Neuroscience Letters 515 (2012) 157–161
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Neuroscience Letters
jou rn al h om epage: www.elsevier.com/locate/neulet
Common and differential brain responses in men and women to nonverbal
emotional vocalizations by the same and opposite sex
Ji-Won Chun
a,b
, Hae-Jeong Park
b
, Il-Ho Park
c
, Jae-Jin Kim
a,b,∗
a
Institute of Behavioral Science in Medicine, Department of Psychiatry, Yonsei University College of Medicine, 134 Shinchon-dong, Seodaemun-gu, Seoul, Republic of Korea
b
Department of Diagnostic Radiology and Research Institute of Radiological Science, Nuclear Medicine, Yonsei University College of Medicine, 134 Shinchon-dong, Seodaemun-gu,
Seoul, Republic of Korea
c
Department of Psychiatry, Myongji Hospital, Kwandong University College of Medicine, Goyang, Republic of Korea
a r t i c l e i n f o
Article history:
Received 31 December 2011
Received in revised form 6 March 2012
Accepted 12 March 2012
Keywords:
Sex difference
Laughter
Crying
Limbic system
fMRI
a b s t r a c t
Nonverbal emotional vocalizations are one of the most elementary ways of communicating in humans.
We examined the impact of sex differences on neural responses to laughter and crying produced by the
same and opposite sex. Thirty subjects (15 women) underwent functional magnetic resonance imaging
during a sex identification task for laughter, crying, and neutral voices. The parahippocampal gyrus was
involved in both men and women while hearing laughter of the same sex, suggesting greater positive
emotional processing and greater attention toward emotional context in response to laughter of the same
sex than of the opposite sex. The posterior cingulate was involved in both men and women while hearing
crying of the opposite sex, suggesting that empathic processing may occur more in response to crying of
the opposite sex than of the same sex. Furthermore, brain responses to crying of the opposite sex seem
to reflect upon men’s efforts to perform emotional regulation and women’s empathic concerns.
© 2012 Elsevier Ireland Ltd. All rights reserved.
1. Introduction
Emotional communication is an efficient way of regulating
social behavior. Nonverbal emotional vocalizations, one of the most
elemental ways of communication, carry basic emotions and can be
easily decoded [25]. They provide important cues for understand-
ing the feelings of others in social interactions, which is referred
to as empathy and involves both emotion sharing and emotional
regulation [5]. In particular, laughter and crying are crucial ele-
ments exhibiting an emotional state in humans. Other’s laughter
elicits positive feelings from the perceiver and allows people to
share positive experiences with one another [21], whereas crying
is a communicative signal with a high potential to elicit empathy
and emotional support [9]. Functional magnetic resonance imaging
(fMRI) is a technique for detecting the changes in blood oxygenation
that occur in response to neural activities, and is useful for mapping
brain activities underlying emotional behaviors. For example, some
fMRI studies have shown that listening to nonverbal emotional
vocalizations activates the limbic cortices including the amygdala
and insula [24].
∗
Corresponding author at: Department of Psychiatry, Gangnam Severance Hos-
pital, 211 Eonju-ro, Gangnam-gu, Seoul 135-720, Republic of Korea.
Tel.: +82 2 2019 3341; fax: +82 2 3462 4304.
E-mail address: jaejkim@yonsei.ac.kr (J.-J. Kim).
Sex differences in brain responses to emotional stimuli have
been also demonstrated. For example, while processing humor,
women showed a stronger limbic reactivity including the amyg-
dala, insula and anterior cingulate, whereas men used more
evaluative, executive resources [11]. The orbitofrontal cortex and
amygdala were selectively activated to anger cues in women,
whereas a less discriminatory pattern of activation was shown in
men [15]. Men as compared to women showed stronger amyg-
dala activation when viewing fear-inducing pictures, suggesting a
tendency for men to be sensitive to cues of aggression in their envi-
ronment [26]. So far, sex differences in brain responses to nonverbal
emotional vocalizations have been studied only for infant laughter
and crying. In response to them, women showed deactivation in the
anterior cingulate, but men did not, suggesting that women may be
innately more competent in evaluating infant vocalizations [27].
Women’s response preference to infant laughter and crying was
demonstrated by stronger activation in the amygdala and anterior
cingulate in women than in men [23]. Taken together, sex differ-
ences in the emotional processing implicate the primary limbic
structure such as the amygdala and the paralimbic regions such as
the insula, orbitofrontal cortex and anterior cingulate. Given that
the paralimbic cortex is interposed between primary limbic regions
and higher neocortical regions [16], it is worth being focused when
studying the processing of nonverbal emotional vocalizations in
which emotion and cognition may interact.
Emotional vocalizations are important cues in social interaction
not only for infants, but also for adults. The present study ventured
0304-3940/$ – see front matter © 2012 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.neulet.2012.03.038