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Social vocalizations can release oxytocin in humans

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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.
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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
Proc. R. Soc. B (2010)
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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
Proc. R. Soc. B (2010)
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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).
REFERENCES
Acher, R., Chauvet, J. & Chauvet, M. T. 1995 Man and
the chimera: selective versus neutral OT evolution. In
0
50
100
150
200
250
urinary oxytocin (pg/mg creatinine)
arrival post-stressor
1 h
post-stressor
15 m
baseline
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.
2664 L. J. Seltzer et al. Social vocalizations
Proc. R. Soc. B (2010)
on September 1, 2010rspb.royalsocietypublishing.orgDownloaded from
OT: cellular and molecular approaches to medicine and research
(eds R. Ivell & J. A. Russell), pp. 615–627. New York, NY:
Plenum Press.
Amico, J. A., Challinor, S. M. & Cameron, J. L. 1990 Pattern
of oxytocin concentrations in the plasma and cerebrosp-
inal fluid of lactating rhesus monkeys (Macaca mulatta):
evidence for functionally independent oxytocinergic path-
ways in primates. J. Clin. Endocrinol. Metab. 71,
1531–1535. (doi:10.1210/jcem-71-6-1531)
Arnold, W. & Whiten, A. 2001 Post-conflict behaviour of
wild chimpanzees (Pan troglodytes schweinfurthii) in the
Budongo Forest, Uganda. Behaviour 138, 649– 690.
(doi:10.1163/156853901316924520)
Bales, K. L., Van Westerhuyzen, J. A., Lewis-Reese, A. D.,
Grotte, N. D., Lanter, J. A. & Carter, C. S. 2007
Oxytocin has dose-dependent developmental effects on
pair-bonding and alloparental care in female prairie
voles. Horm. Behav. 52, 274– 279. (doi:10.1016/j.yhbeh.
2007.05.004)
Bass, A. H., Gilland, E. H. & Baker, R. 2008 Evolutionary
origins for social vocalization in a vertebrate hindbrain–
spinal compartment. Science 321, 417 421. (doi:10.
1126/science.1157632)
Brizendine, L. 2006 The female brain. New York/Cambridge:
Morgan Road Books/Harvard University Press.
Campbell, A. 2008 Attachment, aggression and affiliation:
the role of oxytocin in female social behavior. Biol.
Psychol. 77, 1–10. (doi:10.1016/j.biopsycho.2007.09.
001)
Campbell, P., Ophir, A. G. & Phelps, S. M. 2009 Central
vasopressin and oxytocin receptor distributions in two
species of singing mice. J. Comp. Neurol. 516, 321–333.
(doi:10.1002/cne.22116)
Carmichael, M. S., Humbert, R., Dixen, J., Palmisano, G.,
Greenleaf, W. & Davidson, J. M. 1987 Plasma OT
increases in the human sexual response. J. Clin. Endocrinol.
Metab. 64,2731.(doi:10.1210/jcem-64-1-27)
Carter, C. S. 1998 Neuroendocrine perspectives on social
attachment and love. Psychoneuroendocrinology 23,
779– 818. (doi:10.1016/S0306-4530(98)00055-9)
Carter, C. S., Williams, J. R., Witt, D. M. & Insel, T. R. 1992
Oxytocin and social bonding. Ann. NY Acad.
Sci. 652, 204–211. (doi:10.1111/j.1749-6632.1992.
tb34356.x)
Chauvet, J., Hurpet, D., Michel, G., Chauvet, M. T.,
Carrick, F. N. & Acher, R. 1985 The neurohypophysial
hormones of the egg-laying mammals: identification of
arginine vasopressin in the platypus (Ornithorhynchus ana-
tinus). Biochem. Biophys. Res. Commun. 127, 277– 282.
(doi:10.1016/S0006-291X(85)80155-8)
Couzin, J. 2009 Social science: friendship as a health factor.
Science 323, 454–457. (doi:10.1126/science.323.5913.
454)
Cushing, B. S. & Carter, C. S. 2000 Peripheral pulses of OT
increase partner preferences in female, but not male,
prairie voles. Horm. Behav. 37, 49– 56. (doi:10.1006/
hbeh.1999.1558)
Cushing, B. S., Martin, J. O., Young, L. J. & Carter, C. S.
2001 The effects of peptides on partner preference
formation are predicted by habitat in prairie
voles. Horm. Behav. 39, 48– 58. (doi:10.1006/hbeh.
2000.1633)
deWaal, F. B. M. 2000 Primates: a natural heritage of conflict
resolution. Science 289, 586–590. (doi:10.1126/science.
289.5479.586)
Donaldson, Z. R. & Young, L. J. 2008 Oxytocin, vasopressin,
and the neurogenetics of sociality. Science 322, 900– 904.
(doi:10.1126/science.1158668)
Engelmann, M., Ebner, K., Landgraf, R., Holsboer, F. &
Wotjak, C. T. 1999 Emotional stress triggers
intrahypothalamic but not peripheral release of oxytocin
in male rats. J. Neuroendocrinol. 11, 867– 872. (doi:10.
1046/j.1365-2826.1999.00403.x)
Goodson, J. L., Evans, A. K. & Bass, A. H. 2003 Putative
isotocin distributions in sonic fish: relation to vasotocin
and vocal-acoustic circuitry. J. Comp. Neurol. 462, 1– 14.
(doi:10.1002/cne.10679)
Grewen, K. M., Girdler, S. S., Amico, J. & Light, K. C.
2005 Effects of partner support on resting oxytocin,
cortisol, norepinephrine, and blood pressure
before and after warm partner contact. Psychosom.
Med. 67, 531–538. (doi:10.1097/01.psy.0000170341.
88395.47)
Grippo, A. J., Trahanas, D. M., Zimmerman II, R. R.,
Porges, S. W. & Carter, C. S. 2009 Oxytocin
protects against negative behavioral and autonomic
consequences of long-term social isolation. Psychoneuro-
endocrinology 34, 1542 1553. (doi:10.1016/j.psyneuen.
2009.05.017)
Gunnar, M. R., Wewerka, S., Frenn, K., Long, J. D. &
Griggs, C. 2009 Developmental changes in hypothala-
mus–pituitary– adrenal activity over the transition to
adolescence: normative changes and associations with
puberty. Dev. Psychopathol. 21, 69–85. (doi:10.1017/
S0954579409000054)
Insel, T. R. 1997 A neurological basis of social attachment.
Am. J. Psychiatry 154, 726– 735.
Insel, T. R., Winslow, J. T., Wang, Z. & Young, L. J.
1998 Oxytocin, vasopressin, and the neuroendocrine
basis of pair bond formation. Adv. Exp. Med. Biol. 449,
215–224.
Jezova
´, D., Jura
´nkova
´, E., Mosna
´rova
´, A., Kriska, M. & Skul-
te
´tyova
´, I. 1996 Neuroendocrine response during stress
with relation to gender differences. Acta Neurobiol. 56,
779–785.
Kanwal, J. S. & Rao, P. D. 2002 Oxytocin within auditory
nuclei: a neuromodulatory function in sensory proces-
sing? Neuroreport 13, 2193–2197. (doi:10.1097/
00001756-200212030-00006)
Kirschbaum, C., Pirke, K. M. & Hellhammer, D. H. 1993
The ‘Trier Social Stress Test’: a tool for investigating
psychobiological stress responses in a laboratory
setting. Neuropsychobiology 28, 76–78. (doi:10.1159/
000119004)
Kramer, K. M., Cushing, B. S. & Carter, C. S. 2003 Devel-
opmental effects of oxytocin on stress response: single
versus repeated exposure. Physiol. Behav. 79, 775–782.
(doi:10.1016/S0031-9384(03)00175-6)
Landgraf, R. & Neumann, I. D. 2004 Vasopressin and oxyto-
cin release within the brain: a dynamic concept of
multiple and variable modes of neuropeptide communi-
cation. Frontiers Neuroendocrinol. 25, 150–176. (doi:10.
1016/j.yfrne.2004.05.001)
Lim, M. M. & Young, L. J. 2006 Neuropeptidergic regu-
lation of affiliative behavior and social bonding in
animals. Horm. Behav. 50, 506– 517. (doi:10.1016/j.
yhbeh.2006.06.028)
Liu, H. X., Lopatina, O., Higashida, C., Tsuji, T., Kato, I.,
Takasawa, S., Okamoto, H., Yokoyama, S. & Higashida, H.
2008 Locomotor activity, ultrasonic vocalization and oxyto-
cin levels in infant CD38 knockout mice. Neurosci. Lett. 19,
67–70. (doi:10.1016/j.neulet.2008.09.084)
Modahl, C., Green, L., Fein, D., Morris, M., Waterhouse, L.,
Feinstein, C. & Levin, H. 1998 Plasma oxytocin levels in
autistic children. Biol. Psychiatry 43, 270 277. (doi:10.
1016/S0006-3223(97)00439-3)
Neumann, I. D. 2007 Stimuli and consequences of
dendritic release of oxytocin within the brain.
Biochem. Soc. Trans. 35, 1252–1257. (doi:10.1042/BS
T0351252)
Social vocalizations L. J. Seltzer et al. 2665
Proc. R. Soc. B (2010)
on September 1, 2010rspb.royalsocietypublishing.orgDownloaded from
Seltzer, L. J. & Ziegler, T. E. 2007 Non-invasive measure-
ment of small peptides in the common marmoset
(Callithrix jacchus): a radiolabeled clearance study and
endogenous excretion under varying social conditions.
Horm. Behav. 51, 436–442. (doi:10.1016/j.yhbeh.2006.
12.012)
Seyfarth, R. M. & Cheney, D. L. 1984 Grooming, alliances
and reciprocal altruism in vervet monkeys. Nature 308,
541–543. (doi:10.1038/308541a0)
Silk, J. B. 2007 Social components of fitness in primate
groups. Science 317, 1347–1351. (doi:10.1126/science.
1140734)
Takayanagi, Y. et al. 2005 Pervasive social deficits, but
normal parturition, in oxytocin receptor-deficient mice.
Proc. Natl Acad. Sci. USA 102, 16 096–16 101. (doi:10.
1073/pnas.0505312102)
Taylor, S. E., Klein, L. C., Lewis, B. P., Gruenewald, T. L.,
Gurung, R. A. & Updegraff, J. A. 2000 Biobehavioral
responses to stress in females: tend-and-befriend, not
fight-or-flight. Psychol. Rev. 107, 411– 429. (doi:10.
1037/0033-295X.107.3.411)
Uvna¨ s-Moberg, K. 1996 Neuroendocrinology of the mother-
child interaction. Trends Endocrinol. Metab. 7, 126–131.
(doi:10.1016/1043-2760(96)00036-7)
Uvna¨ s-Moberg, K. 1997 Physiological and endocrine effects
of social contact. Ann. NY Acad. Sci. 807, 146–163.
(doi:10.1111/j.1749-6632.1997.tb51917.x)
Uvna¨ s-Moberg, K. 1998 Oxytocin may mediate the bene-
fits of positive social interaction and emotions.
Psychoneuroendocrinology 23, 819 835. (doi:10.1016/
S0306-4530(98)00056-0)
Wismer Fries, A. B., Ziegler, T. E., Kurian, J. R., Jacoris,
S. & Pollak, S. D. 2005 Early experience in humans is
associated with changes in neuropeptides critical
for regulating social behavior. Proc. Natl Acad. Sci.
USA 102, 17 237 –17 240. (doi:10.1073/pnas.0504
767102)
Ziegler, T. E., Scheffler, G. & Snowdon, C. T. 1995 The
relationship of cortisol levels to social environment and
reproductive functioning in female cotton-top tamarins,
Saguinus oepdipus.Horm. Behav. 29, 407– 424. (doi:10.
1006/hbeh.1995.1028)
2666 L. J. Seltzer et al. Social vocalizations
Proc. R. Soc. B (2010)
on September 1, 2010rspb.royalsocietypublishing.orgDownloaded from
... Although uOT may not replace time course measurements in CSF or plasma (Figure 1), this technique affords us a noninvasive methodology that can be used to ascertain the impact of IN-OT dosage levels on targeted behaviors. For example, researchers have reported pre-post associations between uOT and social outcomes, including children's responding to vocal, nonverbal, and physical comfort, men's visual search for infant and adult faces, and the relationship anxiety or parenting stress among mothers [37][38][39]. Whereas a handful of publications have included measures of both uOT and pOT, results have been inconsistent. For example, while social and behavioral outcomes have been associated with both uOT and pOT levels in some studies of typical development and ASD [37,[39][40][41], research with AN participants has demonstrated poor correspondence between OT levels collected via plasma and urine (e.g., Hoffman et al., 2012) [36]. ...
... Whereas a handful of publications have included measures of both uOT and pOT, results have been inconsistent. For example, while social and behavioral outcomes have been associated with both uOT and pOT levels in some studies of typical development and ASD [37,[39][40][41], research with AN participants has demonstrated poor correspondence between OT levels collected via plasma and urine (e.g., Hoffman et al., 2012) [36]. Further, studies that compare pOT with uOT levels directly to assess quality of measurement are lacking. ...
... In order to account for variability in participants' daily intake of fluids, we first measured levels of creatinine in each urine sample and then adjusted for the hormonal concentration ([OT]/[creatinine]), yielding uOT levels reported as the OT-to-creatinine ratio (pg/mg creatinine). Enzyme-linked immunosorbent assay (ELISA) procedures were implemented [49] using ELISA kits (Assay Designs, Inc./Enzo Life Sciences, Ann Arbor, MI, USA) as described previously [39,[50][51][52]. ...
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Oxytocin (OT), a mammalian neurohormone associated with social cognition and behavior, can be administered in its synthetic form intranasally (IN) and impact brain chemistry and behavior. IN-OT shows potential as a noninvasive intervention for disorders characterized by social challenges, e.g., autism spectrum disorder (ASD) and anorexia nervosa (AN). To evaluate IN-OT’s efficacy, we must quantify OT uptake, availability, and clearance; thus, we assessed OT levels in urine (uOT) before and after participants (26 ASD, 7 AN, and 7 healthy controls) received 40 IU IN-OT or placebo across two sessions using double-blind, placebo-controlled crossover designs. We also measured uOT and plasma (pOT) levels in a subset of participants to compare the two sampling methods. We found significantly higher uOT and pOT following intranasal delivery of active compound versus placebo, but analyses yielded larger effect sizes and more clearly differentiated pre–post-OT levels for uOT than pOT. Further, we applied a two-step cluster (TSC), blinded backward-chaining approach to determine whether active/placebo groups could be identified by uOT and pOT change alone; uOT levels may serve as an accessible and accurate systemic biomarker for OT dose–response. Future studies will explore whether uOT levels correlate directly with behavioral targets to improve dosing for therapeutic goals.
... In humans, uOT has been associated with perceptions of a romantic partner's bonding behavior, regardless of gender (Algoe et al., 2017), and with performance on a facial visual search task in men (Saito et al., 2014). In children, a mother's touch and speech after a stressful event increased uOT while decreasing salivary cortisol (Seltzer et al., 2010). Interestingly, in mothers, uOT was higher after interacting with other people's children compared to their own children, perhaps due to oxytocin's role in the onset-rather than maintenance-of maternal behavior, or perhaps simply due to a novelty effect (Bick and Dozier, 2010). ...
... Even when extensive validation work has been conducted (e.g. Seltzer et al., 2010;, assessment of potential false-positive signal has not been possible, lacking a "ground truth" (i.e. known concentrations). ...
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Oxytocin has become a popular analyte in behavioral endocrinology in recent years, due in part to its roles in social behavior, stress physiology, and cognition. Urine samples have the advantage of being non-invasive and minimally disruptive to collect, allowing for oxytocin measurements even in some wild populations. However, methods for urinary oxytocin immunoassay have not been sufficiently optimized and rigorously assessed for their potential limitations. Using samples from oxytocin knockout (KO) and wildtype (WT) mice, we find evidence of considerable interference in unextracted urine samples, with similar distributions of measured oxytocin in both genotypes. Importantly, although this interference can be reduced by a reversed-phase solid-phase extraction (SPE), this common approach is not sufficient for eliminating false-positive signal on three immunoassay kits. To better understand the source of the observed interference, we conducted epitope mapping of the Arbor Assays antibody and assessed its cross-reactivity with known, biologically active fragments of oxytocin. We found considerable cross-reactivity (0.5-52% by-molarity) for three fragments of oxytocin that share the core epitope, with more cross-reactivity for longer fragments. Given the presence of some cross-reactivity for even the tripeptide MIF-1, it is likely that many small protein metabolites might be sufficiently similar to the epitope that at high concentrations they interfere with immunoassays. We present a new mixed-mode cation-exchange SPE method that minimizes interference-with knockout samples measuring below the assay's limit of detection-while effectively retaining oxytocin from the urine of wildtype mice. This method demonstrates good parallelism and spike recovery across multiple species (mice, dogs, sifakas, humans). Our results suggest that immunoassays of urine samples may be particularly susceptible to interference, even when using common extraction protocols, but that this interference can be successfully managed using a novel mixed-mode cation exchange extraction. These findings imply that previous conclusions based on urinary oxytocin measurements-especially those involving unextracted samples-may need to be reassessed.
... In fact, one study found that TMC generates the release of the same negligible amount of oxytocin, a neurotransmitter associated with a soothing, relaxing feeling of high connection quality, as no interaction at all. Even the voice sharing associated with telephone interaction yields significantly higher oxytocin release than the decontextualized medium of TMC (Seltzer, Prososki, et al., 2012;Seltzer et al. 2010). Perhaps for this reason, there is a "negative affective bias" associated with TMC such that when an organizational member intends for an electronic message to be positive in emotional tone, it is most often interpreted by the receiver as emotionally neutral. ...
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Teleworking experienced exponential growth worldwide during the Covid-19 lockdown. It is very likely that once the limitations for travelling and gathering are over, an important share of the work of organizational members will still be done remotely. We offer a new set of considerations for employees that communicate remotely via text-based technology-mediated communication (TMC) by focusing on the emotional labor challenges associated with TMC and how these challenges influence the connection quality of workplace relationships. We also delineate the mediating effects of two outcomes of TMC, decreased co-presence and informational and interactional demands, in this process. We build on previous literature, especially Walther’s (1996) triadic theory of impersonal/interpersonal/hyperpersonal TMC, to support our theoretical assertions. We develop specific propositions and a theoretical model related to the mediating effects of decreased co-presence, informational and interactional demands, and emotional labor on the link between text-based technology-mediated communication (TMC) and the connection quality of workplace relationships.
... In addition, studies sometimes measure the two hormones in different matrices (e.g. Ditzen et al., 2007;Seltzer et al., 2010;Pierrehumbert et al., 2012;Engert et al., 2016) and/or at different time frames following the stressor (e.g. Neumann et al., 1998;Pierrehumbert et al., 2012;Engert et al., 2016), making it difficult to compare hormonal responses within and between studies. ...
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Animals respond to inherently rewarding or punishing stimuli with changes in core affective states, which can be investigated with the aid of appropriate biomarkers. In this study we evaluate salivary cortisol (sCORT) and salivary oxytocin (sOXT) concentrations under baseline conditions and in response to two negatively- and two positively-valenced social challenges in 75 young pigs (Sus scrofa domesticus), housed and tested in eight social groups. We predicted that: (1) Relative to baseline, weaning and brief social isolation would be associated with increases in sCORT, due to psychosocial stress, and reductions in sOXT, due to a lack of opportunities for social support; and (2) Opportunities for social play, and reunions with group members after a separation would be associated with weaker sCORT responses, and increases in sOXT concentrations compared to baseline and to negative social challenges. Testing and sample collection occurred between 28 and 65 days of age and involved a within-subject design, in which every subject was sampled multiple times in neutral (baseline), negative and positive social contexts. We also recorded behavioral data and measured rates of agonism, play and affiliative interactions in the different contexts, prior to saliva sampling. As expected, negative social challenges were associated with robust cortisol responses. Relative to baseline, pigs also had higher sCORT responses to positive social challenges, although these differences were only significant during reunions. Salivary oxytocin concentrations did not differ between the different social conditions, although sOXT was lowest during the brief social isolation. Behavioral analyses confirmed predictions about the expected changes in social interactions in different social contexts, with increases in agonism following weaning, increases in coordinated locomotor play in the play context and high rates of affiliative interactions during reunions. Relative sCORT reactivity to different contexts may reflect the intensity of emotional responses, with greater increases occurring in response to challenges that involve more psychosocial stress. Our results suggest that sOXT is not a reliable indicator of emotional valence in pigs, although more research is needed to characterize sOXT responses to various challenges with and without access to social support.
... In sum, oxytocin modulates attention orienting responses to external contextual cues, amplifying the motivational salience of relevant others and facilitating any cooperative behavior involving them (Alaerts et al., 2021). Both physical touch (Feldman et al., 2010) and social vocalizations with relevant others (Seltzer et al., 2010) release oxytocin in humans improving their engagement in collective actions. ...
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What makes physical and digital communities different? In this paper, I will attempt to answer this question using recent research findings from social and cognitive neuroscience related to social networks and collective intentionality. Physical communities are born in places. And places activate different “we-mode” neurobiological and cognitive processes – behavioral synchrony, joint attention, intentional attunement, inter-brain synchronization, etc.- that generate cohesive social networks composed of individuals who can be very different from each other. Digital technologies, by removing the physical boundaries that define a place, allow greater freedom in the behavior of individuals and the selection of community. At the same time, however, the lack of physical co-presence of community members significantly reduces their possibility of activating “we-mode” cognitive processes and their overall level of social motivation. For this reason, digital communities are communities of like-minded individuals, based on common interests and shared knowledge (communities of practice).
... Over the last two decades, research has shown that singing can promote physical and mental health in individuals in a low-cost, non-pharmocological, inclusive, collaborative, embodied, and creative manner, offering a wide raft of biopsychosocial benefits Hancox, 2001, 2010;Dingle et al., 2019;Heydon et al., 2020). Group singing in diverse health and social contexts has been associated with enhanced wellbeing and improved quality of life (Daykin et al., 2018;Campbell et al., 2021); reduction in the stress hormone cortisol (Fancourt et al., 2016) and increase in the comforting hormone oxytocin (Seltzer et al., 2010); enhanced empathy, trust and social bonding (Pearce et al., 2016); regulated breathing and heart rate and a calmer nervous system (Kang et al., 2018); spiritual and communal experience affording transcendence (Camlin et al., 2020); reduction in loneliness (Dingle et al., 2013); and in new and expectant mothers, increased maternal bonding, alleviation of symptoms of depression and social connectedness (Fancourt and Perkins, 2018a,b). Further, as the work of Phelan demonstrates, singing or chanting, across cultures (Phelan, 2017b), has been recognized as a healing and nurturing activity that holds diverse peoples and generations together, recognizing differences while appreciating shared understandings and meanings of spirituality. ...
Article
Plain language summary: How can songwriting show us the meaning of music and language for health and wellbeing in culturally and linguistically diverse mothers? This article examines the artistic processes in music-cum-health workshops involving new and expectant mothers and their midwives. The voices of the mothers of colour have been silenced historically and systemically. To give them social justice in a health context, singing is a powerful tool and songwriting links this tool to useful health messages. Through this article, the formation of a song on the placenta, a key part of the womb in childbearing, is traced through the stories of a music facilitator, a mother and a midwife. The storying highlights the importance of artistic processes for understanding the person within and their cultural identity. The article argues that cultural understanding of the participants in such arts-in-health programmes is important for socially just models of health care for those at the margins. Summary: From being instrumentalized as interventions that are 'administered' with an aim to garner health outcomes, art-based participatory approaches are now recognized as capable of activating culturally founded wellbeing in individuals. Through this article, I propose that as the focus shifts from what art does for health to what art means for a healthy life, the cultural vitality inherent in individuals and societies can be better championed in arts-in-health discourses. I discuss the artistic processes in singing and songwriting in a perinatal context involving mothers from culturally and linguistically diverse backgrounds and their midwives. I argue for lenses to better understand the role of cultural practices in health research involving migrant and refugee communities. Using narrative inquiry, I trace intersecting trajectories wherein the storied life of a coloured mother is intercepted by that of a midwife, and of myself, a coloured female mother-researcher and facilitator. At the intersection emerges a song, as a process and product. This article advances that it is when artmaking processes are centred that the voices from the margins become heard, and it is when their voices are amplified that health research design becomes equitable and ethically sound.
... Our results here suggest that children's immune system may not respond to acute stress, in comparison to adolescents, although their self-perceived stress or their HPA axis may (Marques-Feixa et al., 2021). Interestingly, the functioning of biological systems are known to be mediated by both intrinsic and environmental factors (Seltzer et al., 2010). Accordingly, Ulmer-Yaniv et al., (2018) supports that during early infancy, children's immune system regulation relies on maternal health and interaction rather than on other environmental signals. ...
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Background Mucosal secretory immunoglobulin A (s-IgA) is an antibody protein-complex that plays a crucial role in immune first defense against infection. Although different immune biomarkers have been associated with stress-related psychopathology, s-IgA remains poorly studied, especially in youth. Objectives The present study investigated how s-IgA behaves in front of acute psychosocial stress in children and adolescents, including possible variability associated with developmental stage and history of childhood maltreatment (CM). Methods 94 children and adolescents from 7 to 17 years (54 with a current psychiatric diagnostic and 40 healthy controls) drawn from a larger Spanish study were explored (EPI-Young Stress Project). To assess biological reactivity, participants provided five saliva samples during an acute laboratory-based psychosocial stressor, the Trier Social Stress Test for Children (TSST-C). Samples were assayed for s-IgA, as well as for cortisol. Pubertal development was ascertained by Tanner stage and CM following TASSCV criteria. Results We observed s-IgA fluctuations throughout the stressor, indicating the validity of TSST-C to stimulate s-IgA secretion (F(4,199)=6.200, p<.001). Although s-IgA trajectories followed a reactivity and recovery pattern in adolescents, children exhibited no s-IgA response when faced with stress (F(4,197)=3.406, p=.010). An interaction was found between s-IgA and CM (F(4,203)=2.643, p=.035). Interestingly, an interaction between developmental stage, CM history and s-IgA reactivity was identified (F(12,343)=2.036, p=.017); while children non-exposed to maltreatment exhibited no s-IgA changes to acute stress, children with a history of CM showed a similar response to adolescents, increasing their s-IgA levels after the psychosocial stressor. Conclusion Acute psychosocial stress stimulates s-IgA secretion, but only after puberty. However, children with a history of maltreatment exhibited a response resembling that of adolescents, suggesting an early maturation of the immune system. Further studies are needed to clarify the validity of s-IgA as an acute stress biomarker, including additional measures during stress exposure.
... This hormone is necessary for creating and shaping human relations, it not only determines the relationship between the child and the mother, but also affects the feelings of closeness and attachment between partners, as level of oxytocin rises when they touch, kiss and hug each other, it strengthens the bond, a sense of intimacy, trust and closeness, called the " love hormone" [103]. It helps in developing pregnancy, maternal behaviors for woman and man, and any stress response in children is mitigated by the touch or voice of the mother [104], in male reproductive physiology (playing a role in inducing erections in sperm release, its movement (transport) and production of testosterone by the testes [105,106]). ...
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The article presents the benefits of the interdisciplinary science behind the revolutionary designed neuroarchitecture system and its role in improving the quality of life and well-bing of inhabitants, leaders, heroes, astronauts, on the example of Vinci Power Nap® - Dream’s Space®. The author examines its impact on reducing stress and anxiety levels, helping to prevent and treat depression, trauma and PTSD, also as a tool to support health, sleep, relaxation, alertness, increase productivity, education, focus, sense of safe and happiness, based on wide-ranging, multidisciplinary, objective and subjective in-depth pilot studies on traumatized people and surveyed groups of stressed corporate employees, international students and people with depression from psychiatric clinic. Research shows that this type of design can create a microgravity experience and also relaxing the Zero Gravity Position with gravitational pressure on the skin, which together with the force of inertia and harmonic oscillation motion create aid for the patency of the lymphatic system and can be helpful in protection of newborns from cot death. A specially designed environment allows all six senses to be soothed simultaneously, helping to ensure calm and balance in homeostasis, allows in natural way to lower cortisol levels, increase oxytocin, serotonin, vagus nerve activity, etc, leading to the fast mental and physical regeneration, also improving the immune system. Keywords: Neuroarchitecture Space; Stress Reduction, Trauma; Depression; PTSD; Cot Death; Regeneration; Microgravity; Immune System; Well- being
... Most of what we know about the role of oxytocin in acute social interactions comes from assessments of endogenous oxytocin concentrations measured in peripheral fluids (blood, saliva, or urine) or behavior measured following intranasal administration of (synthetic) oxytocin. Increases in endogenous oxytocin concentrations have been measured in the context of affiliative interactions, including receiving social support after stress [54], sharing gaze and interacting with dogs [55,56], and moving together in synchrony [57]. Endogenous oxytocin concentrations have also been found to predict individual differences in social functioning across children with and without autism [58]. ...
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Significant clinical improvement is often observed in patients who receive placebo treatment in randomized double-blind placebo-controlled trials. While a proportion of this “improvement” reflects experimental design limitations (e.g., reliance on subjective outcomes, unbalanced groups, reporting biases), some of it reflects genuine improvement corroborated by physiological change. Converging evidence across diverse medical conditions suggests that clinically-relevant benefits from placebo treatment are associated with the activation of brain reward circuits. In parallel, evidence has accumulated showing that such benefits are facilitated by clinicians that demonstrate warmth and proficiency during interactions with patients. Here, we integrate research on these neural and social aspects of placebo effects with evidence linking oxytocin and social reward to advance a neurobiological account for the social facilitation of placebo effects. This account frames oxytocin as a key mediator of treatment success across a wide-spectrum of interventions that increase social connectedness, thereby providing a biological basis for assessing this fundamental non-specific element of medical care.
Thesis
The majority of voices encountered in everyday life belong to people we know, such as close friends, relatives, or romantic partners. However, research to date has overlooked this type of familiarity when investigating voice identity perception. This thesis aimed to address this gap in the literature, through a detailed investigation of voice perception across different types of familiarity: personally familiar voices, famous voices, and lab-trained voices. The experimental chapters of the thesis cover two broad research topics: 1) Measuring the recognition and representation of personally familiar voice identities in comparison with labtrained identities, and 2) Investigating motivation and reward in relation to hearing personally valued voices compared with unfamiliar voice identities. In the first of these, an exploration of the extent of human voice recognition capabilities was undertaken using personally familiar voices of romantic partners. The perceptual benefits of personal familiarity for voice and speech perception were examined, as well as an investigation into how voice identity representations are formed through exposure to new voice identities. Evidence for highly robust voice representations for personally familiar voices was found in the face of perceptual challenges, which greatly exceeded those found for lab-trained voices of varying levels of familiarity. Conclusions are drawn about the relevance of the amount and type of exposure on speaker recognition, the expertise we have with certain voices, and the framing of familiarity as a continuum rather than a binary categorisation. The second topic utilised voices of famous singers and their “super-fans” as listeners to probe reward and motivational responses to hearing these valued voices, using behavioural and neuroimaging experiments. Listeners were found to work harder, as evidenced by faster reaction times, to hear their musical idol compared to less valued voices in an effort-based decision-making task, and the neural correlates of these effects are reported and examined.
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Since de Waal & van Roosmalen (1979) rst documented the occurrence of reconciliation between former opponents in captive chimpanzees, the study of the post-conn ict behaviour of primates has provided valuable information about some of the details of primate social organisation. The vast majority of these studies have been carried out on captive subjects and it has been assumed that these ndings are representative of wild primates. We set out to investigate whether this was true for the Sonso community of wild chimpanzees (Pan troglodytes schweinfurthii) of the Budongo Forest, Uganda, using controlled procedures comparable with those used in captive studies. We found that these chimpanzees were much less likely to reconcile than their captive counterparts. Only one dimension of relationship quality had an effect on the likelihood of reconciliation. Individuals which were highly compatible, in terms of time spent af liating, reconciled con icts more often than those with weak relationships. Captive chimpanzees have also been shown to 'console' one another (de Waal & van Roosmalen, 1979; de Waal & Aureli, 1996), where uninvolved bystanders initiate af liative contacts with victims of aggression. This study did not con rm that consolatory behaviour was characteristic of wild chimpanzee post-conn ict behaviour. Nor did these chimpanzees use explicit gestures during post-con ict interactions as they have been shown to do in two out of three captive studies. We conclude that the post-con ict behaviour of 1) Corresponding author; e-mail address: ka11@st-andrews.ac.uk 2) We thank Prof. Vernon Reynolds, the staff of the Budongo Forest Project, and J. Kakura, in particular, for his assistance in the eld. We are grateful to Filippo Aureli and one anonymous reviewer for detailed comments on an earlier version of this paper.
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Cortisol levels were examined in 17 cotton-top tamarin monkeys (Saguinus oedipus) to determine: (1) if first-morning void urine sampling could be used as a noninvasive method for monitoring cortisol excretion. (2) if capture and bleeding were associated with changes in urinary cortisol levels, (3) the relative cortisol levels in reproductively active and reproductively suppressed females, and (4) the relationship between cortisol levels and changes in social condition in cotton-up tamarins. Mean urinary cortisol levels during ovarian cycling did not differ between captured and bled females and undisturbed females. Mean cortisol levels were significantly lower in females who were housed in their natal groups and reproductively suppressed than in the same females when they were removed and placed adjacent to a novel male and ovarian cycling began. For all females, mean cortisol levels were higher during the periovulatory period than during the nonperiovulatory period of the ovulatory cycle, with mean cortisol levels higher in newly cycling females than in long-term cycling females. No differences were found in mean cortisol levels between long-term cycling females and prepubertal females and postpubertal natal females. Cortisol levels from long-term cycling females were much lower than during the first two to three ovarian cycles occurring in newly cycling female tamarins, during the last part of pregnancy, and during the first 6 weeks postpartum. These data provide evidence that (1) suppression of ovarian cycling in postpubertal females remaining in their natal family is not associated with stress-induced changes in cortisol levels. (2) cortisol levels are not strictly tied to reproductive condition, and (3) social change may be reflected in cortisol elevation.
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The macroevolutionary events leading to neural innovations for social communication, such as vocalization, are essentially unexplored. Many fish vocalize during female courtship and territorial defense, as do amphibians, birds, and mammals. Here, we map the neural circuitry for vocalization in larval fish and show that the vocal network develops in a segment-like region across the most caudal hindbrain and rostral spinal cord. Taxonomic analysis demonstrates a highly conserved pattern between fish and all major lineages of vocal tetrapods. We propose that the vocal basis for acoustic communication among vertebrates evolved from an ancestrally shared developmental compartment already present in the early fishes.
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Social impairments are central to the syndrome of autism. The neuropeptide oxytocin (OT) has been implicated in the regulation of social behavior in animals but has not yet been examined in autistic subjects. To determine whether autistic children have abnormalities in OT, midday plasma samples from 29 autistic and 30 age-matched normal children, all prepubertal, were analyzed by radioimmunoassay for levels of OT. Despite individual variability and overlapping group distributions, the autistic group had significantly lower plasma OT levels than the normal group. OT increased with age in the normal but not the autistic children. Elevated OT was associated with higher scores on social and developmental measures for the normal children, but was associated with lower scores for the autistic children. These relationships were strongest in a subset of autistic children identified as aloof. Although making inferences to central OT functioning from peripheral measurement is difficult, the data suggest that OT abnormalities may exist in autism, and that more direct investigation of central nervous system OT function is warranted.
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The neuropeptides arginine vasopressin (AVP) and oxytocin (OT) are key modulators of vertebrate sociality. Although some general behavioral functions of AVP and OT are broadly conserved, the detailed consequences of peptide release seem to be regulated by species-specific patterns of receptor distribution. We used autoradiography to characterize central vasopressin 1a receptor (V1aR) and OT receptor (OTR) distributions in two species of singing mice, ecologically specialized Central American rodents with a highly developed form of vocal communication. While both species exhibited high V1aR binding in the auditory thalamus (medial geniculate), binding in structures involved in vocal production (periaqueductal gray and anterior hypothalamus) was significantly higher in the more vocal species, Scotinomys teguina. In S. xerampelinus, receptor binding was significantly higher in a suite of interconnected structures implicated in social and spatial memory, including OTR in the hippocampus and medial amygdala, and V1aR in the anterior and laterodorsal thalamus. This pattern is concordant with species differences in population density and social spacing, which should favor enhanced sociospatial memory in S. xerampelinus. We propose that V1aR and OTR distributions in singing mice support an integral role for the AVP/OT system in several aspects of sociality, including vocal communication and sociospatial memory.
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