Social vocalizations can release oxytocin in humans

Abstract

Vocalizations are important components of social behaviour in many vertebrate species, including our own. Less well-understood are the hormonal mechanisms involved in response to vocal cues, and how these systems may influence the course of behavioural evolution. The neurohormone oxytocin (OT) partly governs a number of biological and social processes critical to fitness, such as attachment between mothers and their young, and suppression of the stress response after contact with trusted conspecfics. Rodent studies suggest that OT's release is contingent upon direct tactile contact with such individuals, but we hypothesized that vocalizations might be capable of producing the same effect. To test our hypothesis, we chose human mother-daughter dyads and applied a social stressor to the children, following which we randomly assigned participants into complete contact, speech-only or no-contact conditions. Children receiving a full complement of comfort including physical, vocal and non-verbal contact showed the highest levels of OT and the swiftest return to baseline of a biological marker of stress (salivary cortisol), but a strikingly similar hormonal profile emerged in children comforted solely by their mother's voice. Our results suggest that vocalizations may be as important as touch to the neuroendocrine regulation of social bonding in our species.

Full text

doi: 10.1098/rspb.2010.0567
, 2661-2666 first published online 12 May 2010277 2010 Proc. R. Soc. B
Leslie J. Seltzer, Toni E. Ziegler and Seth D. Pollak
Social vocalizations can release oxytocin in humans
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Social vocalizations can release oxytocin
in humans
Leslie J. Seltzer1,*, Toni E. Ziegler2and Seth D. Pollak1
1
Departments of Psychology, Anthropology, and Waisman Center, University of Wisconsin-Madison,
Madison, WI 53705, USA
2
Wisconsin National Primate Research Center, Madison, WI 53705, USA
Vocalizations are important components of social behaviour in many vertebrate species, including our
own. Less well-understood are the hormonal mechanisms involved in response to vocal cues, and how
these systems may influence the course of behavioural evolution. The neurohormone oxytocin (OT)
partly governs a number of biological and social processes critical to fitness, such as attachment between
mothers and their young, and suppression of the stress response after contact with trusted conspecfics.
Rodent studies suggest that OT’s release is contingent upon direct tactile contact with such individuals,
but we hypothesized that vocalizations might be capable of producing the same effect. To test our hypoth-
esis, we chose human mother –daughter dyads and applied a social stressor to the children, following
which we randomly assigned participants into complete contact, speech-only or no-contact conditions.
Children receiving a full complement of comfort including physical, vocal and non-verbal contact
showed the highest levels of OTand the swiftest return to baseline of a biological marker of stress (salivary
cortisol), but a strikingly similar hormonal profile emerged in children comforted solely by their mother’s
voice. Our results suggest that vocalizations may be as important as touch to the neuroendocrine
regulation of social bonding in our species.
Keywords: oxytocin; stress; vocalizations; female; children; social bonding
1. INTRODUCTION
The strength and quality of relationships between
individuals are critical to fitness in many animals. While
the behaviours that may facilitate the formation and main-
tenance of these relationships are readily observable, such
as grooming in primates or social allofeeding in birds,
their biochemical underpinnings are less evident. Since
natural selection operates upon inter-individual variation
in behavioural phenotype, an understanding of the proxi-
mate mechanisms responsible for eliciting or perpetuating
social behaviour is critical to the study of evolution. One
of the ways in which this can be examined is through an
analysis of the hormones involved in behavioural regulation.
(a)Oxytocin, stress and social support
The neuropeptide oxytocin (OT) plays complex roles in the
central nervous system in establishing maternal/infant and
other types of attachments in a species- and sex-specific
manner (Carter 1998), particularly the development of
trust, pair bonding and recognition of familiar individuals
inrodentssuchasprairievoles(Insel 1997;Lim & Young
2006;Bales et al. 2007;Grippo et al. 2009). This makes
OT a candidate for the study of the neurological bases of
human social behaviour.
There is considerable debate as to how OT operates
to promote relationships and/or regulate stress in the face
of differential social contact in endogenous systems. One
such model holds that physical touch is critical to social
bonding as mediated by OT, as is the familiarity of the indi-
vidual providing contact, especially in the case of touch
between mothers and their offspring (Uvna¨s-Moberg
1996,1997). It appears that this type of tactile contact in
the context of complex social interactions can impact fitness
as well; in vervets, for example, individuals recently groomed
by a conspecific respond more quickly to an alarm call from
that individual than they do to others (Seyfarth & Cheney
1984), and touch between chimpanzees appears to reduce
tension and bolster relationships between individuals who
have recently engaged in agonistic interactions (deWaal
2000;Arnold & Whiten 2001). Individuals with strong
social networks as evidenced by extensive grooming, particu-
larly with their own kin, also appear to have more offspring
than those with weaker ties to others (Silk 2007). While a
relationship between OT and these non-human primate
behaviours has not yet been established, such behaviours
are associated with increases in OT in other mammals
such as rats (Uvna¨ s-Moberg 1998), human adults
(Grewen et al. 2005) and children (Wismer Fries et al. 2005).
This construct, however, may belie the complexity of
how the OT system works. For example, OT also seems
to be related to amelioration of social stress, either directly
or through intermediate hormonal factors; indeed, touch in
rodent species tends to take place after stressful inter-
actions, possibly because OT is released in response to
activation of the hypothalamic– pituitary–adrenal axis
(Jezova
´et al. 1996;Campbell 2008). This in turn may
facilitate comfort-seeking and affiliative bonding, particu-
larly in females who may opt to ‘tend and befriend’
during stressful times rather than engage in fight or flight
responses in order to protect their offspring and themselves
(Ta y l o r et al. 2000). It remains to be seen whether or not
OT is released by stress itself in addition to tactile
contact—or potentially by other types of social interactions.
*Author for correspondence (lseltzer@wisc.edu).
Proc. R. Soc. B (2010) 277, 2661–2666
doi:10.1098/rspb.2010.0567
Published online 12 May 2010
Received 17 March 2010
Accepted 20 April 2010 2661 This journal is q2010 The Royal Society
on September 1, 2010rspb.royalsocietypublishing.orgDownloaded from

(b)Vocalizations and touch—neuroendocrine
similarities?
Although it has been conjectured that human vocalizations
in the form of female speech can release OT (Brizendine
2006), this is yet to be demonstrated. Like touch, however,
vocalizations are used by a number of species to communi-
cate aggression, proceptivity, anxiety and a number of other
emotional states. Little is known ofthe role of OT in the pro-
duction of vocalizations, although new studies reveal that
they are likely to be important. In the soniferous fishes, a
counterpart to OT (isotocin) regulates the expression of
vocal communication of the sexes differently, via strongly
steroid-mediated developmental differences in the brain
(Goodson et al.2003). The neuroanatomy of oxytocinergic
neurons have also been explored in the moustached bat
(Pteronotus parnellii), showing numerous terminations in
and around auditory brain regions (Kanwal & Rao 2002).
In ‘singing’ mice (Scotinomys xerampelinus), OT receptors
are distributed densely in regions of the brain that govern
social memory, such as the hippocampus and amygdala
(Campbell et al.2009). Finally, infant OT knockout mice
show both profound social deficits (Kramer et al.2003)
and produce fewer social vocalizations than their peers
(Takayanagi et al.2005), while also demonstrating both
increased frequency of ultrasonic stress vocalizations and
higher levels of circulating cortisol (Liu et al.2008).
With this in mind, we hypothesized that endogenous OT
might change in response to vocal stimuli after a stressful
event, even in the absence of any other type of social contact.
Partly because humans are the only vertebrate capable of
producing a continuous and precisely timed amount of
comforting vocalizations upon request, we selected
mother– daughter pairs as our test subjects and investigated
whether exposure to socially supportive speech (defined as
the combination of prosodic and linguistic vocal cues)
could produce the same physiological effects as direct
physical contact as assayed via peripheral measures of OT.
The validity of peripheral measurement of OT as it
pertains to such behavioural variables is a contentious
issue requiring further empirical work to resolve. In par-
ticular, some studies suggest that the central and
peripheral OT systems operate independently of one
another to the extent that serum, salivary or urinary OT
measurement cannot reflect central processes in the way
that invasive methods such as cerebrospinal draws can
(Amico et al. 1990;Engelmann et al. 1999;Landgraf &
Neumann 2004;Neumann 2007). Other studies, how-
ever, have begun to reveal that a relationship may exist
between peripheral measures of OT and centrally
mediated behaviour, given changes in peripheral OT
with exposure to different behavioural paradigms in a
number of species, including humans (Carmichael et al.
1987;Modahl et al. 1998;Cushing & Carter 2000;Cushing
et al.2001;Wismer Fries et al. 2005;Seltzer & Ziegler
2007). Such methods allow for non-invasive, real-time
analysis of the ways in which different types of contact
may influence neuroendocrine function, potentially making
them more desirable options for use with human subjects.
2. MATERIAL AND METHODS
(a)Subjects
Our subjects consisted of 61 female children, aged 7– 12 years
(M¼9.4 years, s.d. ¼1.61 years) and their mothers. Only
pre-menarchal children were included to minimize
oestrogen-mediated changes and potential serum contami-
nation of urine associated with menstrual cycling. All
children had reached adrenarche, resulting in relative control
of inter-individual variation in cortisol levels. We selected
post-adrenarche, prepubescent females as test subjects
because: (i) we wished to test whether or not OT was released
after a stressful event in females, with and without tactile and/
or verbal contact from a trusted parent; (ii) OT-mediated
phenomena are best studied in females, anchoring our work
in the existing literature; (iii) we wished to examine whether
or not the role of OT in decreasing stress, if any, was present
before oestrogen cycling commenced with puberty; (iv) we
posited that female children would be more accepting of
warm physical touch and verbal contact with their mothers
than male children owing to cultural norms; and finally
(v) we posited that younger children might not be able to
understand instructions well enough to complete our stress
paradigm successfully. All children with a documented history
of abuse, neglect or prior institutionalization were eliminated
for purposes of this study, but are the subjects of future work.
(b)Experimental protocols
To control for potential circadian fluctuations in hormone con-
centrations, each experimental session began at 16.00 h. After
obtaining consent and assent, children underwent the Trier
Social Stress Test for Children, a procedure which
involves completing a series of timed public speaking and math
performance tasks aloud in front of an audience (Kirschbaum
et al. 1993) and that has been specially modified for use
with children (Gunnar et al. 2009). After experiencing this
stressor, children were randomly assigned to one of the three
experimental conditions. In the direct contact condition (n¼
19) children were reunited with their mothers, who comforted
their child with all sensory stimuli including physical contact. A
second group of children (n¼20) received a telephone call
from their mothers from a different location. By virtue of
physical distance, contact was limited to speech. Moreover,
children in this condition were not allowed to make visual con-
tact with their mothers throughout the course of the
experiment and were provided with a phone in order to control
for the possible influence of non-auditory social cues. A third
group of children (n¼22) participated in a control condition
in which they watched a neutral film for 75 min, but did not
have any contact with their mother of any type until the com-
pletion of the experiment. Children in the first two conditions
had 15 min of contact with their mothers (either total contact
or verbal), after which they watched the same film as the chil-
dren in the control group for 60 min. To index children’s stress
responses, salivary cortisol was collected at arrival, baseline
(30 min after the novelty of arriving at the laboratory but
prior to the stressor), immediately after the stressor but
before experimental contact, and then at 15, 30, 45 and
60 min post-maternal contact, if any. OT was assayed from
urine samples collected at the following time points matched
with salivary cortisol: arrival, baseline, post-stressor 30 min
and post-stressor 60 min. This study was approved by the
Human Subjects Committee/Institutional Review Board at
the University of Wisconsin-Madison.
(c)Hormonal assays
(i) Saliva
Saliva samples were frozen on dry ice after collection and
assayed using a microtitre plate coated with monoclonal
2662 L. J. Seltzer et al. Social vocalizations
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cortisol antibodies. Twenty-five microlitres of each sample
was tested duplicate. Bound cortisol peroxidase was
measured by the reaction of the peroxidase enzyme on the
substrate tetramethylbenzidine. Optical density was read
using ASSAY ZAP data reduction software at 450 nm using a
four-parameter sigmoid minus curve fit. Standard concen-
trations range from 3.00 to 0.012 mg/dl, with intra- and
inter-assay coefficients at 3.35 and 3.75, respectively.
(ii) Urine
Urine samples were snap-frozen on dry ice and subsequently
stored at 2808C. After controlled thawing, urinary samples
were subjected to solid-phase extraction using 1 ml SepPak
C18 cartridges (Waters, cat no. WAT023590). Each column
was pretreated with 1 ml of methanol and then 1 ml of
water before application of 1 ml of urine. A 10 per cent
acetonitrile (ACN) plus 1 per cent trifluroacetic acid (TFA)
wash (1 ml) was then applied, after which the elutant was col-
lected in a clean tube via application of a final 1 ml application
of 80/20 per cent ACN solution with 1 per cent TFA to the
column. Samples were then dried down in a water bath with
air stream and reconstituted in the assay-appropriate buffer
supplied in the 96-well enzyme linked immunosorbent assay
kit used (Assay Designs. Cat no. 901-153; cat no. 901-017
for AVP). Intra- and intercoefficients of variation were deter-
mined by a human urine pool, and oxytocin standards were
used to determine recoveries from the extraction method
(intra-assay/inter-assay coefficient of variation ¼24.2/10.5,
recoveries 92.1 +5.23%, n¼8). Each plate was read on a
Molecular Devices Spectramax 340PC 384 at 405 nm. Data
were analysed by weighted least-squares regression analysis
and reduced by log-logit transformation to yield peptide con-
centrations. Creatinine was also collected with each urine
sample and analysed to correct for variation in water content
(simple creatinine value divided by peptide concentration) to
arrive at pg OT per milligram creatinine (Ziegler et al.
1995). Analysis of variance (ANOVA) was used to compare
the experimental groups with one another at each time
point, with post hoc analysis performed via Tukey’s HSD test.
3. RESULTS
(a)Cortisol
Children in all three conditions exhibited an increase in sali-
vary cortisol from baseline to peak (t
68
¼23.4, p,0.01),
indicating that the social stressor was effective. However,
treatment conditions differed following the stressor
(F
2,52
¼3.99, p,0.02). Both direct, interpersonal contact
and vocal contact alone were effective at reducing children’s
cortisol levels after 1 h, although the condition involving
touch resulted in a more rapid decrease and lower levels of
peak cortisol. Across experimental time, reduction in cortisol
in children engaging in speech only was intermediate
between the other two groups, but by the end of the study
children hearing their mother’s voice and those interacting
with their mothers directly were statistically indistinguishable
(comparable to baseline levels across participants). Children
receiving no social contact exhibited higher levels of cortisol
than the other two groups, even an hour after the stressor was
complete (F
2,52
¼4.475, p,0.02; figure 1).
(b)Oxytocin
As predicted by extant studies, urinar y OT was released in
children following normative comforting by their mothers
involving direct physical contact. We also observed, how-
ever, that girls released conspicuously similar levels of OT
in response to speech with their mothers, even in the
absence of all other types of somatosensory contact.
Both physical and speech-only contact affected
children’s OT levels within 15 min post-stressor and this
effect was maintained as long as 1 h post-stressor
(F
2,42
¼4.54, p¼0.02 and F
2,42
¼3.73, p¼0.02,
respectively). By contrast, OT levels did not change
salivary cortisol (mg/dl)
arrival post-
stressor
15 m
post-
stressor
30 m
post-
stressor
45 m
post-
stressor
1 h
post-
stressor
0 m
baseline
0
0.05
0.10
0.15
0.20
Figure 1. Salivary cortisol levels across experimental time, by maternal contact type. The green arrow represents the onset of
the stressor, and the pink arrow the onset of maternal contact (if any). Both speech and direct contact facilitate a more rapid
return to baseline values than simply resting alone. Diamonds and black line, no contact; triangles and red line, direct contact;
squares and blue line, speech-only.
Social vocalizations L. J. Seltzer et al. 2663
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overall for children who rested alone and received no form
of maternal comforting following the stressor (figure 2).
4. CONCLUSION
This work paves the way for understanding the proximate
mechanisms responsible for the formation or mainten-
ance of social ties in humans, and also for arriving at a
model for how OT operates with respect to stress and
social contact. Simply put, our work emphasizes a
model in which social contact of at least two types (tactile
and vocal) can release OT in female children after a
socially stressful event. The implications of these findings
are twofold: those that are relevant to the evolution of
behaviour and those that are relevant to human society
and early development.
First, this work reveals that vocal cues in humans are
similar to tactile contact as seen in other mammals with
respect to the release of OT. It is, however, important to
view these results in the proper evolutionary context.
OT is a uniquely mammalian hormone, probably having
evolved along with the smooth muscle contractions
associated with parturition and lactation approximately
200 million years ago (Chauvet et al. 1985;Acher et al.
1995). Since the anatomical apparatus necessary for pro-
duction of vocal cues is at least 400 million years old
(Bass et al. 2008), it may be the case that maternal–
offspring touch as a facilitator of OT release in mammals
represents an exaptation from these earlier social signal-
ling systems rather than the other way around.
Alternatively, this may be simply another example of
how this single peptide, which has remained essentially
unchanged throughout the course of mammalian
evolution, can differently influence behaviour owing to
hypervariable OT receptor status within the brains of
different species (Donaldson & Young 2008).
Since each vertebrate clade contains famously vocal
members, language in the sense of human’s unique ability
to use recursive grammar may be unlikely to stand alone
in its ability to release OT. It is at least as likely that pro-
sodic cues are responsible for the observed similarities in
OT release between touch and human speech, and that
non-linguistic social vocalizations facilitate attachment
via the release of OT or related peptides in many other
species. Nonetheless, two grammatically identical
instances of human language differ in meaning depending
on tonality, who is speaking, who is listening and the
nuances of the relationship between them. Focusing on
language alone is the focus of a future study, and it is
our hope that students of vertebrate vocalizations will
choose to focus future work on changes in peripheral
OT release in response to vocal cues in other species.
Second, vocal cues may be a viable alternative to phys-
ical contact for servicing human relationships. The work of
Harry Harlow in the 1970s demonstrates that social iso-
lation, especially early in development, is detrimental to
health and behavioural outcomes in primates, and work
with children who have been institutionalized rather than
reared by their biological parents (or early adoptive
ones), abused or neglected show that this work is probably
translational. Indeed, humans lacking social support from
family and friends have poorer health outcomes than
their better-connected peers (Couzin 2009). Vocal cues
may be able to provide some of the same relief from
these outcomes as direct interpersonal interaction includ-
ing touch. This alternative means of buffering stress
while facilitating social bonds in middle childhood may
underscore the relationship between typical development
and hormonally mediated affiliative bonding in our species.
This study was approved by the Human Subjects
Committee/Institutional Review Board at the University of
Wisconsin-Madison.
We would like to thank Bret Larget for his kind assistance, as
well as John Hawks, Karen Strier, Chuck Snowdon and two
anonymous reviewers for their helpful comments. This
research was supported by the US National Institutes of
Health (MH61285).
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Figure 2. Maternal speech releases oxytocin in girls, in much the same way as direct interpersonal interaction including
comforting touch. Diamonds and black line, no contact; triangles and red line, direct contact; squares and blue line, speech-only.
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