Content uploaded by Bianca P Acevedo
Author content
All content in this area was uploaded by Bianca P Acevedo on Nov 13, 2018
Content may be subject to copyright.
Available via license: CC BY 3.0
Content may be subject to copyright.
The highly sensitive brain: an fMRI study of sensory
processing sensitivity and response to others’ emotions
Bianca P. Acevedo
1
, Elaine N. Aron
2
, Arthur Aron
2
, Matthew-Donald Sangster
3
, Nancy Collins
1
&
Lucy L. Brown
4
1
Department of Psychological and Brain Sciences, University of California, Santa Barbara, California
2
Department of Psychology, Stony Brook University, New York, New York
3
Monmouth University, Monmouth County, New Jersey
4
Department of Neurology, Albert Einstein College of Medicine, Bronx, New York
Keywords
Emotion, empathy, highly sensitive person,
magnetic resonance imaging, mirror neurons,
sensory processing sensitivity
Correspondence
Bianca P. Acevedo, Department of
Psychological and Brain Sciences, University of
California, Santa Barbara, CA 93106-9660.
Tel: 516-298-2422;
Fax: 718-565-8728;
E-mail: acevedo@psych.ucsb.edu.
Funding Information
This research was supported by grants from
the National Science Foundation (0958171)
and the University of California at Santa
Barbara’s Brain Imaging Center.
Received: 1 October 2013; Revised: 30
March 2014; Accepted: 30 April 2014
Brain and Behavior 2014; 4(4): 580–594
doi: 10.1002/brb3.242
Abstract
Background: Theory and research suggest that sensory processing sensitivity
(SPS), found in roughly 20% of humans and over 100 other species, is a trait
associated with greater sensitivity and responsiveness to the environment and to
social stimuli. Self-report studies have shown that high-SPS individuals are
strongly affected by others’ moods, but no previous study has examined neural
systems engaged in response to others’ emotions. Methods: This study exam-
ined the neural correlates of SPS (measured by the standard short-form Highly
Sensitive Person [HSP] scale) among 18 participants (10 females) while viewing
photos of their romantic partners and of strangers displaying positive, negative,
or neutral facial expressions. One year apart, 13 of the 18 participants were
scanned twice. Results: Across all conditions, HSP scores were associated with
increased brain activation of regions involved in attention and action planning
(in the cingulate and premotor area [PMA]). For happy and sad photo condi-
tions, SPS was associated with activation of brain regions involved in awareness,
integration of sensory information, empathy, and action planning (e.g., cingu-
late, insula, inferior frontal gyrus [IFG], middle temporal gyrus [MTG], and
PMA). Conclusions: As predicted, for partner images and for happy facial pho-
tos, HSP scores were associated with stronger activation of brain regions
involved in awareness, empathy, and self-other processing. These results provide
evidence that awareness and responsiveness are fundamental features of SPS,
and show how the brain may mediate these traits.
Introduction
Sensory processing sensitivity (SPS) is proposed to be an
innate trait associated with greater sensitivity (or respon-
sivity) to environmental and social stimuli (e.g., Aron
et al. 2012). Originally measured in human adults by the
Highly Sensitive Person (HSP) scale (Aron and Aron
1997), SPS is becoming increasingly associated with identi-
fiable genes, behavior, physiological reactions, and patterns
of brain activation (Aron et al. 2012). A functionally simi-
lar trait—termed responsivity, plasticity, or flexibility
(Wolf et al. 2008)—has been observed in over 100 nonhu-
man species including pumpkinseed sunfish (Wilson et al.
1993), birds (Verbeek et al. 1994), rodents (Koolhaas et al.
1999), and rhesus macaques (Suomi 2006).
Sensory processing sensitivity is thought to be one of
two strategies that evolved for promoting survival of
the species (Aron and Aron 1997; Wolf et al. 2008). By
being more responsive to their environments, these
more sensitive organisms have an enhanced awareness
of opportunities (e.g., food, mates, and alliances) and
threats (e.g., predators, loss of status, competitors), and
thus may be more ready to respond to emerging situa-
tions. This survival strategy is effective as long as the
benefits of increased sensitivity outweigh the costs (such
as increased cognitive and metabolic demand). In addi-
tion to potential costs, those with the sensitive survival
strategy will always be in a minority as it would cease
to yield special payoffs if it were found in a majority
(Wolf et al. 2008).
580 ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. This is an open access article under the terms of
the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
Humans characterized as high SPS (or HSP) are likely
to “pause to check” in novel situations (Aron and Aron
1997; Aron et al. 2012), show heightened awareness of
and attention to subtle stimuli, and appear to be more
reactive to both positive and negative stimuli (Jagiellowicz
2012). This combination supports a tendency to process
stimuli more elaborately and learn from the information
gained, which may be useful in the present moment and
when applied to future situations. In contrast, those low
in SPS pay less attention to subtle stimuli, approach novel
situations more quickly, are less emotionally reactive, and
behave with less reference to past experiences.
At least two brain imaging studies have examined the
attentional and perceptual aspect of SPS in humans, using
the HSP scale as a measure of SPS. One study asked indi-
viduals to notice subtle differences in photographs of
landscapes and found that those with greater SPS showed
stronger activation in brain regions for visual and atten-
tion processing compared to those low in SPS (Jag-
iellowicz et al. 2011). A second study, by Aron et al.
(2010), compared individuals from East Asia and the
United States and showed that SPS moderates the effect
of culture on neural responses to culturally relevant cog-
nitive tasks. There was a strong cultural difference in the
activation of brain regions associated with attention such
that low-SPS participants showed greater activation when
completing tasks that were inconsistent with their cultural
context. However, among those high in SPS, there was no
cultural difference in brain activation in regions associ-
ated with attention. These findings suggest that high- (vs.
low-) SPS individuals focus on the task itself independent
of other factors.
Studies have also identified genetic polymorphisms’
association with SPS. One of these studies (Licht et al.
2011) found an association with polymorphisms of the
low-expressing, short (S) variant of the repeat length
polymorphism 5-HTTLPR (serotonin transporter, 5-HTT,
linked polymorphic region). There is some evidence that
carriers of the S-allele (either two shorts or the short and
long combination) are more likely to be depressed in
response to stressful life events (Homberg and Lesch
2011). Not surprisingly, since “genetically driven deficient
serotonin transporter (5-HTT) function would not have
been maintained throughout evolution if it only exerted
negative effects” (Homberg and Lesch 2011, p. 513),
increasing research suggests that the S-allele also has
advantages (for a review see Homberg and Lesch 2011).
For example, it has been associated with superior perfor-
mance on perceptual tasks—more risk aversion when
there was a low probability of winning, but greater risk
seeking when there was a high probability of winning;
longer reflection before making difficult choices and bet-
ter performance on a delayed pattern recognition task
(Roiser et al. 2006; Jedema et al. 2009). The role of the S-
allele in a social context has also been studied (e.g., Way
and Gurbaxani 2008; Way and Taylor 2010). For example,
marital partners with the S-allele were more affected after
a marital discussion by their partner’s positive or anxious
prediscussion mood (Schoebi et al. 2012). In another
study of the possible genetics behind SPS, researchers
(Chen et al. 2011) sought to find something closer to the
strong associations between genes and traits that are pre-
dicted by twin studies but not being found with single
gene research. They considered essentially all the genes
(98) with polymorphisms that affect the dopamine sys-
tem, and chose a trait, SPS, “deeply rooted in the nervous
system” (p. 1). Employing a multistep approach (ANOVA
followed by multiple regression and permutation), they
found that 15% of the variance of HSP scale scores were
predicted by a set of 10 loci on seven genes.
Evolutionary theories of SPS are still developing and
vary (e.g., Wolf et al. 2008, 2011; Ellis et al. 2011; Aron
et al. 2012; Pluess and Belsky 2013), but all emphasize
that there are advantages to it, many of them being social.
For example, responsiveness to others’ needs is essential
for stabilizing cooperative relationships and trust in
humans and other species (e.g., McNamara et al. 2009).
Indeed, SPS—whether it is measured by questionnaires,
physiological measures, behavioral observations, or
genetic markers—confers benefits to individuals in
“good-enough” social environments but vulnerability to
negative outcomes in poor ones (e.g., Belsky and Pluess
2009; Pluess and Belsky 2013).
At least two experimental studies relevant to SPS sup-
port the idea that it is associated with responsiveness to
both positive and negative stimuli. In one experiment,
participants were led to believe that they did well or
poorly on a general aptitude test (Aron et al. 2005a, Study
4). Those high (vs. low) on SPS had more negative affect
when they thought they had low scores on the test, but
when they thought they had high scores there was a non-
significant crossover. In another study, Jagiellowicz (2012)
examined the association between SPS (as measured by
the HSP scale) and emotional responses to positive and
negative images from the International Affective Picture
System. High- (vs. low-) SPS individuals rated emotional
pictures (especially positive ones) as significantly more
positive or negative and tended to respond faster to posi-
tives. Also, high- versus low-SPS individuals reporting
positive parenting in early childhood reported more arou-
sal to positive pictures. However, the mechanisms by
which positive (or negative) social experiences may poten-
tiate the effect of SPS on emotional reactivity have not yet
been studied. Moreover, given that SPS is responsive to
both positive and negative social environments, we exam-
ined whether highly sensitive individuals might show
ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. 581
B. P. Acevedo et al. fMRI Study of Sensory Processing Sensitivity
stronger neural responses in predicted brain regions to
both positive and negative social stimuli.
The present study
As briefly reviewed above, SPS theory and research sug-
gest that greater awareness and responsiveness to others’
moods and emotions are central features of being highly
sensitive. However, no study has measured the link
between SPS and neural reactivity in response to others’
emotional states. Thus, the primary goal of this study was
to investigate individuals’ brain activity in response to
close others’ and strangers’ positive and negative facial
expressions as a function of SPS. To accomplish this goal,
we adapted a paradigm used in previous research in
which mothers’ brain activity was measured while viewing
happy and sad facial images of their infants and of others’
infants (Strathearn et al. 2008). Using fMRI we examined
the neural activations of individuals in intimate relation-
ships, who were recruited as part of a larger longitudinal
study on marriage (Acevedo 2014). Participants were
scanned twice approximately 1-year apart to provide a
replication of results.
At Time 1 (T1), we varied two factors in a within-sub-
jects design (a) the target (partner vs. stranger) and (b)
emotional expressions (happy vs. sad). By varying partner
versus stranger photos, we were able to explore whether
brain activations of individuals higher on SPS, as mea-
sured by the HSP scale (Aron and Aron 1997), would be
stronger in regions relevant to responding to emotions of
close others versus strangers; particularly in brain regions
reflecting awareness, empathy, and readiness to act. At
Time 2 (T2), we replicated T1 and included an emotion-
ally neutral facial expression condition. This additional
condition enabled us to examine more directly the extent
to which SPS would be differentially associated with neu-
ral reactivity in response to positive or negative facial
expressions versus neutral ones.
Method
Participants
Participants were recruited by flyers, newspaper, and In-
ternet advertisements as part of a larger study of newly-
weds and engaged couples in the Santa Barbara, CA,
community (Acevedo 2014). All participants provided
informed consent and received payment for their partici-
pation. The study was approved by the human subjects
committees at the University of California, Santa Barbara
(UCSB) and Albert Einstein College of Medicine.
Individuals were screened for eligibility criteria (e.g.,
relationship status, age 22–40 years, nonuse of antidepres-
sants, and fMRI contraindications), medications, surger-
ies, and overall health. Approximately 34% of individuals
screened were excluded for not meeting criteria. No
participant included in the study reported a history of
any disorders (e.g., anxiety, personality disorders, social
disorders) or use of medications that might bias responses
to the HSP scale. In addition, as in other studies, neuroti-
cism was partialed out of the HSP scale scores because
neuroticism is correlated with HSP scale scores (e.g.,
Aron et al. 2005a) and answers to negative questions on
the scale can be shifted in a more negative direction by
high neuroticism. Thus, results reported herein are not
confounded with neuroticism.
Participants completed data collection (fMRI and sur-
veys) at two visits, about 1-year apart. At T1, scanned
participants were 18 (10 women) healthy, right-handed
individuals; age 21–32 years (M=27.50, SD =3.13), in
established relationships (M=4.30 years, SD =3.18),
and had completed roughly 16 years (SD =1.09) of edu-
cation. The ethnic/racial composition of the sample was
72% Caucasian, 17% Asian, and 11% Hispanic. At T2, 13
(7 women) of the original 18 participants completed
fMRI scanning, with age ranging from 22 to 33 years
(M=28.38, SD =3.40); and average relationship lengths
of 5.88 years (SD =2.88).
Questionnaires
Participants completed a battery of questionnaires,
including an 11-item version of the HSP scale (Aron and
Aron 1997), of which the full 27-item measure has been
found to be a unidimensional with alphas of 0.65–0.85
across numerous samples (e.g., Meyer et al. 2005; Benham
2006; Hofmann and Bitran 2007). Sample items include
“Are you easily overwhelmed by things like bright lights,
strong smells, coarse fabrics or sirens close by?” “Do
other people’s moods affect you?” “Do you become
unpleasantly aroused when a lot is going on around
you?” Scores in this study ranged from 1 to 7 (T1:
M=3.97, SD =1.32; T2: M=4.08, SD =1.18). The
mean and distribution of SPS scores in the present sam-
ple were nearly identical to those found in larger studies
of HSPs within normative populations (e.g., Aron and
Aron 1997) and with the 11-item version of the HSP scale
(e.g., Aron et al. 2010). In addition, the correlation
between T1 and T2 HSP scores in the present sample was
strong (r=0.99), indicating high test–retest reliability.
Participants also completed a two-item measure of
neuroticism (negative affectivity) used in previous studies
of SPS (e.g., Aron et al. 2005a; Jagiellowicz et al. 2011)
describing themselves on a scale from 1 (strongly disagree)
to 7 (strongly agree) on the items: (1) anxious, easily
upset and (2) calm, emotionally stable (reverse scored).
582 ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
fMRI Study of Sensory Processing Sensitivity B. P. Acevedo et al.
In the present sample, r
T1T2
=0.82; T1: M=2.72,
SD =1.09; T2: M=2.38, SD =1.09; rwith SPS measure;
T1 =0.28, T2 =0.25; both ns. This measure was
included, as in the previous studies, to provide a control
for negative affectivity, which, if not controlled for, dis-
torts HSP scale scores.
Stimuli
Partner and stranger facial photos
We presented digitized color photographs of participants’
romantic partners and of strangers (control) displaying
positive and negative facial expressions using Presentation
software (Psychological Software Tools, Inc., Pittsburgh,
PA). Strangers’ images were matched to each participant’s
partner by sex, approximate age, ethnicity, and attractive-
ness.
Context-based descriptions
Because context plays a central role in emotion processing
and regulation (e.g., Gross and John 2003), each facial
image was preceded by a corresponding contextual
description such as “This person is feeling very happy
because something wonderful has happened to them” or
“This person is feeling very sad and they are suffering
because something terrible has happened to them.” This
was done to enhance emotion-specific effects and reduce
cognitive ambiguity as suggested by emotion research
experts (e.g., McRae et al. 2011).
Countback task
After each photo (of all four types), participants were
shown a four-digit number and instructed to mentally
count back by 7s. Following Aron et al. (2005b), the
countback task served as an attentional control and to
reduce carry-over effects between stimuli. It is possible
that this task creates stress or negative emotion (Wang
et al. 2005), but such effects should balance out when
comparisons are made across conditions since the same
task was used after all four photo types.
Emotion ratings
While still in the scanner, but after completing the scan-
ning session, participants provided emotion ratings for
each photo they viewed during the experiment. The
instructions read “Now you will see a series of emotion
words. Please rate how you felt while viewing images of
X” (where X is either [a] PARTNER SMILING, [b]
PARTNER FROWNING, [c] STRANGER SMILING, or
[d] STRANGER FROWNING appeared). A series of posi-
tive (e.g., joy) and negative (e.g., sadness) emotion words
appeared on the screen and participants were asked to
make responses via a button response box on a scale from
1(not at all)to4(a great deal).
Attractiveness ratings of photos by independent
raters
All photos were rated for facial attractiveness by indepen-
dent coders (matched to participants by age, sex, and
demographics) to verify that partner and stranger images
did not differ systematically in terms of attractiveness.
Design and procedure
Approximately 1 week prior to scanning participants were
provided with a packet of questionnaires, which they
completed and brought with them to the scanning ses-
sion. Scanning was performed at the Brain Imaging Cen-
ter (BIC) at the University of California, Santa Barbara.
Just prior to scanning, participants were given a verbal
description of the study and instructed to read the con-
textual descriptions, view each photo, and allow them-
selves to think and feel any response it might elicit. Once
participants indicated that they were ready, they were
oriented to the scanner. Correct positioning was con-
firmed via localized anatomical scans. At T1, the fMRI
scanning block consisted of four conditions: partner
happy, partner sad, stranger happy, and stranger sad. At
T2 fMRI scanning, we included two additional condi-
tions: partner neutral and stranger neutral. The condi-
tions were randomized. Each condition included the
following stimuli in sequential order: contextual descrip-
tion (6-s), face image (12-s), and a countback task (12-s).
Each trial was presented randomly six times. Immediately
after scanning, participants provided emotion ratings.
Data acquisition and analysis
MRI scanning was performed using a 3T Siemens (Brain
Imaging Center at the University of California, Santa Bar-
bara, CA) magnetic resonance imaging system with a
NOVA head coil. First, anatomical scans were obtained
followed by a circle localizer. Next, functional images
were obtained and the first four volumes were discarded
to allow for proper calibration. A repetition time TR of
2000-msec was used with a TE of 30-msec, a 90°flip
angle, and a voxel size for functional images of
39393 mm collected in volumes of 30; 3-mm axial
slices (0-mm gap) covering the whole brain.
Data were analyzed using SPM5 (http://www.fil.ion.
ucl.ac.uk/spm). For preprocessing, functional EPI volumes
ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. 583
B. P. Acevedo et al. fMRI Study of Sensory Processing Sensitivity
were realigned to the fist volume, smoothed with a Gauss-
ian kernel of 6 mm, and then normalized to the T1.nii
image template. During normalization, we resliced voxels
to 3 9393 mm. No participant showed movement
greater than 3 mm (whole voxel). After preprocessing, con-
trasts were created (e.g., partner happy vs. stranger happy)
followed by regression analyses examining the associations
between each contrast with HSP (controlling for neuroti-
cism). Analyses were carried out using a mixed effects gen-
eral linear model, with participants as the random-effects
factor and conditions as the fixed effect. Following standard
procedures using the HSP scale (as noted earlier), HSP scale
scores were computed controlling for neuroticism in all
conditions used for brain activation correlations.
Region-of-interest analyses
For all conditions, we utilized regions of interest (ROIs)
based on previous fMRI studies of SPS (e.g., Aron et al.
2010; Jagiellowicz et al. 2011), empathy (Lamm et al.
2011), emotional memory encoding (Murty et al. 2011),
responses to romantic partners (Singer et al. 2004), and
emotional faces (e.g., Aharon et al. 2001; Fan et al. 2011;
Fusar-Poli et al. 2009). A list of ROIs with Talairach coor-
dinates as referenced in seed papers are provided in Table
S1. We converted the Talairach to MNI coordinates to be
consistent with the SPM T1.nii template. We adopted a
false discovery rate (FDR) for multiple comparisons cor-
rection (Genovese et al. 2002) with a threshold of
P≤0.05 and report the P(uncorrected) values as we con-
ducted 63 small volume corrections thus increasing the
likelihood of positive results. The ROIs occupied a 10-mm
radius with a 3-voxel minimum. We used a 3 voxel mini-
mum rather than a larger number to detect small regions
in the brainstem, for example, but also cortical regions of
functionally significant activation are not necessarily as
large as 10 or 15 voxels. Anatomic regions were confirmed
with the Atlas of the Human Brain (Mai et al. 2008).
Exploratory, whole-brain analysis
For each contrast, we also conducted exploratory, whole-
brain analyses applying a threshold of P≤0.001 (uncor-
rected for multiple comparisons) with a spatial extent of
≥15 contiguous voxels.
Results
Behavioral results
Emotion ratings
We conducted a series of paired t-tests to confirm that
our manipulation elicited the intended affective responses.
Results from paired t-tests showed that positive emotion
(e.g., joy) ratings were significantly greater for partner
happy images versus stranger happy images at T1 and T2
(both Ps<0.01). Paired t-tests also showed that partici-
pants reported significantly greater intensity of anxiety,
compassion, fear, love, hurt, and sadness in response to
partner sad images versus stranger sad images at T1 and
T2 (all Ps<0.01). (See Figs. 1, 2 for T2 results. Note that
although there was substantial between-subject variance
for many emotion ratings, the within-subject variance
across targets was much smaller, hence the significant
paired t-test results).
Attractiveness ratings of photos by independent
raters
Attractiveness ratings for the six raters (three females)
showed adequate interrater reliability. T1: female raters
(a=0.71), male raters (a=0.84); T2: female raters
(a=0.62), male raters (a=0.82). There were no signifi-
cant differences in facial attractiveness at T1 (partner
[M=4.84, SD =1.34] vs. stranger images [M=4.86,
SD =0.76], t
42
=0.11, P>0.10) nor at T2 (partner
[M=5.93, SD =1.18] vs. stranger images [M=5.98,
SD =0.96], t
41
=0.36, P>0.10).
Covariation of SPS with neural activity in
response to partners’ and strangers’
emotions
First, we compared neural responses to emotional (happy,
sad) versus neutral expressions for each target (e.g., part-
ner happy vs. neutral; stranger happy vs. neutral). Because
the neutral condition was only included at T2, these
analyses are restricted to T2 data. Tables 1 and 2 show
results for positive emotions and negative emotions,
respectively.
Partner happy versus partner neutral
For the partner happy versus neutral contrast, ROI analyses
showed significant positive associations for greater HSP
scores with brain activations in a number of areas as shown
in Table 1. Bilateral findings were seen in the inferior fron-
tal gyrus (IFG), superior temporal sulcus, and middle
occipital gyrus. Right-hemisphere findings were in the ante-
rior insula (AI), angular gyrus (AG), superior parietal lobe
(SPL), temporoparietal junction (TPJ), middle/superior
temporal cortex, dorsolateral prefrontal cortex (DLPFC),
cingulate cortex/cingulate, premotor area (PMA), presup-
plementary motor area (pSMA), and superior occipital
gyrus/precuneus. Left-hemisphere findings were in the
middle temporal gyrus (MTG), precuneus, and inferior
584 ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
fMRI Study of Sensory Processing Sensitivity B. P. Acevedo et al.
occipital cortex. There were no significant negative associa-
tions or any exploratory findings for this contrast.
Stranger happy versus stranger neutral
ROI analysis showed significant positive associations for
HSP scores with brain activations in response to stranger
happy versus stranger neutral images as shown in Table 1.
Bilateral activations were found in the precentral gyrus;
right-hemisphere activations in the AI, IFG, and MTG;
and left-hemisphere activations in the premotor cortex,
hippocampus, parahippocampal gyrus, and in the area of
the anterior hippocampus/amygdala. Exploratory, whole-
brain analyses showed positive associations in the left-
medial prefrontal cortex (mPFC) and subcallosal cingu-
late. There were no significant negative associations.
Overlapping activations for partner and stranger
happy stimuli
Both the partner happy (vs. neutral) and stranger happy
(vs. neutral) conditions showed activations of the right AI
and IFG in similar regions. Activations of the PMA and
MTG also appeared in both contrasts, but in opposite
hemispheres and in slightly different areas.
Partner sad versus partner neutral
ROI analysis showed significant positive associations for
greater HSP scores with brain activations in response to
partner sad versus neutral images as shown in Table 2.
Bilateral activations were seen in the MTG and superior
temporal sulcus; right-hemisphere activations in the AI,
2.00
3.50
1.25
1.58
3.75 3.25
1.50
2.42
1.00
1.17
1.00
1.83
.00
.50
1.00
1.50
2.00
2.50
3.00
3.50
4.00
4.50
Anxiety Compassion Fear Hurt Love Sadness
Partner Sad Stranger Sad
Figure 2. Postscan emotion ratings. The y-
axis indicates the mean and standard error
for the emotion intensity ratings given by
participants while they were in the scanner
at Time 2 for the partner sad versus
stranger sad condition. Scores based on 1–
4 scale, 1 =not at all and 4 =a great deal.
2.42
3.33
3.50 3.77 3.69 3.83
3.31
3.00
1.83
1.50
1.33
1.62
1.92
1.17
1.00
1.08
.00
.50
1.00
1.50
2.00
2.50
3.00
3.50
4.00
4.50
5.00
Partner Happy Stranger Happy
Figure 1. Postscan emotion ratings. The
y-axis indicates the mean and standard
error for the emotion intensity ratings
given by participants while they were in
the scanner at Time 2 for the partner
happy versus stranger happy condition.
Scores based on 1–4 scale, 1 =not at all
and 4 =a great deal.
ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. 585
B. P. Acevedo et al. fMRI Study of Sensory Processing Sensitivity
anterior intraparietal sulcus, inferior parietal cortex,
DLPFC, cingulate, caudate, premotor cortex, PMA, post-
central gyrus, and claustrum; and no significant left-
hemisphere localized activations. There were no signifi-
cant negative associations or whole brain, exploratory
findings.
Stranger sad versus stranger neutral
ROI analysis showed significant positive associations for
HSP scores with brain activations in response to stranger
sad versus neutral images as shown in Table 2.
Right-hemisphere activations were found in the MTG,
supramarginal gyrus, and the hippocampus/para-hippo-
campus; in the left-hemisphere PMA, cingulate gyrus, and
the thalamus. Whole brain, exploratory analyses showed
negative associations (greater SPS scores associated with
less neural activation) in the right occipital lobe and in
the left MTG.
Overlapping activations for partner and stranger
sad facial expressions
Both the partner sad versus neutral and stranger sad ver-
sus neutral conditions showed activation of the right
MTG. Activation of the PMA also appeared in both con-
trasts, but in opposite hemispheres and in slightly differ-
ent areas.
Table 1. Associations of sensory processing sensitivity with regional brain activity in response to partners’ happy (vs. neutral) and strangers’ happy
(vs. neutral) facial images.
Brain region Left Right
Region-of-interest results xyzP, cluster xyzP, cluster
Partner happy versus partner neutral: positive association
Anterior insula 36 21 6 0.006, 54
Inferior frontal gyrus 42 24 3 0.025, 8 48 27 6 0.001, 86
Angular gyrus 63 51 12 0.023, 17
Superior parietal lobe 36 39 42 0.002, 29
Temporoparietal junction 51 54 21 0.006, 38
Middle temporal gyrus 48 54 9 0.019, 30
Middle/superior temporal cortex 60 61 21 0.010, 39
Superior temporal sulcus 54 54 3 0.038, 65 48 54 9 0.019, 26
Dorsolateral prefrontal cortex 42 39 21 0.008, 42
Cingulate cortex 3 24 42 0.009, 58
Cingulate 6 6 57 0.006, 43
Premotor area 48 6 54 0.002, 23
Presupplementary motor area 6 18 54 0.003, 36
Superior occipital gyrus/precuneus 30 72 39 0.007, 45
Precuneus 15 75 21 0.022, 15
Middle occipital gyrus 51 69 6 0.005, 55 39 75 12 0.005, 41
Inferior occipital cortex 57 66 3 0.011, 44
Stranger happy versus stranger neutral: positive association
Anterior insula/inferior frontal gyrus 27 27 0 0.004, 6
Anterior insula 27 27 6 0.004, 19
Inferior frontal gyrus 27 27 2 0.004, 7
Middle temporal gyrus 51 6 24 0.013, 9
Premotor cortex 33 27 12 0.016, 8
Precentral gyrus 63 3 18 0.005, 27 45 12 24 0.002, 11
Hippocampus 27 915 0.002, 25
Amygdala/anterior hippocampus 27 912 0.002, 5
Whole-brain results
Medial prefrontal cortex 18 30 12 <0.001, 35
Subcallosal cingulate 95412 <0.001, 60
Results are for brain activations associated with greater Highly Sensitive Person scale scores (controlling for neuroticism scores). MNI coordinates
(x,y,z) are at the maximum value for the cluster, which may be elongated in any direction. For ROIs, Pvalues are for small volume correction
with P(unc) <0.05. Cluster =cluster size. For whole-brain results, we applied P<0.001 (uncorrected for multiple comparisons) with a spatial
extent of >15 contiguous voxels. AG, angular gyrus; AI, anterior insula; DLPFC, dorsolateral prefrontal cortex; IFG, inferior frontal gyrus; mPFC,
medial prefrontal cortex; MTG, middle temporal gyrus; PMA, premotor area; pSMA, presupplementary motor area; TPJ, temporoparietal junction.
586 ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
fMRI Study of Sensory Processing Sensitivity B. P. Acevedo et al.
Covariation of SPS with neural activity to
partners’ versus strangers’ emotions
In the next series of analyses, we examined the link
between HSP scores and neural responses to emotions
expressed by partners versus strangers (e.g., partner happy
vs. stranger happy). These analyses were conducted at
both T1 and T2, providing a replication.
Partner happy versus stranger happy at T1
ROI analysis showed significant positive associations for
HSP scores with brain activations for the partner happy
versus stranger happy condition as shown in Table 3, sec-
tion 1. Bilateral activations resulted in the insula, anterior
parietal region, and the PMA/supplementary area; right-
hemisphere activations in the AI, IFG, AG, SPL, BA 5,7/
intraparietal sulcus, parietal operculum, DLPFC, premotor
cortex, superior frontal gyrus, and the primary somato-
sensory cortex, and the ventral tegmental area (VTA)
(MNI: 2, 19, 15, cluster =3, as shown in Fig. 3C);
and left-hemisphere activations in the mPFC and MTG.
There were no significant negative associations or whole-
brain findings for this contrast.
Partner happy versus stranger happy at T2
ROI analyses at T2 replicated activations for the 13 of the
18 individuals scanned at T1 for the partner happy versus
stranger happy contrast in the right hemisphere of the
AI/IFG, AG, anterior and superior parietal regions,
DLPFC, premotor cortex, PMA, and the cingulate; and in
the left hemisphere MTG. Findings replicated at T2 are
indicated by a “*” in Table 3, section 1.
Partner sad versus stranger sad at T1
ROI analysis showed significant positive associations for
HSP scores with brain activations for the partner sad
versus stranger sad contrast as shown in Table 3, section
2. Bilateral activations were found in the insula, PMA,
and cingulate gyrus; right-hemisphere activations in the
SPL, intraparietal sulcus, DLPFC, and the cingulate; and
left-hemisphere activations in the anterior parietal region,
Table 2. Associations of sensory processing sensitivity with regional brain activity in response to partners’ sad (vs. neutral) and strangers’ sad (vs.
neutral) facial images.
Brain region Left Right
Region-of-interest results xyzP, cluster xy z P, cluster
Partner sad versus partner neutral: positive association
Anterior insula 33 18 3 0.038, 10
Anterior intraparietal sulcus 36 39 45 0.029, 8
Inferior parietal cortex 45 27 54 0.012, 19
Middle temporal gyrus 42 66 9 0.019, 20 36 63 3 0.010, 29
Superior temporal sulcus 51 45 15 0.037, 3 51 45 12 0.037, 7
Dorsolateral prefrontal cortex 42 39 21 0.010, 32
Cingulate 6 6 57 0.029, 11
Caudate 9 3 30 0.011, 19
Premotor cortex 45 3 33 0.008, 45
Premotor area 27 3 54 0.014, 14
Postcentral gyrus 48 27 57 0.011, 49
Claustrum 36 15 6 0.016, 10
Stranger sad versus stranger neutral: positive association
Middle temporal gyrus 48 48 6 0.005, 17
Middle temporal gyrus 12 915 0.016, 13
Supramarginal gyrus 39 42 30 0.008, 17
Hippocampus/parahippocampus 33 15 21 0.017, 12
Premotor area 33 27 15 0.029, 14
Cingulate gyrus 18 6 30 0.009, 20
Thalamus 333 3 0.009, 7
Stranger sad versus stranger neutral: negative association
Occipital 3 68 9 <0.001, 52
Middle temporal gyrus 48 48 0 <0.001, 86
Results are for brain activations associated with greater Highly Sensitive Person scale scores (controlling for Neuroticism scores). MNI coordinates (x,y,
z) are at the maximum value for the cluster, which may be elongated in any direction. For ROIs, Pvalues are for small volume correction with P(unc)
<0.05. Cluster =cluster size. AI, anterior insula; DLPFC, Dorsolateral prefrontal cortex; MTG, middle temporal gyrus; PMA, premotor area.
ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. 587
B. P. Acevedo et al. fMRI Study of Sensory Processing Sensitivity
superior frontal gyrus, and the thalamus. As shown in
Table 3, section 3, whole brain, exploratory analyses
revealed negative associations of greater HSP scores with
less neural activation in the right hemisphere of the
lateral orbitofrontal cortex and the IFG.
Partner sad versus stranger sad at T2
ROI analysis showed several replications at T2 for the 13
of the 18 individuals scanned at T1 for the partner sad
versus stranger sad contrast as indicated by a “*”in
Table 3, section 2. Overlapping activations were found in
the left hemisphere insula and superior frontal gyrus;
right hemisphere PMA, cingulate, and the cingulate gyrus.
Negative associations did not replicate at T2. However,
exploratory whole-brain analyses revealed significant acti-
vation of the subcallosal area (MNI coordinates: 12, 39,
3, cluster =9) in association with lower HSP scores.
Common findings across all contrasts
Across all conditions, we found activation of the PMA
and premotor cingulate in association with HSP scores
(controlling for neuroticism).
Discussion
Sensory processing sensitivity is proposed to be an innate
trait associated with greater sensitivity to environmental
and social stimuli (e.g., Aron et al. 2012). Behaviorally it
Table 3. Associations of sensory processing sensitivity with regional brain activity in response to partner versus stranger facial images across time
points.
Brain region
Left Right
xyzP, cluster xyzP, cluster
Partner happy versus stranger happy: positive associations
Insula 33 12 6 0.002, 19 36 21 12 0.003, 41
Anterior insula/inferior frontal gyrus* 45 27 21 0.006*, 29
Angular gyrus* 34 72 28 <0.001*, 22
Anterior parietal region* 27 48 66 0.015, 13 27 48 72 0.010*, 28
Superior parietal lobe* 16 63 63 0.005*, 38
Superior parietal lobe/intraparietal sulcus 33 45 54 0.031, 21
Parietal operculum 52 22 30 0.001, 47
Dorsolateral prefrontal cortex* 36 39 27 0.007*, 17
Medial prefrontal cortex 9 66 17 0.012, 6
Premotor cortex* 54 9 48 0.022*, 18
Premotor/supplementary area* 93 51 0.001, 29 24 3 57 <0.001*, 48
Superior frontal gyrus* 9 9 60 0.006*, 14
Primary somatosensory cortex 48 18 48 <0.001, 19
Primary somatosensory cortex 57 15 42 <0.001, 29
Middle temporal gyrus* 45 69 9 0.027*, 5
Partner sad versus stranger sad: positive associations
Insula 33 18 9 0.019, 29 42 24 12 0.025, 28
Insula* 42 33 21 0.007*, 9
Anterior parietal region 27 48 66 0.006, 7
Superior parietal lobe 12 57 60 0.009, 29
Superior parietal lobe/intraparietal sulcus 27 45 51 0.002, 5
Superior frontal gyrus* 9 18 48 0.011*, 15
Dorsolateral prefrontal cortex 27 45 27 0.002, 45
Premotor area* 63 57 0.001, 34 27 3 54 0.009*, 16
Cingulate* 12 6 60 0.001*, 37
Cingulate gyrus* 4 11 29 0.002, 19 10 3 45 0.002*, 52
Thalamus 321 0 <0.001, 15
Partner sad versus stranger sad: negative association at T1
Lateral orbitofrontal cortex 45 45 6<0.001, 62
Inferior frontal gyrus 30 35 12 <0.001, 40
Results are for brain activations associated with greater Highly Sensitive Person scale scores (controlling for Neuroticism scores). MNI coordinates
(x,y,z) are at the maximum value for the cluster, which may be elongated in any direction. For ROIs, Pvalues are for small volume correction
with P(unc) <0.05. Replications at T2 are indicated by a “*”.AG, angular gyrus; AI, anterior insula; DLPFC, Dorsolateral prefrontal cortex; IFG, infe-
rior frontal gyrus; mPFC, medial prefrontal cortex; MTG, middle temporal gyrus; PMA, premotor area.
588 ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
fMRI Study of Sensory Processing Sensitivity B. P. Acevedo et al.
is characterized by more elaborate processing of stimuli
and, to facilitate this, “pausing to check” before
approaching novel situations. Theory and research suggest
that emotional relevance guides this more extensive pro-
cessing such that socially relevant stimuli tend to evoke
stronger reactions in those higher on the trait. Thus, we
examined individuals’ neural activity in response to per-
ceiving others’ emotional expressions as a function of
SPS. Across two time points, we scanned the brains
of newly married individuals while they viewed photos of
their partners and strangers displaying either happy or
sad, and at T2, also neutral, facial expressions. This
enabled us to investigate whether individuals with greater
SPS (assessed by the HSP scale, the standard measure of
SPS) would show stronger activations in brain regions
reflecting awareness, empathy, and motor control in
response to others’ emotions. Inclusion of different stim-
uli also allowed us to examine whether individuals higher
on SPS would show stronger brain activations to the
emotional displays (a) of close others (vs. strangers) and
(b) for positive (vs. negative or neutral) emotions, as sug-
gested by theory and some self-report studies.
As predicted, greater HSP scores were associated with
stronger activations of brain regions involved in aware-
ness, integration of sensory information, empathy, and
preparation for action in response to emotionally evoca-
tive social stimuli. Our results also supported additional
predictions: we found stronger activations in response to
close others and to positive social stimuli, including acti-
vation in the VTA, a dopamine-rich area well-known for
its involvement in reward processing. These findings are
consistent with research showing that emotional bonds
(A) (B)
(C) (D)
(E) (F)
Figure 3. Images showing brain
activations significantly associated with
higher scores on the Highly Sensitive
Person (HSP) scale scores (controlling for
neuroticism scores) at Time 1 for the
partner happy versus stranger happy
condition in the (A) anterior insula (AI), (B)
primary somatosensory cortex (S1), (C)
ventral tegmental area (VTA), and (D)
dorsolateral prefrontal cortex (DLPFC); and
for the partner sad versus stranger sad
condition in the (E) insula and (F) the
DLPFC.
ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. 589
B. P. Acevedo et al. fMRI Study of Sensory Processing Sensitivity
between actors and perceivers facilitate mutual intention
perception, and those with stronger bonds show greater
intention understanding (e.g., Ortigue and Bianchi-Dem-
icheli 2008). Our results were also in-line with previous
SPS studies showing strong responses to positive stimuli
(Jagiellowicz 2012). It is interesting to note that in our
study we found no evidence of activation in the amygdala
—a brain region that is known to be involved in emo-
tional processing—as a function of SPS in response to
emotional social stimuli. These results suggest that at least
when viewing emotionally evocative photographs, SPS
does not necessarily engage limbic emotional processes
but rather influences preparations to act via higher order
systems involved in awareness, integration of sensory
information, and action planning.
The highly sensitive brain: alert and ready
to respond
Across all possible conditions we found positive associa-
tions with HSP scores (controlling for neuroticism) in the
cingulate and PMA, regions involved in attention and
action planning. These findings are robust, as we varied
the target (partner vs. stranger) and emotional display
(positive, negative, and neutral) of our stimuli, and repli-
cated findings after 1 year for the subset of the original
sample that was rescanned. Also, results in the PMA rep-
licated findings from a previous fMRI study of SPS mea-
suring responses to landscape images (Jagiellowicz et al.
2011).
The cingulate area found in this study was very similar
to that reported in a meta-analysis of 40 empathy studies
(Fan et al. 2011). The cingulate is important for the rec-
ognition of others’ actions, in both humans and other
primates (e.g., Rizzolatti et al. 1996), and in conjunction
with the insula (another area activated in association with
SPS, see below) it appears to be involved in moment-to-
moment awareness (Craig 2009). A review of the studies
on cingulate function suggests that it is an area where
motor control, cognition, and drive (or arousal) interface
(Paus 2001). In the present context, activation of the cin-
gulate may reflect greater attention and alertness in
response to socially relevant stimuli consistent with SPS
theory.
The PMA, also found across all conditions in this study,
is involved in unconscious behavioral control and action
planning (e.g., Cross et al. 2006). It is responsible for
action preparation, guidance, and direct control of move-
ments (Graziano 2006), and through connections with the
PFC, it is key site for behavioral control. Activation of the
PMA in this study is consistent with SPS theory and
research which propose that SPS is characterized by behav-
iors such as “pausing to check” (vs. approaching quickly).
Another notable activation found for many conditions
(for partners and strangers and for both happy and sad
facial expressions) appeared in the MTG—a region that is
important for emotional meaning making (e.g., Murty
et al. 2011) and described as a “semantic hub” for lan-
guage, visual, and auditory processing (e.g., Dronkers
et al. 2004; Binder et al. 2009). Stronger activation of the
MTG in association with greater HSP scores is consistent
with SPS theory and research showing that individuals
higher on the trait display greater awareness and respon-
sivity to a variety of stimuli, including loud noises, bright
lights, strong smells, and others’ moods.
Collectively, the present results support the notion that
SPS is a trait associated with enhanced awareness and
responsiveness to others’ moods as it engages brain sys-
tems involved in sensory information processing and inte-
gration, action planning, and overall awareness. These
findings highlight how the highly sensitive brain mediates
greater attunement and action planning needed to
respond to the environment, particularly relevant social
contexts.
The highly sensitive brain: empathy and
integration of others’ emotions
Across most of our conditions (except stranger sad versus
neutral contrast) we found that HSP scores were posi-
tively associated with activation of the insula, implicated
in limbic functions, sensorimotor integration, and a wide
range of functions including attention, emotion, and self-
referential processing (e.g., Phan et al. 2002; Jabbi and
Keysers 2008; Cauda et al. 2011). Activations in this study
were found in an area similar to that reported in two
meta-analyses of 40 and 32 empathy studies and one
study involving perception of a romantic partner’s pain
(Singer et al. 2004; Fan et al. 2011; Lamm et al. 2011).
The insula shows connectivity with other regions of the
brain associated with emotion detection and interpreta-
tion, such as the IFG (which was found for all HSP asso-
ciations for positive emotion conditions in this study).
The IFG is proposed to be part of a Mirror Neuron Sys-
tem (MNS) (e.g., Iacoboni et al. 1999; Jabbi and Keysers
2008; Van Overwalle and Baetens 2009) that permits
humans to rapidly and intuitively sense others’ goals and
intentions (e.g., Cross et al. 2006; Van Overwalle and
Baetens 2009). Primates’ IFG neurons fire both when they
perform and observe hand actions (e.g., Rizzolatti and
Craighero 2004; Nelissen et al. 2005). Numerous studies
have shown activation of the IFG in the same area for the
observation and execution of movements (e.g., Decety
et al. 1997), suggesting its importance in imitation-learn-
ing and understanding others’ intentions (Gallese and
Goldman 1998). These results suggest that highly sensitive
590 ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
fMRI Study of Sensory Processing Sensitivity B. P. Acevedo et al.
individuals “feel” and integrate sensory information to a
greater extent in response to their close others’ affective
states, in particular positive emotional states (relative to a
nonclose other’s and to neutral affect).
Somewhat similarly, high sensitivity was associated with
stronger activation of the AG in response to five of the
six partner conditions (the exception was the T2 partner
sad versus neutral contrast). AG has been implicated in
self-representation, understanding of metaphors, cogni-
tion (specifically internal dialog), and abstract representa-
tion of the self (e.g., Blanke et al. 2002; Arzy et al. 2006).
Activation of the AG has also been shown in several fMRI
studies of romantic love (e.g., Ortigue et al. 2007; Aceve-
do et al. 2011). Taken together (along with activation of
the IFG), this study suggests how the brain, via brain cir-
cuits important for integration of others’ states and
empathy, mediates the experiences of highly sensitive
individuals as being more responsive to others’ moods.
Furthermore, highly sensitive individuals showed stron-
ger activation in the VTA for the partner happy versus stran-
ger happy contrast, but not for the other contrasts. The VTA
has been shown to be activated in response to several posi-
tive stimuli and in other studies of romantic partners (e.g.,
Aron et al. 2005b; Acevedo et al. 2011). The finding that it is
more active under an emotional condition herein is consis-
tent with the idea that sensitive people are more responsive
to emotional and positive stimuli.
Finally, highly sensitive individuals showed stronger
activation of the DLPFC across most partner contrasts.
The DLPFC is involved in higher order cognitive process-
ing, decision making, and complex tasks. We speculate
that significant activation of the DLPFC, specifically in
response to socially relevant stimuli, reflects the greater
depth and higher order processing (Miller 2000) consis-
tent with behavioral descriptions of high-SPS individual’s
greater conscientiousness and responsiveness to others’
moods (Aron et al. 2012).
Is SPS selective?
SPS may be evolutionary advantageous under some con-
ditions, but it is still metabolically costly, so selective
attention to close others may be a way to conserve
energy. Although SPS is expected to increase response to
environmental stimuli in general (especially socially rele-
vant emotional stimuli), the inclusion of both happy and
sad faces permitted us to test emotional responses more
broadly, and examine the possibility that SPS might be
especially strongly associated with positive emotions,
given previous findings noted in the Introduction.
This study suggests that highly sensitive individuals show
similar patterns of neural activation for partner happy and
sad (vs. neutral) facial expressions, and also for happy
strangers (vs. neutral) in areas implicated in empathy, sen-
sorimotor integration (e.g., the insula and IFG). However,
these activations did not appear in the stranger sad (vs.
neutral) condition. Hence, SPS seems to be a selective trait,
whereby partners’ emotional expressions are given priority.
In addition, stronger brain activation of the insula and IFG
in response to all happy conditions, including the happy
strangers are worth noting, perhaps supporting the particu-
lar susceptibility to positive environments.
When partner and stranger were directly contrasted,
highly sensitive individuals showed stronger brain activa-
tions in brain regions known to be involved in self-other
processing (e.g., the AG) in response to partners’ facial
expressions (including stronger reactions to partners’
happy expressions) than to strangers. When directly com-
paring activations to partner happy versus stranger happy
faces, highly sensitive individuals also showed stronger
activation of regions involved in empathy, self-other pro-
cessing, decision-making, integration of sensory informa-
tion, and action planning (e.g., in the insula, IFG, AG,
SPL, DLPFC, PMA, cingulate, and MTG).
Although the above argues for a difference between
partner and stranger, there is at the same time the inter-
esting result that activation in areas related to imitation
and self-other processing (IFG and AG) was somewhat
similar for the partner happy versus neutral condition
and stranger happy versus neutral (but not for stranger
sad vs. neutral), suggesting a bias toward positive expres-
sions. Greater SPS was also associated with stronger acti-
vation of brain regions involved in attention, empathy,
higher order cognitive processing, and action planning in
response to close others (vs. strangers), and particularly
to their positive emotions (vs. negative and neutral).
Collectively, these findings suggest that SPS may be a
selective strategy and that for some evolutionary reason,
such as conservation of metabolic resources, highly sensi-
tive individuals process information about close others
and positive emotions more thoroughly. Perhaps this
greater response to close others’ positive emotions
explains their unusual susceptibility to positive social
environments (Pluess and Belsky 2013). Whether learned
or innate, individuals with greater SPS appear to be
reducing their reactions to negative emotional informa-
tion that may not be particularly salient, as for strangers
versus close others. This is consistent with behavioral evi-
dence of highly sensitive individuals reporting that they
tend to avoid negative overstimulation (such as loud
sirens, horror movies, and having too much to do at
once) and needing recovery time after viewing arousing
stimuli. Nevertheless, activation of regions involved in
awareness, higher order processing, and action planning
suggest that HSPs are attentive and preparing to respond
to their partner’s needs when happy or sad.
ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. 591
B. P. Acevedo et al. fMRI Study of Sensory Processing Sensitivity
Future Directions and Limitations
Our sample consisted of individuals soon-to-be or recently
married. Thus, responses to partners’ may reflect particu-
larly strong activations, as the early stages of marriage tend
to be emotionally charged, and particularly positive
around the time of the wedding. This may not be indica-
tive of responses to others in general, close others, and
across relationship stages. However, we also examined
responses to strangers’ images and partner’s neutral
images, and data with the same group of individuals
1 year after the first scan, thus providing strong evidence
for the pattern of activations. Nevertheless, future research
may aim to examine SPS across other important relation-
ships (e.g., parent–child), relationship stage, and individu-
als with more diverse socioeconomic status and ethnicity.
Although the present results support existing SPS the-
ory and research, there are limitations. First, as men-
tioned previously, our sample was largely homogenous,
constraining the generalizability of our results to other
populations. Second, the only measure of SPS was the
HSP scale. As more nonself-report measures become
available, it would be important to use these in such
studies. Third, as our postscan emotion ratings were col-
lected after the scanning session (although participants
were still in the scanner), it is possible that emotional
states elicited during the experiment were subject to recall
effects or dampened at the time of inquiry. Fourth, fMRI
research, in general, implies several inferences such that
the labeling of some brain regions as “empathy” areas
oversimplifies the complex neural circuitry probably
involved. However, we attempted to highlight the variety
of functions across some key sites. In addition, as we had
numerous ROIs, for each region we applied small volume
corrections independently. This increases the likelihood of
finding a positive result; therefore, we applied FDR to
each ROI (which corrects for multiple comparisons), but
report the uncorrected Pvalues to acknowledge this limi-
tation. Finally, fMRI studies in general do not demon-
strate that any such region is the cause of an experience
(vs. that the experience is the cause of the activation).
Thus, it is best to be conservative in interpretation of
results provided herein as telling us how the brain creates
responses.
Conclusion
The primary goal of this study was to extend research on
SPS by examining the brain activations engaged in pro-
cessing emotional social stimuli. Using fMRI we measured
the brain activity of participants in response to positive
and negative facial images of their partners and strangers
in two studies, providing a replication. Across all condi-
tions, results showed activation of brain regions involved
in awareness, attention, and action planning (in the cin-
gulate and PMA), replicating results from a previous
fMRI study of SPS measuring responses to landscape
images. Other robust neural activations (appearing in
most conditions) were found in regions implicated in the
integration of sensory information, emotional meaning
making, and empathy. Additional notable results for SPS
were found in regions implicated in self-other processing,
the mirror neuron system, self-awareness, and higher
order cognitive processing. These responses were shown
for both partners and strangers, but also showed some
selectivity for partners and for positive emotions. The
present findings support SPS theory and research suggest-
ing that it is a trait associated with enhanced awareness
and behavioral readiness to respond to salient environ-
mental stimuli, particularly important social situations.
These results highlight how the highly sensitive brain may
mediate greater attunement to others’ and responsiveness
to others’ needs.
Acknowledgments
This research was supported by grants from the National
Science Foundation (0958171) and the UCSB Brain
Imaging Center to Bianca Acevedo. We thank Scott Graf-
ton, Geraldine Acevedo, Lauren Baker, Janet Ferrer, Hao-
lei Fang, Cynthia Gonzales, Alexis Goswitz, Flannery
Rogers, Stephanie O’Keefe, and Jonathan Vogelman for
their assistance.
Conflicts of Interest
None declared.
References
Acevedo, B. (2014) Neural correlates of human attachment:
evidence from fMRI studies of adult pair-bonding. In V.
Zayas and C. Hazan, eds. Bases of adult attachment: from
brain to mind to behavior. Springer, New York, NY.
Acevedo, B., A. Aron, H. Fisher, and L. Brown. 2011. Neural
correlates of long-term intense romantic love. Soc. Cogn.
Affect Neurosci. 7:145–159.
Aharon, I., N. Etcoff, D. Ariely, C. F. Chabris, E. O’Connor,
and H. C. Breiter. 2001. Beautiful faces have variable reward
value: fMRI and behavioral evidence. Neuron 32:537–551.
Aron, E. N., and A. Aron. 1997. Sensory-processing sensitivity
and its relation to introversion and emotionality. J. Pers.
Soc. Psychol. 73:345–368.
Aron, E., A. Aron, and K. M. Davies. 2005a. Adult shyness: the
interaction of temperamental sensitivity and an adverse
childhood environment. Pers. Soc. Psychol. Bull. 31:
181–197.
592 ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
fMRI Study of Sensory Processing Sensitivity B. P. Acevedo et al.
Aron, A., H. Fisher, D. Mashek, G. Strong, H. Li, and L.
Brown. 2005b. Reward, motivation and emotion systems
associated with early-stage intense romantic love. J.
Neurophysiol. 93:327–337.
Aron, A., S. Ketay, T. Hedden, E. N. Aron, H. Markus, and J.
E. Gabrieli. 2010. Temperament trait of sensory processing
sensitivity moderates cultural differences in neural response.
Soc. Cogn. Affect Neurosci. 5:219–226.
Aron, E. N., A. Aron, and J. Jagiellowicz. 2012. Sensory
processing sensitivity: a review in the light of the evolution of
biological responsivity. Pers. Soc. Psychol. Rev. 16:262–282.
Arzy, S., G. Thut, C. Mohr, C. M. Michel, and O. Blanke.
2006. Neural basis of embodiment: distinct contributions of
temporoparietal junction and extrastriate body area. J.
Neurosci. 26:8074–8081.
Belsky, J., and M. Pluess. 2009. Beyond diathesis stress:
differential susceptibility to environmental influences.
Psychol. Bull. 135:885–908.
Benham, G. 2006. The highly sensitive person: stress and
physical symptom reports. Personality Individ. Differ.
40:1433–1440.
Binder, J. R., R. H. Desai, W. W. Graves, and L. L. Conant.
2009. Where is the semantic system? A critical review and
meta-analysis of 120 functional neuroimaging studies.
Cereb. Cortex 19:2767–2796.
Blanke, O., S. Ortigue, T. Landis, and M. Seeck. 2002.
Stimulating illusory own-body perceptions. Nature 419:269–
270.
Cauda, F., F. D’Agata, K. Sacco, S. Duca, G. Geminiani, and
A. Vercelli. 2011. Functional connectivity of the insula in
the resting brain. Neuroimage 55:8–23.
Chen, C., C. Chen, R. Moyzis, H. Stern, Q. He, and H. Li.
2011. Contributions of dopamine-related genes and
environmental factors to highly sensitive personality: a
multi-step neuronal system-level approach. PLoS One 6:
e21636.
Craig, A. D. 2009. How do you feel—Now? The anterior
insula and human awareness. Nat. Rev. Neurosci. 10:59–70.
Cross, E. S., A. Hamilton, and S. T. Grafton. 2006. Building a
motor simulation de novo: observation of dance by dancers.
NeuroImage 31:1257–1267.
Decety, J., J. Grezes, N. Costes, D. Perani, M. Jeannerod, E.
Procyk, et al. 1997. Brain activity during observation of
actions. Influence of action content and subject’s strategy.
Brain 120:1763–1777.
Dronkers, N. F., D. P. Wilkins, R. D. Jr Van Valin, B. B.
Redfern, and J. J. Jaeger. 2004. Lesion analysis of the brain
areas involved in language comprehension. Cognition
92:145–177.
Ellis, B. J., W. T. Boyce, J. Belsky, M. J. Bakermans-Kranenburg,
and M. H. van IJzendoorn. 2011. Differential susceptibility to
the environment: an evolutionary–neurodevelopmental
theory. Dev. Psychopathol. 23:7–28.
Fan, Y., N. Duncan, M. de Greck, and G. Northoff. 2011. Is there
a core neural network in empathy? An fMRI based quantitative
meta-analysis. Neurosci. Biobehav. Rev. 35:903–911.
Fusar-Poli, P., A. Placentino, F. Carletti, P. Landi, P. Allen,
and S. Surguladze. 2009. Functional atlas of emotional faces
processing: a voxel-based meta-analysis of 105 functional
magnetic resonance imaging studies. J. Psychiatry Neurosci.
34:418–432.
Gallese, V., and A. Goldman. 1998. Mirror neurons and the
simulation theory of mind-reading. Trends Cogn. Sci.
2:493–501.
Genovese, C. R., N. A. Lazar, and T. Nichols. 2002.
Thresholding of statistical maps in functional neuroimaging
using the false discovery rate. NeuroImage 15:870–878.
Graziano, M. 2006. The organization of behavioral repertoire
in motor cortex. Annu. Rev. Neurosci. 29:105–134.
Gross, J. J., and O. P. John. 2003. Individual differences in
two emotion regulation processes: implications for affect,
relationships, and well-being. J. Pers. Soc. Psychol. 85:348–
32.
Hofmann, S. G., and S. Bitran. 2007. Sensory-processing
sensitivity in social anxiety disorder: relationship to harm
avoidance and diagnostic subtypes. J. Anxiety Disord.
21:944–954.
Homberg, R. J., and K. P. Lesch. 2011. Looking on the bright
side of Serotonin transporter gene variation. Biol. Psychiatry
69:513–519.
Iacoboni, M., R. P. Woods, M. Brass, H. Bekkering, J. C.
Mazziotta, and G. Rizzolatti. 1999. Cortical mechanisms of
human imitation. Science 286:2526–2528.
Jabbi, M., and C. Keysers. 2008. Inferior frontal gyrus activity
triggers anterior insula response to emotional facial
expressions. Emotion 8:775–780.
Jagiellowicz, J. 2012. The relationship between the
temperament trait of sensory processing sensitivity and
emotional reactivity. Doctoral Dissertation at Stony Brook
University, New York. Available at http://dspace.
sunyconnect.suny.edu/bitstream/handle/1951/59701/
Jagiellowicz_grad.sunysb_0771E_10998.pdf? sequence=1.
Jagiellowicz, J., X. Xiaomeng, A. Aron, E. Aron, C. Guikang, F.
Tingyong, et al. 2011. The trait of sensory processing
sensitivity and neural responses to changes in visual scenes.
Soc. Cogn. Affect Neurosci. 6:38–47.
Jedema, H. P., P. J. Gianaros, P. J. Greer, D. D. Kerr, S. Liu,
and J. D. Higley. 2009. Cognitive impact of genetic variation
of the serotonin transporter in primates is associated with
differences in brain morphology rather than serotonin
neurotransmission. Mol. Psychiatry 15:512–522.
Koolhaas, J. M., S. M. Korte, S. F. De Boer, B. J. Van Der
Vegt, C. G. Van Reenen, H. Hopster, et al. 1999.
Coping styles in animals: current status in behavior
and stress-physiology. Neurosci. Biobehav. Rev. 23:
925–935.
ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. 593
B. P. Acevedo et al. fMRI Study of Sensory Processing Sensitivity
Lamm, C., J. Decety, and T. Singer. 2011. Meta-analytic
evidence for common and distinct neural networks
associated with directly experienced pain and empathy for
pain. NeuroImage 54:2492–2502.
Licht, C., E. L. Mortensen, and G. M. Knudsen. 2011.
Association between sensory processing sensitivity and the
serotonin transporter polymorphism 5-HTTLPR short/short
genotype. Biol. Psychiatry 69:152S–153S.
Mai, J. K., G. Paxinos and T. Voss. 2008. Atlas of the human
brain, 3rd edn. Elsevier Academic Press, New York, NY.
McNamara, M. J., A. P. Stephens, R. S. Dall, and I. A.
Houston. 2009. Evolution of trust and trustworthiness:
social awareness favours personality differences. Proc. Biol.
Sci. 276:605–613.
McRae, K., K. N. Ochsner, and J. J. Gross. 2011. The reason in
passion: a social cognitive neuroscience approach to
emotion regulation. Pp. 186–203 in K. D. Vohs and R. F.
Baumeister, eds. Handbook of self regulation: research,
theory, and applications, 2nd edn. Guilford Press, New
York, NY.
Meyer, B., M. Ajchenbrenner, and D. P. Bowles. 2005. Sensory
sensitivity, attachment experiences, and rejection responses
among adults with borderline and avoidant features. J. Pers.
Disord. 19:641–658.
Miller, E. K. 2000. The prefrontal cortex and cognitive control.
Nat. Rev. Neurosci. 1:59–65.
Murty, V. P., M. Ritchey, R. Adcock, and K. S. LaBar. 2011.
fMRI studies of successful emotional memory encoding: a
quantitative meta-analysis. Neuropsychologia 49:695–705.
Nelissen, K., G. Luppino, W. Vanduffel, G. Rizzolatti, and G.
A. Orban. 2005. Observing others: multiple action
representation in the frontal lobe. Science 310:332–336.
Ortigue, S., and F. Bianchi-Demicheli. 2008. Whyisyourspouse
sopredictable? Connecting mirror neuronsystemandself-
expansion modeloflove. Med. Hypotheses 71:941–944.
Ortigue, S., F. Bianchi-Demicheli, A. F. Hamilton, and S. T.
Grafton. 2007. The neural basis of love as a subliminal
prime: an event-related fMRI study. J. Cogn. Neurosci.
19:1218–30.
Paus, T. S. 2001. Primate anterior cingulate cortex: where
motor control, drive and cognition interface. Nat. Rev.
Neurosci. 2:417–424.
Phan, K. L., T. Wager, S. F. Taylor, and I. Liberzon. 2002.
Functional neuroanatomy of emotion: a meta-analysis of
emotion activation studies in PET and fMRI. NeuroImage
16:331–348.
Pluess, M., and J. Belsky. 2013. Vantage sensitivity: individual
differences in response to positive experiences. Psychol. Bull.
139:901–916.
Rizzolatti, G., and L. Craighero. 2004. The mirror-neuron
system. Annu. Rev. Neurosci., 27:169–192.
Rizzolatti, G., L. Fadiga, V. Gallese, and L. Fogassi. 1996.
Premotor cortex and recognition of motor actions. Brain
Res. Cogn. Brain Res. 3:131–141.
Roiser, J. P., R. D. Rogers, L. I. Cook, and B. J. Sahakian.
2006. The effect of polymorphism at the serotonin
transporter gene on decision-making, memory and executive
function in ecstasy users and controls. Psychopharmacology
188:213–227.
Schoebi, D., B. M. Way, B. R. Karney, and T. N. Bradbury.
2012. Genetic moderation of sensitivity to positive and
negative affect in marriage. Emotion 12:208.
Singer, T., B. Seymour, J. O’Doherty, H. Kaube, R. Dolan, and
C. Frith. 2004. Empathy for pain involves the affective but
not sensory components of pain. Science 303:1157–1162.
Strathearn, L., J. Li, P. Fonagy, and P. Montague. 2008. What’s
in a smile? Maternal brain responses to infant facial cues.
Pediatrics 122:40–51.
Suomi, S. J. 2006. Risk, resilience, and gene x environment
interactions in rhesus monkeys. Ann. N. Y. Acad. Sci.
1094:52–62.
Van Overwalle, F., and K. Baetens. 2009. Understanding
others’ actions and goals by mirror and mentalizing systems.
Neuroimage 48:564–584.
Verbeek, M. M., P. J. Drent, and P. R. Wiepkema. 1994.
Consistent individual differences in early exploratory
behaviour of male great tits. Anim. Behav. 48:1113–1121.
Wang, J., H. Rao, G. S. Wetmore, P. M. Furlan, M.
Korczykowski, D. F. Dinges, et al. 2005. Perfusion
functional MRI reveals cerebral blood flow pattern under
psychological stress. Proc. Natl. Acad. Sci. USA 102:17804–
17809.
Way, B. M., and B. M. Gurbaxani. 2008. A genetics primer for
social health research. Soc. Pers. Psychol. Compass 2:785–816.
Way, B. M., and S. E. Taylor. 2010. Social influences on
health: is serotonin a critical mediator? Psychosom. Med.
72:107–112.
Wilson, D. S., K. Coleman, A. B. Clark, and L. Biederman.
1993. Shy-bold continuum in pumpkinseed sunfish (Lepomis
gibbosus): an ecological study of a psychological trait. J.
Comp. Psychol. 107:250–260.
Wolf, M., S. Van Doorn, and F. J. Weissing. 2008.
Evolutionary emergence of responsive and unresponsive
personalities. PNAS 105:15825–15830.
Wolf, M., G. S. Van Doorn and F. J. Weissing. 2011. On the
coevolution of social responsiveness and behavioural
consistency. Proc. Biol. Sci. 278:440–448.
Supporting Information
Additional Supporting Information may be found in the
online version of this article:
Table S1. Regions of interest (ROIs) used to examine
regional brain activations for an fMRI study of sensory
processing sensitivity.
594 ª2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
fMRI Study of Sensory Processing Sensitivity B. P. Acevedo et al.
