ing state. The paper also provides a normative set of data, built onsex and handedness equilibrated in a participant group that can beproductive for future fMRI studies.

The English or French version of the questionnaire can be pro-vided upon request to the authors (e-mail: [email protected]).

Appendix A. Supplementary data

Supplementary data associated with this article can be found, inthe online version, at doi:10.1016/j.brainresbull.2009.11.014.

References

[1] N.C. Andreasen, D.S. O’Leary, T. Cizaddlo, S. Arndt, K. Rezai, G.L. Watkins, L.L.Ponto, R.D. Hichwa, Remembering the past: two facets of episodic memoryexplored with positron emission tomography, Am. J. Psychiatry 152 (1995)1576–1585.

[2] J.R. Andrews-Hanna, A.Z. Snyder, J.L. Vincent, C. Lustig, D. Head, M.E. Raichle,R.L. Buckner, Disruption of large-scale brain systems in advanced aging, Neuron56 (2007) 924–935.

[3] B.J. Baars, How brain reveals mind: neural studies support the fundamental roleof conscious experience, J. Conscious. Stud. 10 (2003) 100–114.

[4] J.R. Binder, J.A. Frost, T.A. Hammeke, P.S. Bellgowan, S.M. Rao, R.W. Cox, Con-ceptual processing during the conscious resting state, A Funct. MRI study. J.Cogn. Neurosci. 11 (1999) 80–95.

[5] W. Brodsky, Y. Kessler, B.S. Rubinstein, J. Ginsborg, A. Henik, The mental repre-

sentation of music notation: notational audiation, J. Exp. Psychol. Hum. Percept.Perform. 34 (2008) 427–445.

[6] R.L. Buckner, D.C. Caroll, Self-projection and the brain, Trends Cogn. Sci. 11(2007) 49–57.

[7] R.L. Buckner, J.L. Vincent, Unrest at rest: default activity and spontaneous net-work correlations, NeuroImage 37 (2007) 1091–1096.

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[8] K. Christoff, A.M. Gordon, J. Smallwood, R. Smith, J.W. Schooler, Experience sam-pling during fMRI reveals default network and executive system contributionsto mind wandering, Proc. Natl. Acad. Sci. U.S.A. 106 (2009) 8719–8724.

[9] M.A. Conway, Sensory-perceptual episodic memory and its context: autobio-graphical memory, Philos. Trans. R. Soc. Lond. 356 (2001) 1375–1384.

10] M.A. Conway, K. Meares, S. Standart, Images and goals, Memory 12 (2004)525–531.

11] M.A. Conway, C.W. Pleydell-Pearce, The construction of autobiographical mem-ories in the self-memory system, Psychol. Rev. 107 (2000) 261–288.

12] A. D’Argembeau, F. Collette, M. Van Der Linden, S. Laureys, G. Del Fiore, C.Degueldre, A. Luxen, E. Salmon, Self-referential reflective activity and its rela-tionship with rest: a pet study, NeuroImage 25 (2005) 616–624.

13] J.S. Damoiseaux, C.F. Beckmann, E.J. Sanz Arigita, F. Barkhof, P. Scheltens,C.J. Stam, S.M. Smith, S.A. Rombouts, Reduced resting-state brain activityin the “default network” in normal aging, Cereb. Cortex 18 (2008) 1856–1864.

14] G.C. Davison, R.S. Vogel, S.G. Coffman, Think-aloud approaches to cognitiveassessment and the articulated thoughts in simulated situations paradigm, J.Consult. Clin. Psychol. 65 (1997) 950–958.

15] D.A. Fair, A.L. Cohen, N.U. Dosenbach, J.A. Church, F.M. Miezin, D.M. Barch, M.E.Raichle, S.E. Petersen, B.L. Schlaggar, The maturing architecture of the brain’sdefault network, Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 4028–4032.

16] P. Fransson, B. Skiold, S. Horsch, A. Nordell, M. Blennow, H. Lagercrantz, U.Aden, Resting-state networks in the infant brain, Proc. Natl. Acad. Sci. U.S.A.104 (2007) 15531–15536.

17] C.R. Glass, D.B. Arnkoff, Questionnaire methods of cognitive self-statementassessment, J. Consult. Clin. Psychol. 65 (1997) 911–927.

18] D.L. Greenberg, D.C. Rubin, The neuropsychology of autobiographical memory,Cortex 39 (2003) 687–728.

19] D.A. Gusnard, E. Akbudak, G.L. Shulman, M.E. Raichle, Medial prefrontal cor-tex and self-referential mental activity: Relation to a default mode of brainfunction, Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 4259–4264.

20] C.L. Heavey, R.T. Hurlburt, The phenomena of inner experience, Conscious.Cogn. 17 (2008) 798–810.

21] E.A. Holmes, A. Mathews, B. Mackintosh, T. Dalgleish, The causal effect of men-tal imagery on emotion assessed using picture-word cues, Emotion 8 (2008)395–409.

22] R.T. Hurlburt, Randomly sampling thinking in the natural environment, J. Con-sult. Clin. Psychol. 65 (1997) 941–949.

23] R.T. Hurlburt, C.L. Heavey, Interobserver reliability of descriptive experiencesampling, Cogn. Ther. Res. 26 (2002) 135–142.

24] R.T. Hurlburt, M. Koch, C.L. Heavey, Descriptive experience sampling demon-strates the connection of thinking to externally observable behavior, Cogn.Ther. Res. 26 (2002) 117–134.

25] S.M. Kosslyn, Image and Brain, MIT Press, Cambridge, 1994.26] S.M. Kosslyn, G. Ganis, W.L. Thompson, Neural foundations of imagery, Nat.

Rev. Neurosci. 2 (2001) 635–642.27] B. Mazoyer, O. Houde, M. Joliot, E. Mellet, N. Tzourio-Mazoyer, Regional cerebral

blood flow increases during wakeful rest following cognitive training, Brain Res.Bull. 80 (2009) 133–138.

[

h Bulletin 81 (2010) 565–573 573

28] B. Mazoyer, L. Zago, E. Mellet, S. Bricogne, O. Etard, O. Houde, F. Crivello, M.Joliot, L. Petit, N. Tzourio-Mazoyer, Cortical networks for working memory andexecutive functions sustain the conscious resting state in man, Brain Res. Bull.54 (2001) 287–298.

29] P.K. McGuire, D.A. Silbersweig, I. Wright, R.M. Murray, R.S. Frackowiak, C.D.Frith, The neural correlates of inner speech and auditory verbal imagery inschizophrenia: relationship to auditory verbal hallucinations, Br. J. Psychiatry169 (1996) 148–159.

30] K.A. McKiernan, B.R. D’Angelo, J.N. Kaufman, J.R. Binder, Interrupting the“stream of consciousness”: an fMRI investigation, NeuroImage 29 (2006)1185–1191.

31] K.A. McKiernan, J.N. Kaufman, J. Kucera-Thompson, J.R. Binder, A paramet-ric manipulation of factors affecting task-induced deactivation in functionalneuroimaging, J. Cogn. Neurosci. 15 (2003) 394–408.

32] E. Mellet, L. Petit, B. Mazoyer, M. Denis, N. Tzourio, Reopening the men-tal imagery debate: lessons from functional anatomy, NeuroImage 8 (1998)129–139.

33] R.C. Oldfield, The assessment and analysis of handedness: the edinburgh inven-tory, Neuropsychologia 9 (1971) 97–113.

34] M.E. Raichle, A.M. MacLeod, A.Z. Snyder, W.J. Powers, D.A. Gusnard, G.L. Shul-man, A default mode of brain function, Proc. Natl. Acad. Sci. U.S.A. 98 (2001)676–682.

35] D.L. Schacter, D.R. Addis, R.L. Buckner, Remembering the past to imagine thefuture: the prospective brain, Nat. Rev. Neurosci. 8 (2007) 657–661.

36] Y.I. Sheline, D.M. Barch, J.L. Price, M.M. Rundle, S.N. Vaishnavi, A.Z. Snyder, M.A.Mintun, S. Wang, R.S. Coalson, M.E. Raichle, The default mode network andself-referential processes in depression, Proc. Natl. Acad. Sci. U.S.A. 106 (2009)1942–1947.

37] G. Shulman, J. Fiez, M. Corbetta, R.L. Buckner, F.M. Miezin, M. Raichle, S.E.Petersen, Common blood flow changes across visual tasks: II. Decreases incerebral cortex, J. Cogn. Neurosci. 9 (1997) 648–663.

38] R.G. Shulman, D.L. Rothman, K.L. Behar, F. Hyder, Energetic basis of brain activ-ity: implications for neuroimaging, Trends Neurosci. 27 (2004) 489–495.

39] C. Sorg, V. Riedl, V.M. Muhlau, V.D. Calhoun, T. Eichele, L. Laer, A. Drzezga, H.Forstl, A. Kurz, C. Zimmer, A.M. Wohlschlager, Selective changes of resting-state networks in individuals at risk for alzheimer’s disease, Proc. Natl. Acad.Sci. U.S.A. 104 (2007) 18760–18765.

40] A.M. Steinbach, Neurolinguistic programming: a systematic approach tochange, Can. Fam. Phys. 30 (1984) 147–150.

41] J. Tracy, N. Goyal, A. Flanders, R. Weening, J. Laskas, P. Natale, B. Waldron, Func-tional magnetic resonance imaging analysis of attention to one’s heartbeat,Psychosom. Med. 69 (2007) 952–960.

42] A.B. Waites, A. Stanislavsky, D.F. Abbott, Effect of prior cognitive state on restingstate networks measured with functional connectivity, Hum. Brain Mapp. 24

(2005) 59–68.

43] S. Whitfield-Gabrieli, H.W. Thermenos, S. Milanovic, M.T. Tsuang, S.V. Faraone,R.W. McCarley, M.E. Shenton, A.I. Green, A. Nieto-Castanon, P. LaViolette, J.Wojcik, J.D. Gabrieli, L.J. Seidman, Hyperactivity and hyperconnectivity of thedefault network in schizophrenia and in first-degree relatives of persons withschizophrenia, Proc. Natl. Acad. Sci. U.S.A. 106 (2009) 1279–1284.