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Elements of creative thought: Investigating the cognitive and neural
correlates of association and bi-association processes
Mathias Benedek
a
,
*
, Julian Jurisch
a
, Karl Koschutnig
a
, Andreas Fink
a
, Roger E. Beaty
b
a
Institute of Psychology, University of Graz, BioTechMed, Graz, Austria
b
Department of Psychology, Pennsylvania State University, USA
ARTICLE INFO
Keywords:
fMRI
Brain
Creativity
Memory
Imagery
Lingual gyrus
Hippocampus
ABSTRACT
Creative thinking relies on the ability to make remote associations and fruitfully combine unrelated concepts.
Hence, original associations and bi-associations (i.e., associations to one and two concepts, respectively) are
considered elementary cognitive processes of creative cognition. In this work, we investigated the cognitive and
brain mechanisms underlying these association processes with tasks that asked for original associations to either
one or two adjective stimuli. Study 1 showed that the generation of more original associations and bi-associations
was related to several indicators of creativity, corroborating the validity of these association performances as basic
processes underlying creative cognition. Study 2 assessed brain activity during performance of these association
tasks by means of fMRI. The generation of original versus common associations was related to higher activation in
bilateral lingual gyri suggesting that cued search for remote representatives of given properties are supported by
visually-mediated search strategies. Parametric analyses further showed that the generation of more original
associations involved activation of the left inferior frontal cortex and the left ventromedial prefrontal cortex,
which are consistently implicated in constrained retrieval and evaluation processes, and relevant for making
distant semantic connections. Finally, the generation of original bi-associations involved higher activation in
bilateral hippocampus and inferior parietal lobe, indicating that conceptual combination recruits episodic
simulation processes. Together, these findings suggest that the generation of verbally cued, original associations
relies not only on verbal semantic memory but involves mental imagery and episodic simulation, offering new
insights in the nuanced interplay of memory systems in creative thought.
1. Introduction
In recent years, an increasing number of studies have explored brain
activity in diverse creative activities ranging from creative problem
solving to artistic activities (Abraham, 2018;Jung and Vartanian, 2018).
One promising approach in this field is to identify basic cognitive pro-
cesses that are assumed to be broadly relevant to different forms of cre-
ative thought (Benedek and Fink, 2019). Considering the role of memory,
for instance, a long-standing notion in the cognitive science of creativity
holds that creative idea generation requires connecting unrelated con-
cepts, which is achieved by finding original associations and combining
them in a meaningful way (Mednick, 1962). Creative thinking hence
relies on the generation of original associations (i.e., remote associations
to one concept) and on the generation of bi-associations (i.e., links be-
tween two concepts), which corresponds to the broad capacities of con-
ceptual expansion and conceptual combination, respectively (Ward et al.,
1997). Here, we sought to investigate the cognitive and neural mecha-
nisms underlying these two elementary processes of creative thought. To
this end, we devised tasks assessing the generation of original associa-
tions and bi-associations in the context of word associations. In a first
study, we explored the criterion validity of these association tasks with
respect to creativity, and in a second study, we examined the brain
activation related to these association abilities by means of fMRI.
1.1. Expanding concepts: the generation of original associations
For many routine cognitive activities, it is crucial to quickly retrieve
relevant, closely related information in order to produce appropriate
responses. Creative thought, however, typically requires avoiding com-
mon, dominant associations in order to produce original responses. The
generation of associations can occur either via spontaneous, free-
associative and or via goal-directed, controlled mechanisms (Beaty
* Corresponding author. Institute of Psychology, University of Graz, BioTechMed, Universit€
atsplatz 2, 8010, Graz, Austria.
E-mail address: mathias.benedek@uni-graz.at (M. Benedek).
Contents lists available at ScienceDirect
NeuroImage
journal homepage: www.elsevier.com/locate/neuroimage
https://doi.org/10.1016/j.neuroimage.2020.116586
Received 24 July 2019; Received in revised form 19 December 2019; Accepted 24 January 2020
Available online 28 January 2020
1053-8119/©2020 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
NeuroImage 210 (2020) 116586
et al., 2014;Benedek and Jauk, 2018;Sowden et al., 2015). Free asso-
ciation reflects the basic spreading of activation in semantic networks,
whereas controlled association generation reflects a goal-directed pro-
cess of constrained recall considering specific search cues. Early con-
ceptions assumed that original associations produced by creative people
are the result of a deviant organization of memory (Mednick, 1962). This
view has been challenged by the observation that creative people do not
only typically find more uncommon (i.e., original) associations but also
more common associations compared to control groups when explicitly
asked to do so (Merten and Fischer, 1999). In fact, creative people were
found to exhibit very similar free association patterns of increasingly
original associations but they produced responses much more fluently,
thus resulting in more original associations within a given time (Benedek
et al., 2012;Benedek and Neubauer, 2013). Moreover, creative cognitive
potential in terms of divergent thinking ability is substantially related to
higher intelligence and executive control (Benedek and Jauk, 2019;
Chrysikou, 2018), with particularly high correlations typically observed
with broad retrieval ability (Gr), suggesting that creative idea generation
relies on highly effective search and retrieval mechanisms (Avitia and
Kaufman, 2014;Forthmann et al., 2019;Silvia et al., 2013).
A few studies have begun to shed light on the brain mechanisms
related to the generation of original associations. One fMRI study asked
participants to generate verb associations to nouns and cued them to
think creatively in half of the trials (Green et al., 2015). The cued trials
resulted in more semantically distant responses (as assessed by latent
semantic distance analysis), and individual differences in cued associa-
tion performance were related to several established measures of creative
potential in a separate behavioral study (Prabhakaran et al., 2014).
Moreover, Green et al. (2015) found that the generation of remote as-
sociations was related to increased brain activity in a left-lateralized
frontal network including medial prefrontal cortex and inferior frontal
gyrus, as well as occipital (cuneus and lingual gyrus) and cerebellar re-
gions. A parametric analysis further revealed that brain activity in a re-
gion of interest in the left frontopolar cortex linearly increased with the
semantic distance of responses, suggesting that this frontopolar region is
implicated in the generation of particularly remote associations.
Another study examined the effect of conceptual interference in the
verb generation task and found that high conceptual constraints resulted
in less semantically distant responses, which corresponded to increased
brain activity in bilateral precuneus, angular gyrus, posterior cingulate,
left middle frontal gyrus, and lingual gyrus (Beaty et al., 2017). More-
over, generative constraints were further related to increased functional
connectivity between a left executive control network and anterior
default network, suggesting that coupling between these executive and
default network regions plays a role in overcoming conceptual interfer-
ence in creative thought (Beaty et al., 2016). Yet another fMRI study
compared brain activation during the generation of free association
chains (i.e., a sequence of consecutively related word pairs) with per-
formance in word fluency and category fluency tasks (Marron et al.,
2018). Free association performance was related to higher divergent
thinking ability and involved higher activation in a left-lateralized
network including the medial prefrontal cortex, posterior cingulate,
temporoparietal junction, as well as inferior, middle, and superior frontal
gyrus.
In the context of creative idea generation, some studies have looked at
the process of passive conceptual expansion, assessed by the evaluation
of more versus less original ideas, and active conceptual expansion,
assessed by actual creative idea generation, and found consistent
involvement of the temporal poles, inferior frontal gyrus and frontopolar
cortex (Abraham et al., 2012;Abraham et al., 2018;Kr€
oger et al., 2012).
Together, these studies show that the generation of original associations
is a valid low-level process of creative cognition that implicates several
regions within the default network (DN) and executive control network
(ECN), as well as visual networks. Brain activation in and functional
coupling between these large-scale brain networks have been consis-
tently related to various forms of creative cognition (Beaty et al., 2016;
Zabelina and Andrews-Hanna, 2016).
1.2. Combining concepts: the generation of original bi-associations
Creativity theories also emphasize that creative thinking requires
uncovering associations that connect two unrelated concepts in a fruitful
way. The generation of such an associative link can be called bi-associa-
tion (or bisociation, see Koestler, 1964), double association, or associative
combination. While an original association represents a distant leap
within one concept’s association network, a bi-association establishes a
link, or identifies a point of overlap, between the association networks of
two largely unrelated concepts. Mednick (1962) devised the Remote
Associates Test (RAT) to assess individual differences in the ability to
flexibly combine concepts. The RAT presents three unrelated cue words
and requires finding a fourth word offering a link to all cues in terms of
building compound nouns with each (e.g., blue, cottage, cake; response:
cheese). Process analyses of RAT performance have shown that it
commonly involved incrementally constrained search processes, where
participants make an association to one cue and then evaluate its fit to the
other cues (Smith et al., 2013). Hence, one approach to bi-association
generation may be to generate original associations to one concept and
evaluating its semantic relation to the other. Notably, the validity evi-
dence for the RAT is mixed as it typically shows high correlation with
verbal intelligence (Lee and Therriault, 2013) and lower associations
with creativity indicators (Taft and Rossiter, 1966), which may be related
to the fact that RAT solutions only represent linguistic links in the form of
compound nouns (e.g., blue cheese, cheese cake), but do not necessarily
establish a semantic link between these concepts. Other work has tapped
more directly into the process of bi-association using tasks asking for
associative combinations of two unrelated nouns or for humorous ex-
planations of arbitrary word combinations (e.g., “yoga-bank”or “cere-
al-bus”, which showed correlations with established measures of creative
potential (Benedek et al., 2012;Nusbaum et al., 2017). Interestingly,
creative people also judge unrelated concepts as more semantically
related, suggesting that they are very sensitive to subtle associative links
between concepts (Benedek et al., 2017;Rossmann and Fink, 2010).
While several studies have examined the brain activation related to
the generation of original associations, neuroscientific investigations of
the bi-association process are more sparse. Some works studied brain
activation when solving the RAT, but they typically focused on the
distinction between subjective experiences of insight versus non-insight
problem solving (Jung-Beeman et al., 2004). Other studies tapped into
similar processes when studying relational integration (Christoff et al.,
2001) or analogical reasoning (Green et al., 2010), which were related to
brain activity in rostrolateral prefrontal cortex (PFC). Bendetowicz et al.
(2017) developed an associative version of the RAT (i.e., solutions
represent semantically related terms rather than compound words that
share one term) and found that higher performance in this task was
related to lower gray matter volume in the left rostrolateral PFC and in
the left inferior parietal lobule. Another study by Bendetowicz et al.
(2018) on patients with focal frontal lesions found that damage to the
right medial PFC affected their ability to generate remote associations,
whereas damage to the left rostrolateral PFC spared remote association
ability but impaired the associative combination ability as measured with
the associative RAT. Further fMRI studies found that the generation of
novel ideas versus recalled ideas implied higher activation of the left
anterior inferior parietal cortex (Benedek et al., 2014b;Benedek et al.,
2018), which was attributed to this regions’role in cross-modal semantic
integration (Binder et al., 2009). These findings offer first insights into
the brain structures relevant to associative combination processes but, to
date, an investigation contrasting association and bi-associations pro-
cesses is still missing.
1.3. Aims of this study
The present study aimed to investigate neurocognitive mechanisms
M. Benedek et al. NeuroImage 210 (2020) 116586
2
underlying the generation of original associations and bi-associations. In
afirst behavioral study, we developed tasks that assess these processes
separately and explored their validity with respect to established mea-
sures of creativity. In a subsequent fMRI study, we measured brain ac-
tivity during the generation of original associations and bi-associations
relative to the generation of common associations. This work extends
available research by assessing brain activation of two elementary
cognitive processes central to creative cognition within the same para-
digm, which allows testing activation differences between the generation
of original versus common associations, and between the generation of
original bi-association versus single associations. Based on the available
literature we hypothesized that conceptual expansion processes, which
are reflected in the generation of original associations, recruit regions of
DN and ECN, including the medial and lateral prefrontal cortex, while
conceptual integration processes, which are specific to the generation of
bi-associations, may be related to brain activity in the left rostrolateral
PFC and left inferior parietal cortex.
2. Study 1: behavioral investigation
2.1. Method
2.1.1. Participants
The final sample consisted of 102 participants (62 females), aged
between 18 and 38 years (M¼25.4; SD ¼4.1). Another five participants
had been excluded from further analyses due to invalid performance in
the association tasks (i.e., generation of other word types than nouns, or
missing data >25%). All participants gave written informed consent.
2.1.2. Tasks and materials
2.1.2.1. Association tasks. This study involved three association tasks,
requiring the generation of either common associations, original associ-
ations, or bi-associations. All tasks used adjectives as stimuli and asked to
generate a semantically related noun (either a single or multi-word
term). In the common association task (Com-Assoc), participants should
find a highly related concept to a given adjective, one that “may first
come to mind to most people”thus representing a common association
(e.g., red: blood). In the original association task (Orig-Assoc), participants
should find a remotely related concept to a given adjective, one that
“only few people would think of”and that “represents an original asso-
ciation”(e.g., red: ketchup stain). These association tasks were inspired
by previous studies comparing free versus individual associations
(Merten and Fischer, 1999), associations versus dissociations (Benedek
et al., 2012), or uncued versus cued verb associations (Prabhakaran et al.,
2014). In the bi-association task (Bi-Assoc), two adjectives were presented
and participants should find a concept that is semantically related to both
cues and links them in an original way (e.g., red - round: clown nose).
Specifically, participants were asked to “think of a concept for which
both adjectives (characteristics) apply”, and, if they have time to
generate different responses, to “choose the more original one”. This task
requires a semantic integration of two largely unrelated concepts and
thus is similar to the associative version of the Remote Associates Test
that used three cue words (Bendetowicz et al., 2017), and to the asso-
ciation combination task that asked to find many bi-associations for given
noun pairs (Benedek et al., 2012). Importantly, generating a balanced
bi-association for two largely unrelated stimulus concepts cannot simply
be achieved by producing a common association to one of the stimuli but
rather requires finding a concept that is somewhat remote yet reasonably
related to both stimuli. Hence, performance of the Bi-Assoc task is
thought to involve remote association processes similar to the Org-Assoc
task, but additionally requires conceptual integration processes.
The stimulus words were taken from a German word corpus (http
://corpora.uni-leipzig.de/de). We selected 60 adjectives that are
frequent in German language (frequency class of 17 or lower, meaning
that each word is not more than 2
17
times infrequent than the most
frequent German word “der”[the]) and that are largely unrelated (i.e.,
not listed as synonym to any other adjective). With the 60 adjectives, we
created 30 trials for each task (i.e., 90 trials in total): half of the adjectives
were randomly assigned to the Com-Assoc task and the other half to the
Orig-Assoc task, and all adjectives were used to build 30 adjective-pairs
for the Bi-Assoc task. For the adjective pairs, we generally strived to
choose adjectives with low semantic similarity. The average cosine
similarity of the adjective pairs (based on latent semantic analysis using
the dewak100k_lsa corpus, a German LSA-type space covering 300 di-
mensions and containing vectors for 100,000 different words) was 0.32
(SD ¼0.15; range ¼0.07 - 0.61). A full list of all stimuli is given in the
Supplemental Material.
The tasks were presented on a computer screen and responses were
written on a response sheet. Participants first performed the single as-
sociation tasks (Com-Assoc and Orig-Assoc) in an inter-leaved fashion.
The stimuli were presented for 5s, during which the participants thought
of an association response (i.e., thinking period). If the stimulus word
was underlined they should think of an original association, but if it was
not underlined they should think of a common association. The Com-
Assoc and Orig-Assoc conditions switched predictably every three trials
to reduce potential switching costs. After the thinking period, a blank
screen was presented for 5 s indicating the response period during which
responses were written down. The subsequent Bi-Assoc task followed the
same procedure, except that the thinking period was 8s to allow enough
time for the more complex task of generating associations for two cue
words.
Valid responses (i.e., not missing, noun responses) were obtained in
96% of the Com-Assoc trials, 92% of the Orig-Assoc trials, and in 91% of
the Bi-Assoc trials. All responses were rated by five raters. Responses of
the single association tasks (Com-Assoc and Orig-Assoc) were pooled and
then rated for creativity using a four-point scale (0–3), with higher rat-
ings given to responses that were judged as task-appropriate and original
(i.e., responses that are semantically related to the stimulus and poten-
tially reflect clever, surprising, or humorous associations). Invalid or
missing responses were assigned a zero rating. Quality of responses in the
Bi-Assoc task was also evaluated on a four-point rating scale, with ratings
of 0 given to responses that were unrelated to both cues, ratings of 1
given to responses that mostly reflect only one cue, ratings of 2 are given
to responses that reflected both cues well, and ratings of 3 given to highly
original responses that reflect both cues well. All raters were trained in a
common session but they rated responses independently. Inter-rater-
reliability was good for the single association tasks (ICC ¼0.80) and
acceptable for the Bi-Assoc task (ICC ¼0.75).
2.1.2.2. Validation measures. Task performance was validated with
respect to common indicators of creativity including divergent thinking
(DT) ability, real-life creative behavior, and creative personality. DT
ability was assessed with the alternate uses task, which asks to name all
the creative uses one can think of for everyday objects. Participants
completed four tasks (rope, car tire, knife, pillow) of 2 min each. All
responses were rated for creativity by five raters on a four-point rating
scale (0–3) with higher ratings given to responses that were judged as
both novel and effective (responses are task-appropriate and clever,
surprising, or humorous; Diedrich et al., 2015;Runco and Jaeger, 2012).
Inter-rater-reliability was acceptable to good (ICC ¼0.79). DT creativity
was defined as the average creativity rating of three most creative re-
sponses as determined by the average across raters (max-3 scoring; for
similar scorings see, Benedek et al., 2013;Silvia et al., 2008). Addition-
ally, we measured DT fluency defined as the number of responses in the
DT tasks.
Real-life creative behavior was measured with the activity scale of the
Inventory of Creative Activities and Achievements (ICAA; Diedrich et al.,
2018). This scale asks how often specific creative activities have been
performed in the last ten years (0 ¼never, to 4 ¼more than 10 times),
M. Benedek et al. NeuroImage 210 (2020) 116586
3
covering eight creative domains (e.g., literature, music etc.) with six
items each. The internal consistency of the ICAA creative activities was
high (ICC ¼0.90).
Openness to new experiences, the most consistent factor of creative
personality (Feist, 1998), was assessed with 12 openness items from the
NEO-FFI (Borkenau and Ostendorf, 1999). Since all tasks required writ-
ten responses, we further assessed writing speed to examine potential
effects of common method bias. Participants were asked to write down as
many number words (1–10) as possible in ascending and descending
sequence within 20 s (i.e., one –two –three …) and the total number of
written words was used as index of writing speed (Benedek et al., 2012).
We further assessed broad retrieval ability (Gr) and fluid intelligence
(Gf), which have been shown to be consistently correlated with creative
potential (Jauk et al., 2014;Silvia et al., 2013). Gr was assessed with two
letter fluency tasks (F, N), two category fluency tasks (professions, types
of sport), and two free association tasks (pure, funny; these adjectives
were not part of the association tasks). Participants generated as many
responses as possible within 1 min per task. The response fluency scores
of all tasks were averaged to obtain a total Gr score. Gf was assessed with
a shorted version of the Ravens Advanced Progressive Matrices (18
even-numbered items; 10 min task duration; Raven et al., 1962) and with
the 20-item number series task from the intelligence structure test (IST,
2000 R; Liepmann et al., 2007). The solution rate in both tasks was
averaged to obtain a total Gf score.
2.1.2.3. Data and code availability. Data and code of Study 1 and 2 are
available upon request from the authors to be further used for scientific
purposes. These conditions comply with the institutions ethics approval
and the requirements of the funding body.
2.1.2.4. Procedure. Participants took part in the experiment individually
or in small groups of up to five persons per session. All tasks were
administered in a fixed sequence: writing speed, single association tasks,
bi-association task, openness, DT, Gr, Gf, ICAA activities. The session
took about 90 min in total. The procedure was approved by the local
ethics committee.
2.2. Results and discussion
Table 1 presents descriptive statistics and inter-correlations of the
three association tasks and all validation measures. As expected, the Orig-
Assoc task elicited more creative association responses (M¼1.64, SD ¼
1.20) compared to the Com-Assoc task (M¼1.35; SD ¼1.07; t[101] ¼
6.58, p<.001, d¼0.64), supporting the general effectiveness of the
creativity instruction. This finding is consistent with previous work
showing that the explicit instruction to “be creative”increases the crea-
tivity of responses (and not just the divergence of responses; Weinberger
et al., 2016) as has been repeatedly demonstrated for divergent thinking
tasks (Acar et al., 2020;Said-Metwaly et al., 2020) as well as for more
elementary association tasks (Merten and Fischer, 1999;Prabhakaran
et al., 2014). For the Bi-Assoc task, an average rating of 1.61 was
observed. Specifically, responses were evaluated with 2 or higher in
61.2% of ratings (67% of valid responses), suggesting that the task was
challenging, but still yielded task-appropriate responses reflecting both
cues in the majority of cases.
Performance in the Com-Assoc task was only correlated with Orig-
Assoc performance but with none of the validation measures. In
contrast, Orig-Assoc performance showed substantial correlations with
DT creativity, DT fluency, openness, Gr and Gf (see Table 1). These
findings replicate the observation that single association tasks, which do
not reflect response fluency (cf. Benedek et al., 2012), are only indicative
of creativity when performed under “be creative”instructions (Prabha-
karan et al., 2014). Similarly, performance in the Bi-Assoc task was
significantly correlated with all validation measures including DT crea-
tivity, DT fluency, creative activity, openness, Gr, and Gf.
Hence, validity evidence for Orig-Assoc and Bi-Assoc tasks was ob-
tained with respect to various established indicators of creativity such as
divergent thinking ability, real-life creative behavior, and openness
(Jauk et al., 2014). Correlations with Gr and Gf are consistent with the
broad evidence on the executive nature of creative thought (Benedek
et al., 2014c;Silvia et al., 2013). Interestingly, Gr tended to be stronger
correlated with Orig-Assoc than with Bi-Assoc, whereas Gf tended to be
higher correlated with Bi-Assoc than with Orig-Assoc. These differences
may highlight relatively higher demands on cued retrieval from semantic
networks versus complex semantic integration and evaluation processes
involved in the Orig-Assoc and Bi-Assoc tasks, respectively. Notably,
despite the substantial correlation between Orig-Assoc and Bi-Assoc, they
predicted unique variance in openness (β¼0.21, and 0.24, p<.05,
respectively), but in none of the other validation measures, suggesting
that they capture at least partly complemental capacities. Taken together,
these findings indicate that original association and bi-association per-
formances reflect elementary cognitive processes of creative cognition. In
study 2, we used these association tasks to study brain processes related
to the generation original and bi-associations relative to common
associations.
3. Study 2: fMRI investigation
3.1. Method
3.1.1. Participants
An independent sample of 44 University students (26 female), aged
between 19 and 36 years (M¼24.34; SD ¼4.35), participated in study 2.
Two additional participants had been excluded from further analyses,
one because of aborting the scanner session due to indisposition, and one
because of insufficient language skills (non-native speaker). Participants
were recruited by local advertisements and gave written informed con-
sent. They were either paid or participated for partial course credit.
Table 1
Descriptive statistics and correlations of all measures.
MSD 12 3 456 789
1 Com-Assoc 1.07 0.11 –
2 Orig-Assoc 1.20 0.21 .33 –
3 Bi-Assoc 1.62 0.18 .17 .44 –
4 DT Creativity 1.61 0.32 .15 .38 .25 –
5 DT Fluency 8.03 2.55 .12 .30 .22 .37 –
6 C-Activity 1.42 0.52 .05 .17 .20 .25 .17 –
7 Openness 2.92 0.51 .12 .32 .33 .22 .13 .40 –
8 Gr 13.26 2.04 .17 .42 .29 .39 .51 .18 .25 –
9 Gf 11.54 2.78 .07 .31 .36 .07 .06 .07 .16 .16 –
10 W-Speed 12.41 1.75 .10 -.08 -.06 .01 .04 -.01 .19 .09 .09
Notes. Com-Assoc ¼common association, Orig-Assoc ¼original association, Bi-Assoc ¼bi-association, DT ¼Divergent thinking, C-Activity ¼Creative activities, Gr ¼
Broad retrieval ability, Gf ¼fluid intelligence, W-Speed ¼Writing speed. For n¼102, correlations of r0.19 are significant at p<.05, correlations of r0.25 are
significant at p<.01, and correlations of r0.31 are significant at p <.001. Significant correlations (p<.05) are indicated in bold.
M. Benedek et al. NeuroImage 210 (2020) 116586
4
3.1.2. Experimental task and procedure
Participants performed the three association tasks (Com-Assoc, Orig-
Assoc, Bi-Assoc) described in Study 1. Outside the scanner, participants
received thorough task instructions, including ten practice trials. In the
scanner, they completed a total of 75 trials, including 25 Com-Assoc
trials, 25 Orig-Assoc trials, and 25 Bi-Assoc trials (a full list of all stim-
uli is given in the Supplemental Material). Trials were grouped in five
blocks of five trials each to reduce task switching demands. Task blocks
were presented in one out of two quasi-randomized sequences. At the
beginning of a block, a task cue (Common association, Original associ-
ation, Combined association) was presented at the middle of the screen
for 5 s. Then, each trial started with a fixation period, presenting a white
fixation cross on black background jittered between 3 and 5 s, followed
by the thinking period (Com-Assoc, and Orig-Assoc: 5 s; Bi-Assoc: 8 s),
presenting the task stimulus in white letters on black background. In the
Bi-Assoc task, the stimulus consisted of two adjectives (e.g., red –round),
whereas in the single association tasks (Com-Assoc, and Orig-Assoc) the
stimulus consisted of one adjective that was presented two times (e.g. red
–red) in order to keep visual demands similar across all tasks. During the
thinking period participants were asked to think about a response but not
verbalize it; when they found a solution before timeout, they were asked
to think of an even better response in the remaining time (Com-Assoc:
more common association; Orig-Assoc and Bi-Assoc: more original
response). After this thinking period, the stimulus appeared in green let-
ters for 4 s (response period), prompting the participants to vocalize their
response (Benedek et al., 2019;Fink et al., 2009). Responses were
recorded with an MRI-compatible microphone and transcribed by an
experimenter outside the scanner room. The whole task took about 20
min. Fig. 1 illustrates the task procedure. The scanner session included a
field-map scan, a T1 scan, and performance of the described tasks and
another short task unrelated to this study (Benedek et al., 2018). The
procedure was approved by the local ethics committee.
3.1.3. fMRI data acquisition
Whole brain imaging was performed on a 3T Siemens Skyra MRI
system (Siemens Healthineers, Erlangen, Germany) using a 32-channel
head coil. Structural brain images were obtained using a T1-weighted
3D-MPRAGE sequence (TR ¼1560 ms, TE ¼2.07 ms, flip angle ¼9,
176 sagittal slices, 1 11 mm, FoV ¼256 256 mm, TI ¼900 ms).
BOLD-sensitive T2*-weighted functional images were acquired using a
single shot gradient-echo EPI pulse sequence (TR ¼2400 ms, TE ¼30 ms,
flip angle ¼90, 39 axial slices, 3 33 mm, distance factor 20%, FoV
¼240 240 mm, interleaved slice ordering). The first two volumes were
automatically discarded to allow for T1 equilibration effects. head. In
addition to structural and functional images, a dual-echo gradient echo
field map (TR ¼403 ms, delta TE ¼2.46 ms) was recorded for distortion
correction of the acquired EPI images. Head motion was restricted using
firm padding that surrounded the head.
Visual stimuli were presented using the software Presentation (Neu-
robehavioral Systems, Albany, CA) on an LCD monitor positioned at the
top end of the scanner bore, viewed through a mirror attached to the
head coil. Verbal responses were recorded by means of an MRI-
compatible noise cancelling microphone (FOMRI-III; Optoacoustics,
Mazor, Israel) also attached to the head coil.
3.1.4. Data analysis
3.1.4.1. Behavioral analysis. All responses were transcribed and
checked. Trials with missing responses or with responses that were not
nouns were flagged as invalid and excluded from further analyses. For
tests of performance differences between Com-Assoc and Orig-Assoc, all
single association task responses were pooled and evaluated for origi-
nality by three independent judges on a four-point rating scale ranging
from 0 (common) to 3 (highly original) following standard rating pro-
cedures (Benedek et al., 2013;Silvia et al., 2008). Inter-rater reliability
was good (ICC ¼0.81) and creativity ratings were averaged across raters.
3.1.4.2. fMRI data analysis. MRI data were converted to BIDS format
ensuring standardization and anonymization of data (Gorgolewski et al.,
2016), and verified using the BIDS validator (http://bids-standard.github
.io/bids-validator/). Data were preprocessed with the preprocessing
pipeline fMRIPrep 1.3.2 (Esteban et al., 2019) using the default pro-
cessing steps. In summary, each structural image was corrected for in-
tensity non-uniformity and skull-stripped. Spatial normalization to the
ICBM 152 Nonlinear Asymmetrical template version 2009c was per-
formed through nonlinear registration with antsRegistration (ANTs
2.2.0). Functional data was corrected for susceptibility distortions based
on a coregistered field map. Slice-timing correction was performed using
3dTshift from AFNI 20160207 (Cox and Hyde, 1997). Based on the
estimated susceptibility distortion, an unwarped BOLD reference was
calculated for a more accurate co-registration with the anatomical
reference. The BOLD reference was then co-registered to the T1w
Fig. 1. Procedure of the scanner tasks involving the common association task (Com-Assoc), original association task (Orig-Assoc) and bi-association task (Bi-Assoc).
M. Benedek et al. NeuroImage 210 (2020) 116586
5
reference using bbregister and resampled to MNI152NLin2009cAsym
standard space. Then, a high-pass filter (128s cut-off) was applied.
Several time-series of potential confounds were calculated including
frame-wise displacement, global signals and physiological regressors to
allow for component-based noise correction (CompCor; Behzadi et al.,
2007). Finally, functional data were smoothed with a 6-mm full-width at
half-maximum Gaussian kernel in SPM 12 (Wellcome Department of
Imaging Neuroscience, London, UK).
Effects were estimated using the General Linear Model (GLM) as
implemented in SPM 12. At the first level, three regressors of interest
were included, representing the generation periods of valid trials in the
three association tasks. The three regressors were modelled with boxcar
functions with the length of task duration convolved with the canonical
hemodynamic response function (HRF). We further included the
response period and twelve control parameters derived during pre-
processing as regressors of no interest to control for susceptibility effects
related to response generation and head motion. Linear contrasts were
used to obtain subject-specific estimates for each effect, which were
entered into a second-level analysis treating subjects as a random effect.
We investigated the brain mechanisms underlying the search for
remotely related concepts (i.e., the process of conceptual expansion) by
contrasting the brain activation during the generation of original versus
common association (Orig-Assoc >Com-Assoc). Linear effects of asso-
ciation remoteness were further analyzed with a parametric analysis
considering the originality of association responses. In a next step, we
examined the process of conceptual combination/integration by con-
trasting brain activation during the generation of original bi-associations
versus original single associations (Bi-Assoc >Orig-Assoc); for the sake of
completeness, we also report the contrast of bi-association versus com-
mon association generation (Bi-Assoc >Com-Assoc). Additionally, we
performed low-level task contrasts by contrasting each task individually
against implicit baseline (findings from these complementary analyses
are reported in the Supplemental Material, Tables S1–S3). Whole-brain
effects were inclusively masked with a binary gray matter mask esti-
mated based on the SPM12 gray matter tissue map (x >0.2), and effects
are reported when they were significant at voxel-level (p<.05, FWE-
corrected for multiple comparisons) and cluster size was 3.
3.2. Results and discussion
3.2.1. Task performance
Participants generated valid responses in 96% of the Com-Assoc tri-
als, 92% of the Orig-Assoc trials, and in 92% of the Bi-Assoc trials. The
responses in the Orig-Assoc task were again significantly more original
(M¼1.55; SD ¼0.30) than in the Com-Assoc task (M¼0.83; SD ¼0.19; t
[43] ¼13.90, p<.001; d¼2.05), supporting the effectiveness of the task
instructions to generate original versus common associations.
3.2.2. Brain activation related to the generation of original associations
We examined task-specific brain activation effects by means of the
task contrast Orig-Assoc >Com-Assoc. The generation of original versus
common associations was associated with higher brain activation in
focused clusters of bilateral lingual gyrus (Table 2, and Fig. 2). This
finding is consistent with previous research, reporting brain activation in
lingual gyri during word association tasks (Andreasen, 2012;Green et al.,
2015) as well as during more complex forms of divergent thinking (Beaty
et al., 2017;Fink et al., 2015). The lingual gyrus plays an important role
for vision encoding and retrieval especially in the context of words and
for the generation of visual mental images (Kosslyn et al., 1997;Leshikar
et al., 2012;Machielsen et al., 2000). These findings suggest that the
generation of original associations for adjective words may actually
involve visually-mediated retrieval strategies. While searching for com-
mon representatives of adjectives may be achieved by simple recall of
primary associations from verbal semantic memory (e.g., round: ball),
finding original representatives of properties (e.g., round: Frisbee) may
be more effective when search is cued by abstract mental images of the
physical property. This notion is further supported by findings from an
fMRI study comparing the generation of metaphors and synonyms, which
showed that metaphor generation based on given adjectives (e.g., this
room is [dark]: a cave) also involved higher activation of the lingual
gyrus besides other regions (Benedek et al., 2014a).
3.2.2.1. Parametric effects of association originality. While Com-Assoc
and Orig-Assoc tasks clearly differed in the originality of associations,
we still observed considerable variance in the originality of associations
within tasks. Hence, as a second approach, we analyzed parametric ef-
fects of rated originality across all valid responses in the two single as-
sociation tasks. This analysis showed that more original association
responses were related to higher brain activation in a left-lateralized
network of clusters including the inferior frontal gyrus, superior frontal
gyrus, superior temporal gyrus and ventromedial prefrontal cortex
(vmPFC) as well as in bilateral clusters of the calcarine cortex extending
to lingual gyri (see Table 3, and Fig. 3). These additional regions mainly
involve frontal regions associated with cued retrieval and response se-
lection and evaluation (Kleinmintz et al., 2018;Thompson-Schill et al.,
1997;Vartanian et al., 2018) highlighting the executive nature of
goal-directed creative thought processes. The parametric analysis thus
indicates the relevance of further brain regions beyond lingual gyri for
the generation of original associations, which is likely related to the
larger variance of responses across both tasks. In fact, separate para-
metric analyses per task show that, in the Com-Assoc task, parametric
originality effects were most prominent in the IFG and calcarine cortex,
whereas in the Orig-Assoc task parametric originality effects were more
prominent in the vmPFC and STG (see Supplemental Materials, Tables S4
and S5).
Similar findings have been previously observed in parametric ana-
lyses of response creativity in the alternate uses task and in metaphor
generation, which implicated the left IFG and the dorsomedial prefrontal
cortex for producing more original responses (Benedek et al., 2014a,
2014b). These findings are also partially consistent with those from a
similar study asking for verb associations either cued or uncued for
creativity (Green et al., 2015), which also found that the generation of
original responses involved higher activation of the right lingual gyrus,
while effects were strongest in the medial frontal gyrus and the right
cerebellum. Moreover, parametric analyses showed that higher origi-
nality of verb responses as measured by LSA was associated with higher
frontopolar brain activation in a predefined ROI located in left medial
PFC, similar to the results of the whole brain analysis in our study, which
also implicated the left medial PFC although peaking more ventrally
(vmPFC). The vmPFC is recruited during episodic simulation such as in
Table 2
Whole-brain task effects (FWE-corrected at voxel-level, p <.05, k 3).
Region Lat. Peak (MNI) T
peak
P
voxel
(FWE) k
xyz
Orig-Assoc >Com-Assoc
Lingual G R 15 72 12 6.24 .003 26
Lingual G L 978 5 5.72 .018 4
Bi-Assoc >Com-Assoc
Lingual G,
Hippocampus
R2163 9 6.52 .001 69
Hippocampus L 30 39 2 8.34 <.001 18
AG L 39 78 41 6.21 .003 12
Cerebellum L 12 72 25 6.87 <.001 3
MOG R 36 81 28 5.94 .009 3
Bi-Assoc >Orig-Assoc
IPL (AG, SMG) R 42 48 51 6.45 .002 41
IPL (AG, SMG) L 39 51 44 6.08 .005 4
Hippocampus R 24 619 5.73 .017 3
Note. AG ¼Angular Gyrus, SMG ¼Supramarginal Gyrus, G ¼Gyrus, MOG ¼
Middle Occipital Gyrus, IPL ¼Inferior Parietal Lobe.
M. Benedek et al. NeuroImage 210 (2020) 116586
6
reconstruction and imagery of novel scenes (Barry et al., 2019;Hassabis
and Maguire, 2007) suggesting that highly original associations re-
sponses resulted from strategies based on scene imagery. Together with
findings relating medial PFC to semantic distance in analogical mapping
(Green et al., 2010), this region seems to play an important in the gen-
eration of semantically distant associations.
To further explore the role of visual areas in association generation,
we ran a post-hoc parametric analysis including imageability ratings of
the adjectives as additional parameter besides response originality
(K€
oper &Schulte im Walde, 2016). This analysis revealed that higher
imageability of stimuli resulted in increased brain activation of bilateral
inferior parietal cortex (especially angular gyrus and supramarginal
gyrus) and right middle and inferior frontal gyrus, whereas lower
imageability of stimuli (higher abstraction) involved increased brain
activation in visual areas including bilateral lingual gyri and superior
occipital gyrus (see Supplemental Material, Table S6). These findings
suggest that imageability of stimulus words (which is highly correlated to
their concreteness; r¼0.81) affects the level of involvement of visual
areas in association generation, with more imaginable, concrete words
implicating higher involvement of semantic brain regions versus more
abstract words implicating higher involvement of visual areas.
3.2.3. Brain activation related to the generation of bi-associations
Contrasts of brain activation during the generation of bi-associations
with common associations (Bi-Assoc >Com-Assoc) revealed higher
activation in bilateral hippocampus extending to the right lingual gyrus
and in the left angular gyrus (see Table 2, and Fig. 2). Similar to the
generation of original associations, the generation of bi-associations
hence involved higher lingual gyrus activity, but additionally recruited
bilateral hippocampus and left angular gyrus. Contrasting the generation
of original bi-associations with the generation of original single associ-
ations (Bi-Assoc >Orig-Assoc) revealed higher activation in dorsal parts
of bilateral inferior parietal lobe involving angular and supramarginal
gyrus and in a ventral part of the right hippocampus. These brain
structures are considered posterior parts of an episodic simulation
network that is involved in reconstructive processes of episodic retrieval
but also in constructive processes such as future thinking or divergent
thinking (Beaty et al., 2018;Schacter et al., 2012). For example, the
generation of novel scenes based on verbal prompts has been related to
Fig. 2. Whole brain task effects (FWE-corrected at voxel level, p <.05, k3).
Slice view at x,y,z-coordinates of cluster peaks: A: Orig-Assoc >Com-Assoc:
Lingual Gyrus (15,-72,-12); B: Bi-Assoc >Com-Assoc: Hippocampus (-30, -39,
-2); C: Bi-Assoc >Orig-Assoc: IPL (42,-48,51).
Table 3
Parametric analysis for response originality across responses in Com-Assoc and
Orig-Assoc tasks (FWE-corrected at voxel-level, p <.05, k 3).
Region Lat. Peak (MNI) T
peak
P
voxel
(FWE) k
xyz
IFG (oper.,
triang.)
L57 21 21 8.66 <.001 147
Calcarine C,
Lingual G
R1266 11 6.18 .004 29
Calcarine C L 12 72 14 6.66 .001 21
NC R 6 6 2 7.28 <.001 17
STG L 60 39 6.26 .003 12
SMA 3 15 61 6.93 <.001 10
NC L 12 18 4 6.16 .004 7
Cerebellum R 36 57 29 6.01 .007 5
Calcarine C L 21 63 8 5.87 .011 4
NC L 6 9 1 5.77 .015 4
vmPFC L 654 15 6.18 .004 3
Note. IFG ¼Inferior frontal gyrus, NC ¼Nucleus caudatus, STG ¼Superior
temporal gyrus, SMA ¼Supplemental Motor Area, G ¼gyrus, C ¼cortex.
Fig. 3. Whole brain parametric effect of association originality (FWE-corrected
at voxel level, p <.05, k3).vmPFC ¼ventromedial prefrontal cortex, IFG ¼
inferior frontal gyrus, STG) superior temporal gyrus, SMA ¼supplemental motor
area, CC ¼calcarine cortex, LG ¼lingual gyrus.
M. Benedek et al. NeuroImage 210 (2020) 116586
7
hippocampus activity driven by vmPFC (Barry et al., 2019). These find-
ings indicate that the generation of bi-associations involves episodic
simulation processes possibly to construct mental scenes that feature
both properties.
4. General discussion
Understanding basic elements of creative thinking is an important
precondition for the investigation of more complex creative behaviors.
Creativity theories posit that creative ideas arise from the retrieval of
remote associations that are combined in novel and appropriate way
(Mednick, 1962). Therefore, this work devised tasks assessing the gen-
eration of original associations and bi-associations, which are thought to
represent the abilities to expand and combine concepts, respectively
(Abraham et al., 2012;Ward et al., 1997). Two studies examined the
cognitive and neural correlates of these association and bi-association
processes as elements of creative thought.
Study 1 showed that the generation of original associations and bi-
associations (but not the generation of common associations) was
correlated with several established indicators of creative potential
including divergent thinking ability, broad retrieval ability, openness,
and creative behavior. Moreover, study 1 and 2 both found that explicit
instructions to find original associations consistently increased response
originality, indicating that people can effectively tune response behavior
towards creativity (Acar et al., 2020;Said-Metwaly et al., 2020;Wein-
berger et al., 2016). Together, these findings corroborate the notion that
basic association processes capture valid elementary cognitive aspects of
creative cognition (Benedek et al., 2012;Merten and Fischer, 1999;
Prabhakaran et al., 2014).
At the neural level, the generation of original associations and bi-
associations clearly differed from common association generation. The
task contrast between original and common associations revealed higher
activation in bilateral lingual gyrus, a region implicated in visual
encoding and retrieval and in the generation of mental images (Kosslyn
et al., 1997;Leshikar et al., 2012;Machielsen et al., 2000). Moreover, the
parametric analysis offered a more nuanced result, showing that beyond
bilateral activation in lingual and calcarine cortex, more original asso-
ciations were related to higher brain activation especially in the left IFG.
IFG plays a crucial role in cued search and selection of information from
semantic memory and was actually found to be prominently involved in
all three association tasks. Yet, higher IFG activity was related to more
original associations suggesting that higher IFG activity facilitates more
effective search and evaluation processes (Kleinmintz et al., 2018)
allowing access to more remote locations within the solution space (i.e.,
semantic network). Activation of lingual gyrus and calcarine gyrus
indicated that the generation of original associations to adjectives does
not only rely on simple verbal association processes but may additionally
imply visually-mediated search strategies.
Additional parametric analyses indicated that the involvement of
visual strategies may actually be moderated by the imageability of
stimuli. Interestingly, more abstract words prompted higher involvement
of visual areas. These findings are consistent with previous research
showing that different strategies within the same task imply different
brain activation patterns. For example, Leshikar et al. (2012) compared
brain activation during encoding of word pairs based on either sentence
generation and visual imagery strategies and found higher right lingual
gyrus activity related to sentence generation strategy, but also higher
right lingual gyrus activity predicting successful recall when employing
the visual imagery strategy. Another study showed that right lingual
gyrus was more strongly activated when using scene encoding compared
to sentence encoding strategies, whereas the left lingual gyrus was more
strongly activated during sentence encoding (Johnson and Rugg, 2007).
Together, our findings suggest that generating original associations may
imply both verbally and visually-mediated retrieval mechanisms. Verbal
mechanisms, driven by regions including the left IFG, involve the scan-
ning of semantic memory to retrieve remotely associated concepts. Visual
mechanisms, driven by lingual gyri, may additionally imply the genera-
tion of mental images in order to cue relevant representations in visual
semantic memory. Future research may test the role of verbal versus
visual mechanisms in original association generation more directly by
means of explicit instructions to use either verbal or visual strategies
(Johnson and Rugg, 2007;Leshikar et al., 2012). As an alternative
approach, studies may systematically vary the modality of cues (Chrys-
ikou et al., 2016) or the concreteness versus abstractness of cue words
(K€
oper &Schulte im Walde, 2016).
The generation of bi-associations differed from the generation of
single associations by stronger activation within hippocampus and infe-
rior parietal lobe (e.g., angular gyrus), which represent hubs of a core
network associated with episodic memory and simulation (Schacter
et al., 2012). This result suggests that the integration of two unrelated
concepts is supported by episodic simulation processes, where the two
adjectives trigger the construction of relevant scenes representing these
cues. This is a remarkable finding as it shows that bi-association gener-
ation does not just represent a more constrained version of association
generation, where retrieval considers two cues instead of one, but rather
implies qualitatively different cognitive mechanisms to achieve effective
conceptual integration. This notion is consistent with previous research
showing that the core network of episodic memory and simulation is
consistently involved in divergent thinking (Beaty et al., 2018;Madore
et al., 2017) and that particularly the left inferior parietal lobe is crucial
to the generation of novel ideas (Benedek et al., 2014b;Benedek et al.,
2018). These findings help to elucidate the role of episodic simulation in
creative cognition by suggesting that they already occur at the level of
basic constructive processes, such as the conceptual combination of
concepts.
As a potential limitation of this study, the Bi-Assoc and Org-Assoc
tasks differed in how explicitly they instructed to be creative. We as-
sume that the generation of valid, balanced bi-associations also involves
remote association processes because common associations for one
stimulus typically would not be reasonably related to the other. Hence,
Bi-Assoc and Org-Assoc both require remote associations while Bi-Assoc
performance involves higher conceptual integration demands. Future
research could examine the role of originality in bi-association genera-
tion more directly, by instructing participants explicitly about the need to
be creative and analyzing differences in originality across responses.
Moreover, stimuli could be pre-selected specifically in terms of their
semantic distance, imageability versus abstractness and maybe other
features in order to be able to study their effect on strategies and brain
process in the association process.
Together, these findings offer new insights in the brain mechanisms
underlying the generation of remote associations and conceptual inte-
gration, two key processes of creative thinking. Importantly, they advise
caution when attributing cognitive tasks to specific modalities such as
verbal or visual (Benedek et al., 2019). While the association tasks of this
study involved verbal stimuli (one or two adjective words), the brain
activation findings indicate that generating original associations and
bi-association for characteristics recruits structures related to the gen-
eration of mental images and scenes, thus suggesting the relevance of
visually-mediated search strategies. These findings extend our under-
standing of the role of basic memory processes in creative cognition
(Benedek and Fink, 2019). Hence, considering evidence from neurosci-
ence can help us to revise overly simplistic cognitive models of creativity,
and the investigation of elementary cognitive processes in creative
thought is viewed a particularly useful approach to this end.
Acknowledgements
This research was supported by a grants from the Austrian Science
Fund (FWF): P23914 and P29801. We gratefully acknowledge the help of
Simon Ceh, Marcel Jud, and Thomas Zussner in this work.
M. Benedek et al. NeuroImage 210 (2020) 116586
8
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.neuroimage.2020.116586.
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