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ORIGINAL RESEARCH
published: 25 November 2016
doi: 10.3389/fnhum.2016.00597
Edited by:
Daniel J. Graham,
Hobart and William Smith Colleges,
USA
Reviewed by:
Ming Meng,
Dartmouth College, USA
Hiram H. Brownell,
Boston College, USA
*Correspondence:
Ori Amir
oamir@usc.edu
Received: 29 February 2016
Accepted: 10 November 2016
Published: 25 November 2016
Citation:
Amir O and Biederman I (2016)
The Neural Correlates of Humor
Creativity.
Front. Hum. Neurosci. 10:597.
doi: 10.3389/fnhum.2016.00597
The Neural Correlates of Humor
Creativity
Ori Amir1,2*and Irving Biederman1,3
1Department of Psychology, University of Southern California, Los Angeles, CA, USA, 2Media Neuroscience Lab,
Department of Communication, University of California, Santa Barbara, Santa Barbara, CA, USA, 3Neuroscience Program,
University of Southern California, Los Angeles, CA, USA
Unlike passive humor appreciation, the neural correlates of real-time humor creation
have been unexplored. As a case study for creativity, humor generation uniquely affords
a reliable assessment of a creative product’s quality with a clear and relatively rapid
beginning and end, rendering it amenable to neuroimaging that has the potential
for reflecting individual differences in expertise. Professional and amateur “improv”
comedians and controls viewed New Yorker cartoon drawings while being scanned.
For each drawing, they were instructed to generate either a humorous or a mundane
caption. Greater comedic experience was associated with decreased activation in the
striatum and medial prefrontal cortex (mPFC), but increased activation in temporal
association regions (TMP). Less experienced comedians manifested greater activation of
mPFC, reflecting their deliberate search through TMP association space. Professionals,
by contrast, tend to reap the fruits of their spontaneous associations with reduced
reliance on top-down guided search.
Keywords: humor creation, fMRI, creativity, expertise, comedians, cartoon captions, temporo-occipital junction
(TOJ), medial prefrontal cortex (mPFC)
INTRODUCTION
A handful of studies have recently begun exploring the neural correlates of creativity, with tasks
ranging from narrative generation (Howard-Jones et al., 2005) to jazz improvisation (Limb and
Braun, 2008) to creative drawing (Schlegel et al., 2015). Unfortunately, the cortical regions reported
by the various studies to be associated with “creativity” were as diverse as the tasks employed,
save for the often observed involvement of the prefrontal cortex (Dietrich and Kanso, 2010). It
has been suggested that activation of the medial prefrontal cortex (mPFC) and a deactivation of
the dorsolateral prefrontal cortex (dlPFC) were the hallmarks of creative processing, along with
regions associated with the particular type of creative task (e.g., Limb and Braun, 2008;Liu et al.,
2012, 2015). However, a one-dimensional comparison between creative and non-creative control
conditions (e.g., jazz improvisation vs. playing from memory; Limb and Braun, 2008) may be
inadequate for revealing the roles played by different brain regions in a creative endeavor, as it
can only reveal a set of regions, typically unsurprising (e.g., visual regions for book cover design,
Ellamil et al., 2012; language regions for poetry composition, Liu et al., 2015), associated with a
particular creative task (as well as, commonly, the mPFC). Exploring two additional dimensions of
a creative domain can further enhance its value as a testbed for the study of creativity: quality and
expertise. With humor, the quality of the creative product (i.e., funniness) can be easily evaluated
by a spontaneous laugh as well as a readily generated judgment. Although the laugh reflects a
subjective state, it is one that is readily accessible for ratings and typically has high agreement
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Amir and Biederman Neural Genesis of Humor
across individuals. Unlike the study of passive humor
appreciation (e.g., Goel and Dolan, 2001;Watson et al.,
2007;Samson et al., 2008;Chan et al., 2013;Vrticka et al.,
2013;Amir et al., 2015), the rarity and spontaneous origin of
humor creation have rendered that domain an unlikely target
of fMRI investigation (Martin, 2010). To meet this challenge,
we recruited professional “improv” comedians who routinely
generate humorous ideas rapidly and on cue.
Previous studies of creativity rarely examined expertise effects,
since often the tasks have no experts, e.g., generate alternative
uses of objects, and others would be too challenging for a control
group, e.g., improvise jazz. Imaging studies comparing experts
to non-experts are typically limited to perceptual/technical
judgments requiring no creativity (e.g., Calvo-Merino et al., 2005;
Kirk et al., 2009). Generating humorous ideas, however, is a
task nearly anyone can attempt, and participants with different
levels of expertise/talent can be identified. Thus far, only the
acts of poetry composition and creative drawing have been
studied with the aim of determining the neural correlates of
both quality and expertise (Liu et al., 2015;Schlegel et al., 2015).
Finally, a humorous creation based on a particular stimulus—a
captionless cartoon in the present study–affords a natural and
tighter control than most creativity studies: the generation of
a mundane statement that would be appropriate for the same
cartoon drawing. Such a control allows a distinction between
standard problem solving and creative thinking (Mednick,
1962).
MATERIALS AND METHODS
Participants underwent fMRI scanning while looking at a
series of cartoon drawings, minus the captions, of human
interactions in various contexts (e.g., office, cocktail party;
see Figure 1), that originally appeared in the NewYorker
Magazine. In a post-session debriefing, in which participants
described an introspection of their creative process during
the experiment, none of the particpants reported familiarity
with the drawings. In order to isolate active humor generation
from any effects of passive humor appreciation, we selected
drawings that were not funny by themselves. The captions that
originally accompanied the drawings and all other text were
removed, and some drawings were processed with Photoshop
to remove elements that were inherently funny. Prior to the
presentation of each cartoon, subjects were cued to generate
(a) a humorous caption, (b) a mundane caption or (c) no
caption (Figure 2 shows the overall activation for the contrast
of the conditions (a)–(b)). Each participant rated on a 4-
point scale how funny their caption was on each trial. At
the end of the scanning, participants were asked to recall as
many of the captions as they could. Their recall was cued
by presentation of the drawings. Independent ratings of those
recalled captions were made by other raters (students at the
University of Southern California) who judged the funniness of
the recalled captions in the context of the drawings, allowing us
to compare the neural correlates of successful vs. unsuccessful
humor generation.
Participants
The participants constituted three groups:
(a) Professional Comedians (13 individuals, mean age 35.4,
range: 26–47; one female). Six were members of the renowned
Los Angeles’ “Groundlings” improv troupe and seven were
professional stand-up comedians, all of whom write their own
material, with significant stand-up related TV credits (e.g.,
multiple late night show appearances, stand-up specials). (The
proximity of USC to Hollywood facilitated the recruitment
of these professional and promising amateur comedians.) No
significant differences were observed in the pattern of activity
of Professional Improv or Stand-Up Comedians, so the two
groups were collapsed into a Professionals’ group, in all but
one of the analyses. That exception is shown in Figure 3: bar
graphs of group differences in selected ROIs, and the associated
analysis.
(b) Nine promising Amateur Comedians (Mean age 27.2,
range: 20–33; two females) each with several years of
experience in stand-up and/or improv, who demonstrated
a significant potential for developing into a professional
comedian relative to their peers. While the amateurs’ focus
may be in either stand-up or improv, all had at least some
experience with both, so they are treated here as one group.
(c) Eighteen Controls (Mean age 24.9, range: 19–34; 7 females).
Controls were all either honor students, graduate students or
faculty at the University of Southern California, selected to
roughly match the high intelligence reported for successful
comedians (Greengross et al., 2012). Age and sex effects have
been statistically assessed in all group comparisons.
The study was approved by the Institutional Review Board
of the University of Southern California and the participants all
signed informed consent.
Procedure
Each trial (Figure 1) lasted 17 s. For the first 2 s of a trial,
a single word cued the desired caption type: (1) “Humorous”
was the cue for the participants to think of a funny caption
(caption =something one of the characters would say) for
the drawing (Humor [HUM] condition); (2) “Expected” was
the cue to think of a caption that would fit the drawing but
be mundane and expected (Mundane [MUN] condition); (3)
“Nothing” (NOTH condition) was the cue look at the drawing
without thinking of a caption. Then a drawing depicting a human
interaction appeared at the center of the screen (subtending
a visual angle of ∼8◦). In the HUM and MUN conditions,
participants had 15 s to generate a caption for the drawing and
rate it for funniness. Once participants thought of a caption
they were instructed to immediately rate it using a keyboard,
on a 4-point scale (1 – not funny, 2 – a little funny, 3 – pretty
funny, 4 – very funny). Each participant saw each drawing
once, and drawings were approximately counterbalanced across
the three conditions between participants. (The balancing was
approximate as the number of participants was not divisible by
the number of conditions for some groups). Each run lasted
7.9 min with 24 jittered trials sequenced such that each sequence
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FIGURE 1 | The time-course of a trial. Participants were prompted to think of a Humorous (HUM), Expected (MUN), or no caption. Try quickly to think of a funny
caption, before you continue reading the following sample caption by one of the participants during the HUM condition: “So this is awkward. I am the woman your
husband has been cheating with. Either way it will be $200 for the marriage counseling...” Original cartoon by Robert Mankoff © Published on September 23, 2002,
in the NewYorker magazine, and was modified from the original for the experimental task so that all text was removed (in the original drawing the diploma on the wall
read “Marriage Counselor”). Adapted and modified with permission.
of two conditions appeared the same number of times. Most
participants completed six runs; all completed at least four.
No runs or participants were discarded. Presentation sequences
were programmed with Psychophysics Toolbox (Brainard, 1997;
Pelli, 1997) running on MATLAB (The MathWorks, Natick, MA,
USA).
Data Acquisition
Data acquisition and preprocessing parameters were matched
with those of a previous investigation of the neural correlates
of passive humor perception (Amir et al., 2015), to allow a
comparison to humor generation. All fMRI images were scanned
at USC’s Dana and David Dornsife Cognitive Neuroscience
Imaging Center on a Siemens Trio 3T scanner with a standard
16-channel head coil. Each subject ran in a high-resolution T1-
weighted structural scan using MPRAGE sequence. [Repetition
time (TR) =1100 ms, 192 sagittal slices, 256 ×256 matrix size,
1mm×1mm×1 mm voxels].
Functional images were acquired using an echo-
planar imaging (EPI) pulse sequence with the parameters:
TR =2000 ms, TE =30 ms, flip angle =62◦, 256 ×256 matrix
size, in-plane resolution 3 ×3, 3 mm thick slices, 32 axial slices
covering as much of the brain as possible, always including the
Temporal Poles, but occasionally missing the superior rim of the
primary motor and somatosensory cortices.
Data Analysis
Preprocessing (3D motion correction using Trilinear
interpolation, 3D spatial smoothing using a 4-mm full-width at
half-max Gaussian filter, linear trend removal using a high-pass
filter set to three cycles over the run’s length) was done with
the Brain Voyager software package (Brain Innovation BV,
Maastricht, The Netherlands). Statistical analysis was done
using MATLAB scripts along with Brain Voyager, and Python.
Motion corrected functional images were coregistered with the
same session’s anatomical scan. Coregistered images were then
transformed to Talairach coordinates and underwent statistical
analysis.
Statistical analysis was based on a general linear model with
a separate regressor for 12 TRs from the beginning of each trial
type (so TR # 1 was recorded during the 2 s interval in which the
instruction cue word was displayed). The six motion correction
parameters (3D translation and 3D rotation) were included in the
design matrix of the regression to eliminate any potential motion
artifacts. We then conducted a whole-brain, random-effects
group average analysis. We defined regions of interest (ROIs)
using the data from all participants with different contrasts
(HUM−MUN, HUM+MUN−2×NOTH), TR-intervals (3–6,
7–10), as well as ROIs obtained in a previous experiment on
passive humor appreciation. For the purpose of defining ROIs,
we used different p-values for different (contrast, TR-interval)
combinations, never higher than p=0.001 uncorrected. Pvalues
were made more conservative in order to define smaller, well
defined, ROIs as necessary (e.g., for the main contrast of HUM-
MUN, we used p<0.01 Bonferroni corrected). The ROIs were
then used to compare activation in the different groups, and to
assess whether the pattern activation in the region encoded the
funniness of the caption.
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FIGURE 2 | Regions with higher activation for HUM (red) vs. MUN (blue). Graphs depict percent BOLD signal change over time (sec).
Evaluating Group Differences
The statistical measures of expertise effects (reported in the
main text) were computed with a regression analysis of the
average difference between HUM and MUN condition over
the full duration of a trial and at peak activity (TRs 5–7),
with age and sex included as regressors of no interest, with
βs the (normalized) regression coefficients of expertise, pits
significance, and d(Cohen’s d) the effect size of the difference
between professional comedians and controls. For the regression
analysis, we defined the variable “expertise” as: Controls =0;
Amateurs =1; Professionals =2. Note that we are treating
the ordinal scale of expertise as interval for the purpose of the
regression analysis, since it captures a surprisingly linear fit of
activation in certain ROIs (Figure 3) – the expertise effects
are further validated, however, by the t-test analysis of the
activation differences between professionals and controls. For
the sake of data exploration, we have further subdivided the
Professionals groups to Professional Stand-Ups and Professional
Improv Comedians, reasoning that since the task is closer to an
improv than stand-up performance the latter group should show
greater “expertise effects.” To illustrate that relationship we re-
ran the regression analysis with Controls =0; Amateurs =1;
Professional Stand-Ups =2; Professional Improv =3. That
analysis resulted in similar βs and pvalues in the major ROIs,
and the striking pseudo-linear relationship is illustrated in
Figure 3.
Assessing Funniness
Participants’ ratings of their own captions, as well as ratings
obtained by the independent raters, were used to evaluate
whether the ROIs obtained by contrasting the different
conditions (e.g., HUM minus MUN) show a funniness magnitude
effect, i.e., whether early activation in these regions (TRs 4–6)
was related to how funny the subsequently generated caption
would be. We chose early TRs in an attempt to target the
process of generating a humorous caption rather than the
evaluation of the fully generated caption. However, our previous
work suggested that the two processes are intertwined – as the
greater activation in temporal regions associated with successful
linking of remote associations in joke generation/comprehension
may also index the joke’s funniness (Biederman and Vessel,
2006;Amir et al., 2015). That said, it is unlikely that such
activity only indexes passive humor appreciation as the peak
of activity is early–before the humorous idea is fully formed
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FIGURE 3 | Group differences among Professional Improv Comedians (PI), Professional Stand-Ups (PS), Amateurs (A) and Controls (C).(A–C) bars
represent average HUM minus MUN activation during its peak; (D–F) bars represent activation averaged across the entire trial. Significance of expertise effect is
represented by ∗p<0.05, ∗∗p<0.01.
(see Results)–and involves the high level semantic regions
where remote associations are expected to converge meaningfully
during humor creation (rather than mere classical reward regions
activation). An ROI was considered to display a “funniness
magnitude” effect if it was localized with the contrast HUM
minus MUN, i.e., the ROI is humor selective, and greater
activation in the ROI preceded the generation of funnier
captions.
Obtaining Independent Ratings
Following the fMRI scan, participants were presented with the
images from their last 1–2 runs (time permitting) and were asked
to recall and write down the captions that they had generated. 81
undergraduate students of the Department of Psychology were
recruited to rate the recalled captions for course credit. Each
spent an hour rating a fraction (typically a quarter) of the total
number of captions on a 7-point scale for funniness, cleverness,
and offensiveness. Ratings were normalized for each participant
before all ratings were averaged.
Eliminating “Double Dipping” Concerns
Whenever the same data are used for localizing ROIs and for
statistical analysis within the ROI there is a concern about a
potential bias due to non-independence (Kriegeskorte et al.,
2009). In the present analysis, we first localized our ROIs using
data from all 40 participants. For the main contrast of HUM
minus MUN, a highly conservative threshold was used (p<0.01,
Bonferroni corrected) and the same regions were localized
independently using only data from each group of participants
(professionals, amateurs, and controls).
We then examined activation within those ROIs to observe
between group differences in HUM minus MUN activation.
While unlikely under the conservative threshold, this scheme
could lead to non-independence concerns in the following
manner: since the “controls” were the largest group of
participants (n=18) they might shift the boundary of the
ROIs localized slightly to favor voxels in which activation
is greatest in the control group. If that were the case, and
there were no real group differences, a pattern in which the
subsequent between group analysis showed greater activation
in the control group might emerge from non-independence
alone. We found the opposite effect of expertise in the temporo-
occipital junction (TOJ; see results and Figure 3). To ensure
these results were not an artifact of biased ROI boundaries we
repeated the analysis using adjacent ROIs (in mPFC and STR)
localized with independent data from a previously published
study on passive humor appreciation (Amir et al., 2015), as no
previous fMRI studies of humor creation exist. This analysis
yielded nearly identical results in trend (PI <PS <A<C; see
Figure 3), statistical significance and effect sizes – thus none
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of the group effects could be explained as an artifact of double
dipping.
RESULTS AND DISCUSSION
Behavioral Reaction Times
Reaction times (RTs) of the three groups (Professionals,
Amateurs, and controls) as measured by the time for the key
press for rating the funniness of the generated caption was 2.37 s
greater for the HUM relative to the MUN condition; a difference
that was significant for all levels of expertise (Supplementary
Table S1). RTs for rating the captions were significantly longer for
professional comedians relative to amateurs, apparently taking
greater advantage of the 15 s trial duration, t(20) =3.23,
p<0.005. No significant difference in RTs was observed
between amateurs, and controls, t(24) <1. The differences in
RTs reported above were unlikely to have produced the fMRI
differences between groups as the main ROIs were localized
with the early peak of activation, which coincided for the two
conditions (HUM and MUN). The RT gap between HUM and
MUN did not differ significantly between the three groups (all
ts<1), and all group comparisons of BOLD activity were
restricted to that obtained by first contrasting HUM vs. MUN
activity within subjects. A related concern is that the difficulty
of the HUM condition was greater than that of the MUN
condition, as suggested by the longer RTs and that task difficulty
rather than the requirement to be creative or humorous might
explain any activation differences observed in the HUM vs.
MUN contrast. However, as discussed below, several of the
regions which showed greater activation in HUM than MUN
also exhibited a “funniness magnitude” effect, that is, greater
activation in those regions early in the trial correlated positively
with funnier captions produced by the subject later in the trial
(with funniness judged by independent raters) – rendering it
more plausible that the regions were involved in the creative
process.
Neural Signature of Creating Humorous
vs. Mundane Captions
Taken as a group the 40 participants showed significantly
greater activation during HUM relative to MUN trials in
bilateral striatum, mPFC, TOJ and primary visual cortex
(V1; p<0.01, Bonferroni corrected; see Figure 2 and
Table 1). A conjunction analysis of MUN and HUM conditions,
contrasted with activation during the NOTH condition revealed
additional activations in temporal regions – particularly the
bilateral anterior temporal regions (p<0.001, uncorrected;
Supplementary Table S5). That activation occurred early in the
trial, suggesting the regions’ involvement in the initial efforts to
generate a humorous idea rather than the evaluation of the final
product, or humor appreciation.
Most studies of passive humor appreciation have reported
involvement of high-level semantic regions in the temporal lobes
(Vrticka et al., 2013) and we have previously suggested that
is the region where remote associations converge meaningfully
when “getting” a joke (Amir et al., 2015). The present results
suggest that those regions are involved in creating humor as well,
albeit with a different time course (see section Active Humor
Creation vs. Passive Humor Appreciation). The mPFC has been
implicated in most studies of creativity (Liu et al., 2015), as
well as in some studies of humor appreciation (e.g., Amir et al.,
2015). It appears to be involved in humor creation as well, but is
likely not the source of humorous ideas (see General Discussion).
The greater activation of V1 during the HUM condition may
reflect a greater engagement of visual search for aspects of the
drawing, perhaps an incongruity, with a comedic potential. In
the case of passive humor appreciation (Watson et al., 2007),
greater visual cortex activation was reported for visual gags
(relative to non-humorous visual stimuli), but not to language
gags – this additional visual activation was suggested by Watson
et al. (2007) to reflect the resolution of the punchline, but such
reactivation of visual areas occurs for any reinterpretation of a
visual stimulus, humorous or not (Sterzer et al., 2009;Amir et al.,
2015).
Independent Funniness Ratings
Associated with Greater Early Activation
in Temporal Regions and Striatum
Amir et al. (2015) found that temporal regions, TOJ and TP,
exhibited a funniness “dose response.” That is, activity in those
regions were greater for humorous than non-humorous stimuli
and for the humorous stimuli, the same regions responded more
strongly to the instances with higher funniness ratings. Similarly,
in professional comedians we observed that early in the trial,
the generation of funnier captions elicited greater activity in
the striatum, bilateral TOJ, and other temporal regions (but
not in mPFC). The regions were localized by subtracting MUN
from HUM trials, that the activation was even greater for the
funnier captions in those regions can be described as a funniness
magnitude effect. The relationship held whether funniness was
evaluated based on the comedians’ own ratings or by independent
raters (only rated captions from the HUM condition were
included in this analysis; see Table 1, Supplementary Table S5).
The funniness magnitude effect was observed early in the time-
course of the trial (TRs 4–6), suggesting it reflects the process
of creating the humorous caption rather than the evaluation
of its final product. Controls and amateurs, however, showed
no funniness magnitude effect in the regions localized by the
contrast HUM minus MUN. Controls did show such correlations
in some of the regions localized by the conjunction of HUM and
MUN (Supplementary Table S5). The funniness magnitude effect
cannot be explained away by mere increased effort or engagement
as that would entail an increase of activity in all regions of the
network (defined by the contrast HUM minus MUN, which
includes mPFC) during the generation of the funnier captions,
which was not the case as mPFC showed higher activation, on
average, during the generation of the less funny captions.
Of the few MRI creativity studies, only a handful attempted
to correlate the quality of the creative product with BOLD
activation. The results of those studies are difficult to compare
as they used different measures for “quality” (from novelty
and complexity to “craft”) with some of those studies (ours
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TABLE 1 | ROIs as localized by the contrast of HUM minus MUN (Random
Effects Analysis) with a threshold of p<0.01 Bonferroni corrected
(TR =3–6).
ROI NrOfVoxels X Y Z OWN FUN CLV OFF
V1 4523 −3−78 −11 P∗∗ P∗
mPFC 637 −3 49 27
STR 11985 −1−3 6 P∗ ∗ P∗
CER 539 0 −49 −32
lTOJ 5978 −32 −78 −6 P∗∗ P∗ ∗ ∗ P∗
rTOJ 3395 30 −82 5 P∗∗ ∗ P∗∗
With number of Voxels, Talairach coordinates and funniness magnitude effect
for Professionals (P), Amateurs (A) and Controls (C). For self-rating (OWN), and
independent ratings of funniness (FUN), cleverness (CLV) and offensiveness (OFF).
Significance levels are: ∗p<0.1, ∗∗ p<0.05, ∗ ∗ ∗ p<0.01. Key: r, right; l, left;
V1, primary visual cortex; mPFC, medial prefrontal cortex; CER, cerebellum; STR,
striatum; TOJ, temporo-occipital junction.
included) correlating the trial-by-trial quality scores to activity,
while others approximated it with subjects’ general creativity
scores on a separate creativity task. Nevertheless, a pattern
emerges suggesting that the quality of different creative tasks
correlate with activity in different regions: complexity of
pianists’ improvisation correlates with activity in pre-SMA cortex
(Bengtsson et al., 2007), creativity of rhythm improvisation
is associated with bilateral prefrontal cortex and right insula
(Villarreal et al., 2013), creative writing with the left fronto-
temporal network (Shah et al., 2013), free style rap performance
with activity in medial temporal regions, posterior cingulate
cortex and left mPFC (Liu et al., 2012), and skillful drawing with
changes in prefrontal white matter connectivity and a distinct
pattern of activation in temporal, motor and prefrontal cortices
(Schlegel et al., 2015). Even within the same imaging study during
a poetry creation task, different measures of quality, craft and the
linguistic creativity evident in the poetry, were associated with
different networks involving mPFC and dlPFC, respectively (Liu
et al., 2015). The lack of consistency suggests that there is no
one region acting as a general creativity fount so that greater
activity in that region correlates with creative products that are of
higher quality. Distinct regions appear to play this role for distinct
creative tasks. Here we find the quality of humor creativity, i.e.,
funniness, is associated with temporal and striatal activity.
Neural Correlates of Comedic Expertise
We observed a clear function of comedic experience/talent
throughout the trial so that HUM minus MUN activity in the
mPFC (regression coef. β= −0.55, p<0.01, Cohen’s d=1.43)
and striatum (right: β= −0.43, p<0.05, d=1.07; left: β= −0.46,
p<0.05, d=1.47) was greatest for Controls than Professional
comedians with Amateurs falling in between. The reverse was
true in the right TOJ with peak activation (β=0.31, p<0.05,
d=1.05) greatest for Professionals and smallest for Controls.
The left TOJ exhibiting a similar pattern that failed to reach
significance. Of the Professionals, Improv Comedians showed
even greater activation in TOJ on average and lower activation
in mPFC and STR than the Stand-Up Comedians. That result
is in line with the trend set by Controls vs. Amateurs and the
Professionals group as a whole, since the experimental task is
more similar to an improv comedy scene than stand-up, so
Improv Comedians would be judged to possess the greatest
level of expertise on the experimental task (Figure 3). These
results cannot be explained by non-independent selective analysis
biases (a.k.a. “double dipping”; see Materials and Methods). We
propose that the temporal regions are where remote associations
converge meaningfully in the process of constructing the joke,
while mPFC directs the process of deliberate search in a top-
down manner, and that the expertise/talent effects suggest that
with greater comedic expertise less involvement of control
processes (localized in mPFC) is needed as the Comedians
reap the fruits of their spontaneous associations (see General
Discussion).
The Comedians had a smaller proportion of females than the
controls, a statistic that roughly reflects the high proportion of
males among comedians (Greengross et al., 2012). In computing
the beta values above, age and sex were controlled for as
regressors of no interest, and typically showed no significant
correlations with the ROIs’ activations, with the one exception
of sex in rTOJ. During humorous caption generation, maleness
was positively correlated with rTOJ activity, in a similar fashion
to comedic expertise (β=0.35, p<0.05).
Active Humor Creation Vs Passive
Humor Appreciation
While passive humor appreciation has been extensively studied
(Vrticka et al., 2013;Amir et al., 2015), the present study is the
first yet to explore humor creation. The regions we found to
be involved in humor creation (or, at least, adjacent regions)
have been implicated in passive humor appreciation in some
of the previous studies (including our own, Amir et al., 2015).
However, there are distinct time course differences for passive
vs. active humor processing. In this section, we characterize
the differences between humor creation and appreciation by
comparing the current results to those of Amir et al. (2015), as
well as comparing activity in the early vs. late stages of humor
creation. Humor creation, at least with improv comedy, has
another favorable feature facilitating its MRI investigation: it is
a well-defined cognitive event, long enough to tease apart both
in its early (Figures 2–5) as well as its later stages (Figure 4).
A whole-brain contrast of HUM minus MUN late in the trial
(Supplementary Table S6; Figure 4) revealed that activation
shifted from bilateral TOJ toward the TPJ and more anterior
temporal regions, closer to regions that have previously been
identified as selective for passive humor appreciation (Vrticka
et al., 2013;Amir et al., 2015). During humor appreciation,
the time-course of temporal activation peaks early and declines
rapidly relative to humor creation, presumably reflecting that
“getting a joke” generally would occur more quickly—and end
earlier—than the act of creating a joke. In contrast to the
shorter activity peak of passive humor appreciation, active humor
creation resulted in a gradual increase in anterior temporal
and TPJ activation throughout the trial, suggesting the gradual
construction of comedic meaning via the discovery and linkage
of remote associations.
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FIGURE 4 | Top: ROIs selective to humor creation (HC) early in the trial (red), late in the trial (blue), and in passive humor appreciation (HA) – overlaid
from a previous study (Amir et al., 2015; yellow). Graphs show activation of HUM minus MUN in early (Top, in red) and late (Bottom, blue) HC areas, with
passive HA activation (data obtained from Amir et al., 2015) in the same regions in black.
Funniness Ratings
Eighty-one independent raters (that did not take part in the
fMRI experiment) rated the captions obtained in the fMRI
experiment (each rated about a quarter of the captions with
the ratings normalized within by the individual rater prior
to their compilation). Reassuringly, all subjects self-rated their
captions as funnier in the HUM that in the MUN trials
(Supplementary Table S2) and the independent raters also
rated HUM captions significantly higher for all groups of
participants (Supplementary Table S3), with overall significant
covariance between subjects’ own ratings and independent
raters ratings (Supplementary Table S4). The differences in self-
ratings between HUM and MUN trials were similar among
the three groups (all ts<1), but independent raters saw
a greater difference in funniness between HUM and MUN
trials for the controls compared to the professional comedians
[t(24) =2.10, p<0.05, Cohen’s d=0.95]. Taken together, it
appears that regardless of expertise, when generating captions,
people (at least intelligent adult Americans) have some degree
of control over the funniness of the outcome, but professional
comedians may be less successful in suppressing funny ideas
when asked to generate mundane captions (as also volunteered
by several professional comedians’ introspections during the
debriefing).
In contrast to the expectation that at least professional
comedians should produce funnier captions than the other
groups, the funniness scores from the independent raters did not
distinguish among the three participant groups (professionals,
amateurs or controls), all ts<1. This should not in any way
cast doubt as to the “expert” classification of our professional
comedians, as having a Netflix Comedy Special or gaining
membership in the Groundlings are extraordinarily competitive
achievements. Rather, the nature of our drawings–cartoons in
which any incongruous or funny elements were removed–
resulted in a particularly difficult setting for the comedians
who seek an incongruous or unusual element in a scene as
the point of departure for their humor (Mankoff, 2002). That
said, the incongruity and humor-free nature of our stimuli
has the advantage of not confounding the neural correlates
of the participants generating humorous ideas from those of
appreciating the humor in the prompt itself. The effects of
incongruity in the settings would appear to be a problem worth
studying for understanding the nature of humor creativity.
The average (HUM/MUN) number of captions remembered
differed among professionals (7.2/6.8), amateurs (12.1/11.9)
Controls (9.5/10.6). Not much is to be made of those group
differences as they partially resulted from extraneous factors such
as professionals having a busier schedule and so less time to
spend after the experiment remembering captions. To ensure the
group comparisons of funniness were not biased by the number
of captions remembered (e.g., if participants who remembered
fewer captions remembered the funnier ones) the analysis was
repeated with the funniest 5, 3, and 1 captions with similar
results.
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FIGURE 5 | Striatum activation in professional comedians is greater in HUM then MUN condition (Left), and within the HUM condition is greater prior
to the generation of funnier captions, as rated by the participant (Middle) or independent raters (Right). Stars indicating significance: ∗p<0.05,
∗∗ p<0.01, ∗ ∗ ∗ p<0.001.
GENERAL DISCUSSION
Professional comedians, amateurs, and controls generated
captions to NewYorker cartoons, revealing a network of regions–
including bilateral TOJ, mPFC and the striatum–that exhibited
greater activation during humorous (HUM) vs. mundane (MUN)
caption generation.
Many of the MRI studies of humor appreciation have
found greater activation in some high-level semantic regions
in the temporal lobes (e.g., TOJ, TPJ, TP, STS) during the
humorous condition (Vrticka et al., 2013). These regions, where
information converges from diverse lower level regions (Man
et al., 2013) are likely the site were remote associations converge
meaningfully during the comprehension of a humorous product.
There is greater activation in those regions for humorous than
non-humorous discoveries/insights, as well as a dose response
function, i.e., among humorous stimuli, those rated funnier
by the participants produce greater activation in those regions
(Amir et al., 2015). Based on the discovery of a gradient of
µ-opioid receptors (Lewis et al., 1981) peaking in associative
regions in the temporal lobes, activation in semantic temporal
association regions (TMP) has been found to be pleasurable
and likely a factor in the feeling of mirth itself (Biederman and
Vessel, 2006). That temporal associations tend to elicit positive
emotions has been documented in preferences for scenes (Yue
et al., 2007), simple shapes (Amir et al., 2011) and jokes (Amir
et al., 2015;Amir, 2016). Thus, it was not surprising that we
found greater activation there during humor creation during
which, presumably, remote associations are generated and linked
in the process of joke construction. While temporal activity
is observed during both humor appreciation and creation,
peak activity during creation is observed in adjacent but more
posterior regions and shows a temporal pattern of continuous
gradually increasing activity throughout the trial in contrast to
the shorter rise and fall of activation during humor appreciation,
presumably corresponding to the act of “getting the joke.”
Analogous to the temporal lobes’ “dose response” of passive
humor appreciation, our professional comedian participants
show a “funniness magnitude” effect so that greater activation
in the temporal lobes early in the trial correlates with the
generation of funnier captions later in the trial. Finally, the
contrast HUM-MUN yielded greater activity in temporal regions
for professional comedians followed by amateurs and controls
in declining order, suggesting reliance on those regions during
comedy creation increases with experience (and/or talent). Taken
together the findings suggest that the temporal regions are likely
where comedic meaning is represented and constructed.
Since all drawings depicted people interacting, could the
temporal activity during the HUM condition reflect a greater
engagement of theory of mind (Saxe and Kanwisher, 2003) rather
than convergence of remote associations? Since both the HUM
and MUN used the same drawings and required participants
to generate a statement one of the characters would say in the
situation, contrasting the two conditions is expected to control
for theory-of-mind effects on activation, unless during humor
creation participants engage in theory of mind processing to a
greater extent. While the current paradigm does not allow us to
determine the exact cognitive processes indexed by the temporal
activity (be it convergence of remote associations, theory of
mind, or other processes), it appears to be related to humor
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Amir and Biederman Neural Genesis of Humor
creation as it is greater for humorous than mundane caption
generation, and correlates positively with caption’s funniness as
well as participants’ comedic expertise.
The mPFC is the region most consistently reported in fMRI
creativity studies (Dietrich and Kanso, 2010;Liu et al., 2015;
Saggar et al., 2015), in jazz improvisation (Limb and Braun,
2008), rap improvisation (Liu et al., 2012), and story generation
(Howard-Jones et al., 2005), but also in problem solving tasks that
would appear to require less creativity, such as anagram solutions
(Aziz-Zadeh et al., 2009). The mPFC’s role is likely to extend
cognitive control over the creative process (Ridderinkhof et al.,
2004;Passingham et al., 2010). However, our findings suggest the
mPFC might not be the source of creative ideas as it does not
show a funniness magnitude effect (i.e., there was no correlation
between activity there and caption funniness, in contrast to
the temporal regions) and is less activated in professional
comedians relative to amateurs and controls. The mPFC showed
less activation, while the TOJ (as well as some anterior temporal
regions), were more active in professional comedians, relative to
controls, suggesting professionals rely more on the spontaneous
flow and linking of associations in the temporal regions, with
less mPFC engagement for deliberate search. This result is in line
with Schlegel et al. (2015) who found that fractional anisotropy
in prefrontal white matter progressively decreased with visual
art training, suggesting a reorganization of connectivity to the
region. The pattern of decreased mPFC and increased temporal
activity may be the translation to neuroscience language of the
most common advice offered by improv comedy coaches: “get out
of your head.”
The striatum is part of the classical reward system and is
activated in response to any pleasurable stimulus, including
humor as well as other forms of art (Vessel et al., 2012).
Unlike the case of humor appreciation (Amir et al., 2015),
where striatal activation follows or coincides with activation
of temporal regions, peak striatal activation preceded the peak
of temporal activation in the case of humor creation. The
striatum also showed a correlation between early activation
and the creation of funnier captions in professional comedians
(Figure 5). Whether the magnitude of the funniness effect in
the striatum of professional comedians reflects an on average
accurate expectation that the caption they will generate later in
the trial will be funnier or is playing a more causal role, e.g.,
by helping the retrieval of associations with a greater potential
for humor (Scimeca and Badre, 2012) remains to be determined.
The latter interpretation is consistent with a common comedy
coaches’ advice: “have fun and you will be funnier.” Some of
the alternative explanations for the expertise effect on striatal
activation, e.g., that comedians have a more depressive emotional
style or that comedians are adapted to the reward of humor
creation, are inconsistent with the finding that the BOLD
response of professional comedians to the HUM condition by
itself (i.e., not contrasted with MUN) is as high as that of controls.
CONCLUSION
Humor creation is marked by activation in a network of regions
including mPFC, the striatum, and temporal regions. Only
activation in the temporal regions exhibited both a positive
correlation with expertise as well as a “funniness magnitude”
effect (greater activation early in the trial predicts a funnier
caption at trial’s end) suggesting the temporal regions are a
likely source of the humorous ideas. While greater mPFC activity
was observed during humor creation (relative to generation
of mundane captions) the activity decreased with occupational
experience, suggesting that while mPFC might help to direct the
search through association space taking place in the temporal
regions, such intervention is needed less for more experienced
comedians who, to a greater extent, reap the fruits of their
spontaneous associations.
AUTHOR CONTRIBUTIONS
OA and IB conceived and designed the experiment, and written
the manuscript. OA conducted the experiment and data analysis.
FUNDING
This study was supported by NSF BCS 04-20794, 05-31177,
06-17699 to IB.
ACKNOWLEDGMENTS
We would like to thank neuroscientists Jonas Kaplan and Bosco
Tjan, and comedians Troy Conrad, Dave Reinitz, Shane Mauss,
and Greg Wilson for their helpful insights.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: http://journal.frontiersin.org/article/10.3389/fnhum.
2016.00597/full#supplementary-material
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Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
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