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Mitchell, I. J., Gillespie, S. M., & Abu-Akel, A. (2015). Similar effects of intranasal oxytocin
administration and acute alcohol consumption on socio-cognitions, emotions and behaviour:
Implications for the mechanisms of action. Neuroscience & Biobehavioral Reviews, 55, 98-
106.
This article is the final version of the article accepted
for publication following peer review. The article was
published in the journal Neuroscience and
Biobehavioral Reviews, August 2015.
Title: Similar effects of intranasal oxytocin administration and acute alcohol consumption on
socio-cognitions, emotions and behaviour: Implications for the mechanisms of action
Running title: Oxytocin and alcohol
Authors: Ian J. Mitchell1, Steven M. Gillespie1*, Ahmad Abu-Akel1
Affiliation: 1School of Psychology, University of Birmingham, Birmingham, B152TT, UK.
Corresponding Author: Dr. Steven M. Gillespie, School of Psychology, University of
Birmingham, Birmingham, B15 2TT, UK.
E mail: S.M.Gillespie@bham.ac.uk Tel: +44 121 414 3665
Similar effects of intranasal oxytocin administration and acute alcohol consumption on socio-
cognitions, emotions and behaviour: Implications for the mechanisms of action
1. Introduction
Oxytocin (OT), a neuropeptide hormone released from the posterior pituitary gland, plays
well established roles in childbirth and lactation. More recently, studies of monogamous
voles have led to an understanding of the role that oxytocin plays in the formation of long
lasting social attachments (Carter 1998; Ross et al., 2009; Young & Wang, 2004). Such work
has emphasised how oxytocin released from terminals and dendrites of neurons within the
brain (Ludwig & Leng, 2006) can act on oxytocin receptors expressed by structures such as
the medial nuclei of the amygdala to drive the formation of partner preference (Ferguson et
al., 2001; Young & Wang, 2004; Insel & Young, 2001).
The effects of raising intracerebral oxytocin levels, by intranasal (inOT) administration, on
human social functioning have been extensively researched. Much of this work has involved
studying the effects of inOT on socio-cognitions and emotions. The findings have led to the
general conclusion that raising oxytocin levels is associated with increases in prosocial
behaviours including increased tendencies to behave altruistically, generously and
empathically, and to trust others more (Zak et al., 2007; Barraza & Zak, 2009; Baumgarter et
al., 2008; Kosfeld et al., 2005). This has led to excitement with respect to the possibility of
treating some psychological/psychiatric conditions with the compound (Meyer-Lindenberg et
al., 2011). It should, however, be noted that intranasal oxytocin administration is also
associated with amplifying some aspects of antisocial behaviour, including gloating and
envious responses in relation to competitors (Shamay-Tsoory et al., 2009), and exaggerating
ethnocentric biases (De Dreu et al., 2010, 2011).
One complication relating to interpreting the actions of inOT relates to the degree to which
the peptide can penetrate the blood brain barrier. Systemically administered neuropeptides in
general do not enter the brain with ease. However, the use of inOT procedures may be more
effective than intravenously and other systemic routes. Studies in both animals and humans
have shown that inhalation administered neuropeptides do enter the CSF and can affect
neural activity in structures such as the amygdala without inducing significant peripheral and
hormonal effects (Born, Lange, Kern, McGregor, Bickel, & Fehm, 2002; Striepens et al.
2013).
Much of the detail of the mechanisms by which oxytocin exerts its effects on human social
behaviour is still to be determined. There is currently debate as to whether these changes are
mediated by the neuropeptide exerting specific actions in a selective manner on particular
aspects of social behavior, or whether they result secondarily as a product of more low level
general effects (Churchland & Winkielman, 2012). In this paper we highlight the strong
similarities in the effects elicited by inOT and by acute consumption of modest doses of
alcohol on an array of social-cognitions and emotions, ranging from fear, anxiety and stress,
to aggression and in-group favouritism. We hypothesise that, although the two compounds
work on very different receptors, they nonetheless will induce common effects on GABA
transmission in the prefrontal cortex and limbic structures. Having explored this potentially
common neural mechanism behind the similar socio-affective responses we then explore the
possibility that both drugs act by unmasking modes of acting and thinking that are acquired
earlier in development.
2. Effects of oxytocin and acute alcohol consumption on social-cognitions and behavior
2.1. Fear, anxiety and stress
The potential anxiolytic effects of oxytocin have been inferred from the observation of
reduced anxiety and stress responses in breast feeding/suckling mammals which is
accompanied by increased release of the peptide (UvnasMoberg, 1998). Work with
experimental animals has confirmed this postulated relationship. For example, OT reduces
anxiety when administered directly in to the cerebral ventricles (Windle et al., 1997, Carter et
al., 1998), paraventricular nucleus of the hypothalamus (Blume et al., 2008) and prelimbic
area of the medial prefrontal cortex (Sabihi et al., 2014) of experimental rodents. Sub-
cutaneous injections of OT have also been shown to reduce startle responses in rodents in a
fear-potentiated startle paradigm (Missig et al., 2010), and cause reductions in stress
responses as indicated by attenuated corticosterone (Windle et al., 1997; Mantella et al.,
2004) and ACTH release in rodents and primates (Parker et al., 2005) respectively. It has also
been shown in humans that both plasma and CSF levels of OT significantly negatively
predict trait anxiety scores (Carson et al., 2014).
A series of studies have shown that inOT can similarly reduce fear responses, exert anxiolytic
effects and reduce the release of corticosteroid stress hormones in humans. One of the most
persuasive studies is that by Kirsch et al. (2005), which looked at the acute effects of inOT on
amygdala responses to fear-inducing visual images as shown by fMRI. This work
demonstrated that boosting OT levels in healthy participants reduces both fear responses in
the amygdala itself and the coupling of amygdala activity with that of midbrain structures
involved in autonomic and behavioural aspects of fear responses (see Table 1).
Table 1 about here
Other studies have focused on individuals who suffer from anxiety disorders. In this regard,
Guastella et al. (2009) showed that inOT improves mental representations of the self in
individuals with social anxiety disorder when taken in addition to exposure therapy.
Similarly, Labuschagne et al. (2012) showed in a fMRI study that inOT tempered medial
prefrontal and anterior cingulate responses to negative social cues, including fearful faces, in
patients with generalized social anxiety disorder.
Moreover, inOT reduces cortisol levels in response to acute psychological stressors,
including experimentally induced social rejection (Linnen et al., 2012) and social stress tests,
where an interaction with social support is seen (Heinrichs et al., 2003). These effects,
however, may be attenuated in men who experienced early parental separation (Meinlschmidt
& Heim, 2007). inOT is also reported to reduce the magnitude of cortisol release induced by
physiological stressors such as intense exercise (Cardosa et al., 2013).
The capacity for acute alcohol consumption to reduce anxiety has been known for centuries.
This relationship has been subject to experimental scrutiny in recent years. For example,
Sayette et al. (1992) demonstrated that acute alcohol consumption reduced negative
emotional reactions in social drinkers on a social stressor test. Alcohol can also moderate fear
reactions, and has been shown to reduce amygdala responses in social drinkers to threatening
stimuli (Gilman et al., 2008; Sripada et al., 2011). Similarly, it is thought that individuals who
suffer from social phobia may self-medicate with alcohol (Carrigan & Randall, 2003). These
anxiolytic and fear reducing responses are most likely mediated via an effect of alcohol on
the central and medial nuclei of the amygdala (Pandey, 2006). Alcohol may also be able to
reduce stress effects via an action on the central amygdala (CeA) nuclei. For example, Nie et
al. (2004) showed that alcohol interacts with CRF1 receptors to enhance GABAergic synaptic
transmission in the CeA.
Although acute inOT administration elicits anxiolytic effects, elevated levels of oxytocin may
be associated with prolonged exposure to stressors, especially in early life. For example,
maltreated children show raised urinary OT levels (a marker of cerebral OT levels) as do
adult offenders who experienced early childhood maltreatment (Seltzer et al., 2014; Mitchell
et al., 2013). Similarly, Hoge et al. (2008) showed that plasma oxytocin levels correlated with
higher social anxiety symptoms in patients with Generalized Social Anxiety Disorder
(GSAD). A parallel relationship may occur with alcohol whereby acute consumption
decreases anxiety but chronic consumption and dependence is associated with anxiety
disorders (Schuckit & Hesselbroc, 1994).
2.2. Trust, Generosity and Altruism
A succession of papers has reported that elevated OT levels are associated with increases in
trust, generosity and altruism as measured in social decision making games. For example,
inOT has been associated with the maintenance of trust even after betrayal (Baumgartner et
al., 2008) and irrespective of the tendency to take risks (Kosfeld et al., 2005). Similarly,
Theodoridou et al. (2009) demonstrated that inOT increased the ratings of trustworthiness
and attractiveness of others. Furthermore, inOT can enhance generosity and to a lesser extent,
altruism in one-shot decision making games (Zak et al., 2007).
Similar effects have been reported following acute alcohol consumption. Lynn et al. (1988)
demonstrated that there is a relationship between alcohol consumed and size of tip in
restaurant diners. More formally, Steele et al. (1985) showed that alcohol can dose
dependently make individuals more generous on tasks which involve helping another
complete an unpleasant task. The data suggest that the effect is mediated by alcohol helping
to override inhibiting pressures which act to prevent the expression of generosity.
2.3. Social decision making games
In these games, which include the ultimatum game and the dictator game, participants are
required to carve up either real or imaginary monetary rewards between themselves and in-
groups and out-groups. Both inOT and acute alcohol consumption have been shown to affect
responding behavior on these games by affecting the generosity of responses to out-group
members (Radke & De Bruijn, 2012), and by increasing rejection rates of apparently unfair
offers (Morewedge et al., 2014).
2.4. Morality
Although inOT may increase prosocial behaviours such as trust and generosity, its actions
may be more circumspect than first appears. inOT caused individuals to be more dishonest in
a coin-tossing prediction game in order to benefit fellow group members (Shalvi & De Dreu,
2014). Similarly, acute alcohol consumption can also induce changes in moral behaviour. For
example, Denton and Krebs (1990) demonstrated that alcohol consumption is associated with
transient decreases in moral maturity.
2.5. Facial emotional expression recognition
Several studies have examined the role of OT in the recognition of facial emotional
expressions. Much of this work has contrasted the effects of the neuropeptide on the
recognition of positive versus negative emotions. Several studies have reported that OT
improves the perception of happy faces (Marsh et al., 2010; Schulze et al., 2011). These
findings are supported by the results of a meta-analysis, which concluded that inOT
significantly improves recognition accuracy for happy faces (Shahrestani et al., 2013). In
equivalent experiments involving experimental primates, Parr et al. (2013) showed that inOT
reduced the monkey’s attention to negative facial expressions. However Shahrestani et al.,
(2013) also concluded that fearful faces are also recognised more accurately following inOT,
suggesting that the beneficial effects on recognition may also apply to this negative emotional
expression.
Alcohol, like inOT, affects emotional facial expression recognition. For example, Kano et al.
(2003) showed that a low dose of alcohol significantly improved the recognition of happy
faces but not negative facial emotional expressions. Moreover, others have shown that
alcohol makes sad faces harder to recognise accurately. For example, Kamboj et al. (2013)
showed that alcohol causes sad faces to be classified as neutral, while Craig et al. (2009)
reported that alcohol raised the threshold for the accurate identification of sad faces.
Similarly, Stevens et al. (2006) showed that both social phobic and control participants rated
angry faces as less rejecting following alcohol consumption.
2.6. Risk taking
Although the literature on OT and risk taking in humans is relatively small (for example, see
Kosfeld et al., 2005), there is some impressive literature on this in rodents. This work has
demonstrated that sexual activity and mating induces the release of OT within the
hypothalamic paraventricular nucleus, reduces the level of anxiety and increases risk-taking
behavior in male rats (Waldherr & Neumann, 2007; Kavaliers et al., 2008). Similarly, alcohol
has long been associated with increased risk taking in humans, with recent interests focusing
on the effects of alcohol in increasing the likelihood of risky sexual practices (Cooper, 2002;
Halpern-Felsher et al., 1996).
2.7. Analgesia
The potential analgesic effects of OT are reviewed by Uvnas Moberg (1998). Daily injections
of OT for 5 days increased the withdrawal latency to a hot noxious stimulus in a tail flick test
(Agren et al., 1995). Furthermore, Kavaliers et al. (2006) showed that OT knockout mice
show an attenuation of the analgesic response, as shown by decreased latency in foot
withdrawal in a hot-plate test, which is normally elicited by exposure to an infected
conspecific.
The analgesic effects of alcohol have been known since ancient Greek times (Rosso, 2012).
Experiments have shown that acute alcohol administration results in a transient lowering of
the sensitivity to painful electric shocks (Stewart, 1995) and a significant increase in pain
tolerance but not pain threshold (Perrino et al., 2008).
2.8. Aggression
Although OT is associated with prosocial behaviours, there are nonetheless positive
relationships between OT and aggressiveness under particular circumstances. This may
reflect the role of OT in parenting and maternal aggression (Debiec, 2005). However, inOT
also increases the probability of aggression towards an intimate partner as self-disclosed by
participants following a provocation task (De Wall et al., 2014). This effect, however, was
limited to participants with high trait physical aggressiveness.
An association between the expression of aggressive behaviours and alcohol is well
established (e.g., Giancola & Parrott, 2008; Hoaken & Pihl, 2000). However, Giancola
(2002) demonstrated that, like inOT, the effect of alcohol on increasing aggressive responses
in the Taylor Aggression Paradigm, where electric shocks are administered to a fictitious
opponent during a competitive task, is limited to individuals with high dispositional
aggressivity.
Related observations of how the effects of inOT are dependent on both personality traits and
context have been reviewed by others (Bartz, Zaki, Bolger, & Ochsner, 2011; Quintana,
Alvares, Hickie, & Guastella, 2015). These reports emphasize how personality and individual
differences along with situational factors can markedly influence the cognitive, affective and
behavioural responses to inOT.
2.9. Reward
The role that OT plays in driving the formation of attachments between conspecifics has led
to the hypothesis that OT can act on the brain’s reward circuits by encouraging the release of
dopamine by ventral tegmental area (VTA) neurons into the nucleus accumbens. This
hypothesis has been supported by Liu and Wang (2003) who showed that interactions of
dopamine and oxytocin systems in the striatum are needed for forming and maintaining
attachment bonds. Further support is provided by the observation that OT dose-dependently
excites dopamine neurons in the VTA (Tang et al., 2014), and acts as a reinforcer, like other
drugs and natural rewards, under both solitary and social conditions (Kent et al., 2013).
Similar observations have also been made with respect to alcohol. For example, Xiao and Ye
(2008) showed that alcohol boosts activity in VTA dopamine neurons by an action on local
GABAergic mechanisms. Furthermore, Gilman et al. (2008) showed in an fMRI study that
alcohol strongly activated striatal reward circuits, with the level of activation correlating with
the levels of self-rated intoxication.
2.10. Empathy/Theory of Mind (ToM)/Eye gaze
Understanding the role of OT in mediating empathic responses is made difficult by the
complexity of the empathy concept in itself. There is general agreement that empathy can be
subdivided into affective empathy, or emotional contagion, and cognitive empathy, which
includes perspective taking and ToM (Bernhardt & Singer, 2012; Decety, 2011; Shamay-
Tsoory, 2011). Shamay-Tsoory et al. (2009) have elegantly demonstrated that these two
different components of empathy are mediated by dissociable neuronal networks.
Furthermore, it appears that affective empathy appears earlier in development than cognitive
empathy (Shamay-Tsoory et al. 2009).
There are reports of inOT increasing empathic sensitivity. For example, Krueger et al. (2013)
reported that inOT increased the perception of harm for victims. Moreover, Shamay-Tsoory
et al. (2013) showed that inOT increased estimates of how much pain a member of an ethnic
out-group was experiencing as a product of an accident. Hurlemann et al. (2010) similarly
reported that inOT potentiated emotional empathic responses to both positive and negative
valence stimuli. However, no equivalent effects were seen for cognitive empathy.
By contrast, Domes et al. (2007) showed that inOT improved performance on the Reading the
Mind in the Eyes Test, a test of ToM which necessitates inferring an individual’s emotions on
the basis of images of the eye region of their face. inOT may also exert an influence over
emotion recognition by affecting eye scan paths. Both Domes et al. (2013) and Guastella et
al. (2008) have shown that inOT increases the number of fixations and total gaze time toward
the eye region of faces, that is, the facial region that is particularly rich in emotional cues.
There are surprisingly few articles reporting the effects of acute alcohol consumption on
empathy. However, one study has reported that alcohol increases affective empathy, whereby
acute alcohol consumption increases the contagion of true smiles (Duchenne smiles),
especially in males interacting with females (Fairbairn & Sayette, 2014).
2.11. In-group favouritism/out-group derogation and in-group conformity
Despite the predominance of articles on the pro-social effects of OT, there are nonetheless
some reports of it generating negative social cognitions. For example, Shamay-Tsoory et al.
(2009) reported that inOT increases envy and gloating in competitive game situations. In a
similar vein, De Dreu and colleagues (2010, 2011) have reported that inOT promotes
parochial altruism, that is, a tendency to support an in-group at the expense of an out-group.
De Dreu et al. (2011) showed that inOT was associated with a tendency to promote in-group
trust and cooperation, alongside defensive aggression toward competing out-groups.
Moreover, Sheng et al. (2013) reported that inOT enhances an EEG correlate of empathic
responding to images of ethnic in-group faces, but not out-group faces, feeling pain. Stallen
et al. (2012) also showed that inOT enhanced the tendency for individuals to express the
same opinions and judgments as members of their in-group.
Equivalent effects have been reported following acute alcohol consumption. For example,
Mitchell et al. (2015) showed that drinking modest doses of alcohol resulted in Caucasian
participants judging White faces to be more attractive than when sober. However, this effect
was not seen when the participants judged black faces and is thus indicative of alcohol
promoting in-group favouritism. Moreover, Kirchner et al. (2006) showed that acute alcohol
consumption increases the co-ordination of verbal and non-verbal behaviours and self-
reported bonding between in-group members. Furthermore, Sayette et al. (2012) showed in a
large scale study with over 700 participants, that alcohol facilitated bonding in social groups,
promoted smiling and reduced individual level behaviours associated with negative affect.
2.12. Subjective effects of inOT and acute alcohol consumption
Although a myriad of socioaffective effects have been described following inOT, the
procedure is not generally associated with marked subjective changes in mood (Kirkpartrick
et al., 2014; MacDonald et al. 2011). With the typically used single dose of OT, in the range
of 20-40 IU, effects of euphoria, light headedness and drowsiness have only occasionally
been reported and participants are only rarely able to reliably determine whether they
received inOT or placebo (MacDonald et al. 2011). By contrast, alcohol clearly has the
capacity to induce marked changes in mood. It should be noted, however, that low to
moderate doses of alcohol do not necessarily induce subjective changes in mood. Indeed,
double blind laboratory based experiments with low to moderate doses of alcohol are
frequently conducted where the participants are unaware of whether they consumed the
alcoholic drink or placebo (Kirchner et al., 2006; Sayette et al., 2012; Sripada et al., 2011;
Steele et al., 1985).
3. Potential common neurobiological mechanisms underlying the effects of inOT
and acute alcohol consumption and therapeutic implications
This extensive list of similar socio-cognitive responses resulting from the administration of
inOT and acute alcohol consumption implies that the two drugs are ultimately acting on
common neural circuits. Thus, although the two ligands act at different receptors they may
nonetheless exert equivalent actions on prefrontal and limbic circuits.
Alcohol exerts its primary pharmacological action by acting synergistically with GABA,
primarily at variants of the GABA-A receptor complex which contain a delta subunit
(Roberto et al., 2003; Akk & Steinbach, 2003). Most of the effects of alcohol on social
behaviour are thus thought to reflect the ligand modifying GABA transmission in: the
amygdala to reduce anxiety, the VTA/nucleus accumbens to elicit a sense of reward, and
parts of the prefrontal cortex. Many of the socio-affective actions of oxytocin may likewise
reflect modifications of GABAergic transmission. Indeed, Viviani et al. (2010) have shown
using in vitro techniques that oxytocin acts presynaptically to induce a massive release of
GABA from neurons in the central amygdala nuclei while benzodiazepines induce similar
effects at a circuit level by acting synergistically with GABA post-synaptically (see Figure 1).
Consequently, both inOT and acute alcohol consumption would result in an equivalent
increase in GABAergic mediated inhibition of the circuit. Similarly, Bulbul et al. (2011)
demonstrated that some of the anxiolytic effects of OT are mediated via its actions on
GABA-A receptors in the hypothalamus and Owen et al. (2013) has argued that analogous
OT/GABA interactions operate in the hippocampus to inhibit pyramidal neurons.
Figure 1 about here
If this model of oxytocin functioning is correct, it follows that the potential therapeutic
actions of OT could be mimicked by alcohol, or by any manipulation that boosts GABA-A
receptor mediated function, including administration of benzodiazepines. Tentative support
for this claim can be found. Preliminary evidence suggests that inOT can ameliorate the
symptoms of autism and increase socio-cognitive functioning in affected individuals (Andari
et al., 2010; Hollander et al., 2007, 2003; Guastella et al., 2010). Equally Han and colleagues
have shown that low, non-sedative and non-anxiolytic, doses of benzodiazepines improve
deficits in social interaction in a mouse model of idiopathic autism (Han et al., 2014). The
hyper-connectiveness model of autism (see Courchesne et al., 2007) speculates that aberrant
functioning in autism results from early brain overgrowth. This overgrowth is thought to
result in an excess of local cortical interactions which impede the functional interactions
between more distant brain sites. Pharmacological manipulations which increase GABA
transmission and so reduce the activity of these local cortical systems would consequently be
expected to have a therapeutic effect.
4. Effects of acute alcohol consumption and inOT on prepotent responses and
socio-affective responses seen in children
Although alcohol exerts its primary pharmacological action by boosting GABA-mediated
inhibition, its effects on socio-affective behaviours are typically attributed to a process of
disinhibition. For instance, alcohol can be seen as impeding the activity of high level
prefrontal cortical regions and the resultant compromised executive function allows the
expression of an otherwise suppressed behavioural response. Alcohol induced release of
prepotent responses can, for example, be seen in Stroop tasks (Marinkovic et al., 2012; Rose
& Duka 2008), n-back working memory tasks (Casbon et al., 2003) and go/no-go tasks (Rose
& Duka, 2008).
The release of prepotent responses following alcohol consumption may lead to socio-
cognitive behaviours that are similar to those observed among young children at early stages
of prefrontal development. Executive functioning is known to be limited in infants, with
children around the age of 4-5 showing difficulties in inhibiting prepotent responses (Livesey
& Morgan,1991; Kerr & Zelazo, 2004). However, adolescents still perform more poorly than
young adults on Stroop tests (Vijayakumar et al., 2014, Veroude et al., 2013). This gradual
and protracted development of executive functioning is assumed to reflect the prolonged
maturation of the prefrontal cortex which continues into adulthood. This slow process is
characterised by a shift in reliance on ventromedial areas of the prefrontal cortex for
resolving cognitive interference to structures which lie more dorsolaterally. This mirrors the
shift from the ready expression of emotional and instinctual behaviors to more controlled and
abstract responses (Fuster, 2002).
Following on from this it can be argued that acute alcohol consumption, and by analogy
inOT, will encourage the release of prepotent responses, that is, responses that would be more
typical of those made at an earlier developmental stage. A considerable array of evidence
supports this position as follows.
4.1. Trust
There is some evidence to suggest that young children intrinsically trust others prior to
developing a sense of mistrust (See Table 2). Vanderbilt et al. (2011), for example, showed
that three year old children accept advice from reliable and unreliable helpers in an
experimental game, whereas 5 year olds showed selective trust and would only take advice
from reliable helpers. Similarly, Heyman et al. (2013) showed that 3 year old children have
trouble ignoring misleading advice if it appears to have been intentionally offered by others.
Thus, inOT could be seen as enabling the release of the default condition of trusting.
Table 2 about here
4.2. Altruism
Warneken and Tomasello (2008, 2009) argue that although altruism is rare in non-humans it
is present in very young children. For example, it has been shown that 18 month old children
readily help others to achieve their goals. This altruistic behaviour appears to be intrinsically
driven and can be disrupted if extrinsic rewards are given in an attempt to reinforce the pro-
social behaviour. Similarly, Harbaugh et al. (2000) showed that children around the age of 6
years respond differently to 12 year old children and adults in a public goods game.
Participants of all ages show initial altruistic behaviour but this is only maintained in younger
children. This parallels the inOT maintenance of trust following betrayal as shown by
Baumgartner et al. (2008).
4.3. Gloating/spite
Fehr et al. (2013) reported that spitefulness decreases with increasing age amongst children
aged from 8-17 years. This effect matches the increase in envy and gloating that can be
elicited by inOT (Shamay-Tsoory et al., 2009).
4.4. In-group favoritism
In-group love can be seen in preschool children (Buttelmann & Boehm, 2014) and can drive
in-group biases. However, out-group hate only appears in children over the age of six years.
Similarly, Inguglia and Musso (2013) studied reactions to national out-groups in Italian
children. In-group favouritism was seen in children from the age of six, whereas derogation
of a national out-group was only seen in older children. These observations are equivalent to
those of De Dreu and colleagues who showed that inOT promotes in-group favouritism
without necessarily inducing large out-group derogation effects (De Dreu et al., 2010). (See
table 1)
4.5. Empathy and sympathy
Roth-Hanania et al. (2011) showed that children as young as 24 months old can show
empathy for the distress of another. Furthermore, Decety and Michalska (2010) imaged the
brain mechanisms that respond to seeing pain intentionally inflicted on another individual.
Neural activity shifted from medial prefrontal structures, which predominated in the brains of
7 year olds, to lateral prefrontal areas in adults. This may underlie a move from visceral
responses to the affective stimuli to more abstract cognitive responses and so parallel the
effect of inOT in potentiating emotional but not cognitive empathy (Hurlemann et al., 2010).
4.6. Happy facial expressions
Gao and Maurer (2010) demonstrated that children are as sensitive as adults to facial
expressions of happiness from the age of 5 years. However, sensitivity to other facial
emotional expressions develops gradually up to the age of 10 years with sensitivity to anger
and sadness developing last. This would correspond to the observed effects of inOT on
preferentially boosting the recognition of happy facial expressions relative to negative ones
(Marsh et al., 2010; Schulze et al., 2011; Shahrestani et al., 2013).
5. Conclusion
The similarity in behavioural/cognitive/emotional effects induced by inOT and alcohol, taken
together with their common effects on GABAergic transmission in identified neural circuits,
implies that the two compounds act in similar ways. A plausible model to account for their
social effects would be the removal of inhibitory brakes which normally act to suppress the
expression of response tendencies that are characteristic of earlier developmental stages.
From this it would be predicted that both inOT and alcohol would exert greater effects on
inhibiting circuits in the dorsolateral prefrontal cortex than the more primitive ventromedial
cortex.
This analysis also implies that any therapeutic effects induced by inOT could potentially be
elicited by other pharmacological manipulations which boost GABAergic transmission in
specific neural circuits. Such manipulations would include the administration of
benzodiazepines. Indeed, as noted above, low doses of benzodiazepines have recently been
shown to be beneficial in an animal model of autism (Han et al., 2014). However, given the
addictive and dependency issues surrounding both alcohol and benzodiazepines, their long
term use in treating chronic neuropsychiatric conditions would have to be pursued with
extreme caution. Against this background it is chastening to note how little is known about
the chronic effects of inOT.
The conclusion that oxytocin is exerting many of its socio-cognitive effects by suppressing
the action of prefrontal and limbic cortical circuits may at first sight seem surprising.
However, few psychoactive drugs exert their actions by boosting neuronal activity in the
sophisticated ways needed to encode for trust, generosity, empathy etc. Psychoactive drugs
are far more likely to elicit effects by reducing unwanted neural activity. Exceptions would
include drugs that boost monoamine transmission such as dopaminergic agents used to treat
the symptoms of Parkinson’s disease. But even here, the drugs are most likely enabling
normal cortical functioning to resume by reducing the interference from abnormally
discharging basal ganglia structures (Mitchell et al., 1989). If this conjecture is correct, then it
would appear that inOT may act by unmasking your inner child.
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Figure 1
Cartoon to illustrate the amygdala circuitry underlying OT and GABA
mediated neurotransmission.
Oxytocin acts at presynaptic oxytocin receptors to induce a massive release of
GABA from neurons in the central amygdala nuclei, while both
benzodiazepines and alcohol act synergistically with GABA post-synaptically
(Viviani et al., 2010). Both mechanisms will result in opening of the GABA-A
receptor associated chloride ion channel and so lead to inhibition of the
postsynaptic neuron. Equivalent circuits can be found in the prefrontal cortex.
