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Int J Adolesc Med Health 2015; 27(2): 195–201

Review

Timothy R. Rice* and Nicole E. Derish

Oxytocin and callous-unemotional traits: towards


a social-cognitive approach to forensic analysis
Abstract: Callous-unemotional (CU) traits in children Introduction
and adolescents are an important risk factor for forensic
behaviors in youth and in adulthood. There is a strong
Childhood and adolescence are key periods in the life
biologic basis in CU traits, offering the possibility to
span in forensic study. The importance of developmental
design biological interventions to address this risk factor.
risk factors in addition to static risk factors of adult crimi-
This paper advances the hypothesis that the administra-
nal history in predicting recidivism is increasingly evident
tion of exogenous oxytocin is a biological intervention
(1). As histories of premeditated rather than impulsive
worthy of further investigation to address CU traits and
aggression are of far greater importance in the prediction
moderate future risk factors for forensic behaviors. The
of future aggression (2), there is great reason to study the
evidence for this assertion rests in the empiric evidence
disorders of childhood and adolescence that predispose to
that social cognitive deficits play a major role in child
premeditated acts of aggression.
and adolescent CU traits and psychopathy. Simultane-
Callous unemotional (CU) traits are a novel speci-
ously, emerging evidence suggests that youth with CU
fier of childhood- and adolescent-onset conduct disorder
traits have defined neuroendocrinological correlates
that is of great importance in developmental models of
within the oxytocin system. A review of the normal neu-
forensic behaviors (3). It is of increasing value as a bio-
rohormonal physiology of this system is presented to
logically based risk factor for premeditated aggression (4),
provide a groundwork for the delineation of these cor-
including proactive physical bullying (5). The presence
relates. That deficits in this system are found in alternate
of CU traits moderates the ability of positive parenting
psychopathologies that present with deficits in social
interventions (6–9) and other psychosocial interventions
cognition serves as the basis for the hypothesis that
(10) to reduce conduct problems, suggesting a weak envi-
these deficits may play a key role in the development
ronmental responsiveness of these youth to psychosocial
and manifestation of CU traits. Their correction through
interventions. Additionally, there is a substantial genetic
psychopharmacologic and alternate means may provide
component to CU traits (11): heritability is nearly 50% (12)
a future route to addressing a central area of adolescent
and up to 80% when combined with aggressive behaviors
forensic psychiatry.
in general (11). Biological routes to helping these children
are therefore greatly needed and could serve as a potential
Keywords: aggression; callous unemotional (CU) traits;
avenue for the primary prevention of forensic behaviors.
child and adolescent psychiatry; conduct disorder; foren-
Evidence of social cognitive deficits in CU traits sug-
sics; men’s mental health; oxytocin; social cognition.
gests that interventions targeting this neurally based
system may show promise. Recent work concerning the
DOI 10.1515/ijamh-2015-5011 role of the neuropeptide hormone oxytocin in CU traits
Received July 6, 2014; accepted August 18, 2014; previously pub- has begun to affirm this hypothesis. CU traits appear
lished online November 20, 2014
highly related to abnormalities in the oxytocin neuroen-
docrinological system, suggesting one avenue for bio-
logical therapeutics. The aim of this communication is to
review the oxytocin hormonal system and the evidence
that suggests the presence of disturbances of this system
*Corresponding author: Timothy R. Rice, Department of Psychiatry,
in CU traits. Specific attention is paid to evidence suggest-
The Icahn School of Medicine at Mount Sinai, 1 Gustave L Levy Place,
Box 1230, New York, NY 10029, USA, E-mail: timothy.rice@mssm.edu
ing direct correlations with oxytocin abnormalities and
Nicole E. Derish: Department of Psychiatry, The Icahn School of premeditated aggression. The implications for treatment
Medicine at Mount Sinai, New York, USA and forensic analysis conclude the piece.

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196      Rice and Derish: Oxytocin and callous-unemotional traits

Callous-unemotional traits and with biological models. This is in alignment with the goals

social cognition of the Research Domain Criteria (RDoC) project (20–22).


Five areas of social cognition (23–26) have been
described in the literature. Theory of the mind (ToM)
Although CU traits are new to the DSM5, they have a rich
describes the representation of others’ mental states,
history in clinical psychiatry (13). Its precedents included
allowing interference with others’ feeling, intentions
the undersocialized type of Conduct Disorder in DSM-III
and beliefs. Social perception is the understanding of
(14), a subtype that was historically recognized to be
complex and/or ambiguous social roles and rules, using
poorly responsive to psychotherapeutic interventions (15).
social cues as a guide. It is closely related to the RDoC
In addition to the clinical utility of this specifier, there was
subconstruct “understanding mental states” within the
evidence that these traits were temporally stable through-
perception and understanding of others construct in the
out development. The undersocialized subtype was not
social processes domain (27). Social knowledge refers to
retained in DSM-IV. An increasing interest in biological
the ability to determine what rules to adhere to in social
psychiatry has led to its reincarnation in DSM5 in the
contexts (23). Emotion recognition indicates the ability
form of CU traits (3). There is a validated scale to address
to recognize non-verbal cues, such as facial expressions
CU traits dimensionally (16), as well as a commonly used
and vocal tone. Emotion recognition closely overlaps with
broader screen for sociopathy, the Antisocial Process
the RDoC subconstruct “reception of facial communica-
Screening Device or APSD (17), which includes a CU sub-
tion” within the social communication construct in the
scale; there are at least 17 assessments for psychopathic
social processes domain. Attributional style refers to the
traits in youth (18). Although some suggest that CU traits
tendency to assign causality to events (28). Healthy indi-
may be valid only as a specifier to conduct disorder, there
viduals have a bias to assign external causality to negative
is evidence that CU may be a transdiagnostic phenomenon
events, while attributing positive events to circumstances
with particular relevance to oppositional defiant disorder
within their control.
and attention deficit hyperactivity disorder (18).
A review of these sub-dimensions of social cogni-
The DSM-V criteria for CU traits as a categorical speci-
tion with sociopathy in mind suggests that child and
fier are as follows:
adolescents with CU traits have deficits in one or more
–– Lack of remorse or guilt does not feel bad or guilty when
of these overlapping sub-domains; that is, there is face
he/she does something wrong (except if expressing
validity to this claim. A deficit in any of these subdomains
remorse when caught and/or facing punishment).
would impair or preclude the youth from associating
–– Callous-lack of empathy disregards and is uncon-
their aggressive violations of the social rules (social per-
cerned about the feelings of others.
ception, social knowledge, and attributional style) with
–– Unconcerned about performance does not show con-
negative induced states in their victims (theory of mind,
cern about poor/problematic performance at school,
emotion recognition). From a behavioral perspective,
work, or in other important activities.
aversive conditioning can therefore not occur. Models
–– Shallow or deficient affect does not express feel-
have hypothesized social cognitive deficits, including
ings or show emotions to others, except in ways that
ToM deficits, in psychopathy (29), and there is now con-
seem shallow or superficial (e.g., emotions are not
firmatory empiric neurobiologic evidence in child and
consistent with actions; can turn emotions “on” or
adolescent populations.
“off” quickly) or when they are used for gain (e.g., to
Studies show that youth with high APSD scores dem-
manipulate or intimidate others) (13).
onstrate deficits in emotion recognition and social per-
ception. Relevance to CU traits is evident, for example,
To meet the criteria, two or more of the preceding items in the inability of these youth to appreciate fearful vocal
must be shown persistently over one year and in more affect (30) and body posture (31). Such a deficit impairs
than one relationship or setting. the social cognitive ability to detect fear in hypothetical
These criteria suggest that CU traits are related to defi- victims, which may deter from aggressive acts. Similarly,
cits in social cognition. Studies have shown that this is the fMRI studies show that youth with CU traits demonstrate
case (19). The dissection of the heterogenous construct reduced amygdala reactivity to fearful, but not angry or
of social cognition into sub-dimensions assists in under- neutral, facial expressions (32, 33). Whereas one study
standing the deficits of CU traits. It also enables greater (34) found these deficits restricted to sad rather than
approximation to neurally correlated observable behaviors fearful faces, and two studies, one of which (35) was con-
and social information processes, facilitating integration ducted exclusively with female adolescents, found no

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Rice and Derish: Oxytocin and callous-unemotional traits      197

correlations between amygdala dysfunction and CU traits, Oxytocin


there are a series of studies in adults that do suggest that
“fear blindness” may be central to CU traits and psycho­ Oxytocin is a nine amino acid neuropeptide that is pro-
pathy (36). The reason for the disparity should be clarified duced in the paraventricular and supraoptic nuclei of the
to determine whether this may be accounted for by insuffi- hypothalamus (53). It is stored in hypothalamic axonal
cient power in these studies and/or whether this presents terminals within the pituitary’s posterior lobe where it
a true developmental divergence. is released into the peripheral circulation. In addition
Impaired emotion recognition may be a product of to its actions on the mammary glands, where it effects
the decreased salience of fearful affect to these youth milk letdown, and on the uterus, where it promotes con-
(37). Youth with CU traits demonstrate reduced atten- tractions during labor, it has pro-social neurobehavioral
tion to the eyes (38, 39). One study that examined these effects (54) that occur in interaction with vasopressin
deficits in interaction with these children’s mothers when (55). These effects are produced as it circulates through
their mothers were asked to show love found that the the bloodstream and returns to the brain; as such, it is a
deficits are independent of maternal behavior (40). The hormone and is situated squarely in the emerging field of
eye deficits in some ways mirror the gaze avoidance and psychoneuroendocrinology.
amygdala dysfunction that is seen in the autism spectrum Pro-social effects are mediated through increases in
disorders (ASDs) (41) and in schizophrenia (42). Whereas the salience (56, 57) and the rewarding properties (58–60)
earlier studies suggested hypoactivation of the amygdala of social stimuli. Oxytocin additionally reduces anxiety in
in schizophrenia, more recent studies suggest hyperacti- social settings (61, 62). Mechanisms include interactions
vation as it occurs in the ASDs. This difference in amyg- with the monoaminergic (63) and hypothalamic-pitui-
dalar activation patterns suggests an interesting point of tary-adrenal axis (61, 62, 64, 65). Animal studies suggest
divergence between CU traits and the ASDs and schizo- that receptors may be congregated in nucleus basalis
phrenia; it may be that differential activation within the of Meynert, pedunculopontine tegmental nucleus, the
amygdala is important to clarify in psychopathy (43) and superficial gray layer of the superior colliculus, the trap-
other disorders. ezoid body, and the ventromedial hypothalamus – areas
Processing deficits are also demonstrated in the CU that are important in salience and attentional tasks. Func-
trait literature. A sample of adolescents in a diversion tional neural correlates include decreases in amygdalar
program found CU traits to be associated with increased activation and brainstem connectivity in the presence of
(slower) reaction time latency when viewing negative stressors (65).
emotional words (44). The decreased emotion recognition Whereas some (66) suggest that oxytocin promotes
demonstrated by these youth may be related not only to pro-social effects in all individuals, others suggest that
attentional artifacts, but also to preattentive processing pro-social effects occur only in individuals with primary
deficits (45). social cognitive deficits (67). Contextual and inter-indi-
There is also evidence suggesting ToM deficits in vidual differences may also influence oxytocin effect
youth with CU traits. In an evaluation of putative asso- (68). These suggestions are supported by the findings
ciations between the set of sociopathic characteristics of that studies of oxytocin in relation to the negative symp-
CU traits, narcissism, impulsivity, and Machiavellianism toms of schizophrenia (69), and in particular of the ASDs
with ToM as assessed through scores on a story-based (70), generally produce positive findings, but these find-
measure, the Advanced Test of Theory of Mind (46), only ings have not been replicated elsewhere. A prime case
CU traits were significantly negatively associated with in point are studies in borderline personality disorder,
ToM (47). In another study, a correlation analysis between where oxytocin may decrease pro-sociality (71). These
a community sample of youth scores on the Reading the inter-individual differences may be a product of the social
Mind in the Eyes Test (48), an assessment of ToM capa- stimuli salience effect of oxytocin: as individuals with
bilities, and the APSD revealed a statistically significant borderline personality disorder have increased incidences
negative correlation (r = –0.36, p = 0.01, n = 91) (49). This of insecure attachments and negative expectations from
association remained significant while controlling for social interaction, increased salience to such stimuli may
gender, IQ-sustained attention, and working memory promote defensive behaviors and distress. Supporting evi-
performance. This finding replicates in a community- dence for this hypothesis includes findings that oxytocin
based youth population an association that had been may be most deleterious in individuals with borderline
known among psychopathic adults in incarcerated set- personality disorder who are anxiously attached (72) or
tings (50–52). reporting a history of emotional neglect in childhood (73).

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198      Rice and Derish: Oxytocin and callous-unemotional traits

Additionally, there are temporal and developmental children with CU traits have decreased oxytocin receptor
considerations in the effect of oxytocin on the human expression. This emerging finding explains that cumula-
central nervous system. It is hypothesized that oxytocin tive environmental exposure to psychosocial stressors,
can contribute to aggressive behavior through both pre- which can promote methylation, among other potential
disposing genotypes (74) and epigenetic modifications explanations such as developmental processes to which
(75, 76), especially those which occur during sensitive the adolescent with CU traits is predisposed, may account
periods of development. for this finding.
Other alternations have been observed that suggest
a relation between the oxytocin system and CU traits.
These studies investigate aggression and characteristics
Oxytocin system hypotheses and that may be highly associated with CU traits. Significantly

emerging findings regarding CU increased levels of IgM autoantibodies against oxytocin


have been found in both young men with histories of
traits conduct disorder and male prisoners (87). Significantly
reduced cerebrospinal fluid levels of oxytocin are found in
The above discussion suggests that the social deficits individuals with histories of aggression (88).
demonstrated in CU traits may be responsive to thera-
peutics based within the oxytocin system. There are also
detectable biological markers in the oxytocin system in
youth with CU traits, which further suggest that oxytocin Conclusions
is a candidate intervention for addressing forensic behav-
ior risk in these youth. At a time when there is an increasing interest in and
Previous studies have shown that certain genetic poly­ means of addressing the biological substrates of the crimi-
morphisms of the oxytocin receptor are associated with nal mind via direct neuromodulation irrespective of legal
pro-social behavior (77), empathy and stress reactivity and ethical dilemmas (89), this developmental approach
(78), and receptivity to social support (79). More recently, of addressing CU traits through the correction of deficits in
it has been discovered that there are also single nucleotide the oxytocin system offers a humane possible alternative
polymorphisms (SNPs) of the oxytocin (74) and the oxy- that is worthy of further research.
tocin receptor (80–82) genes that are also associated with The limitations to the current research include that
CU traits and conduct problems. Two of these studies were most studies are single-dose, short-term evaluations of
case-control studies of approximately 160 children with the effect of oxytocin administration. Rather than discour-
extreme, persistent and pervasive aggressive behavior. age, these deficits should promote optimism regarding the
The relatively small sample size of these studies, as well as future possibilities worthy of investigation. For example,
some methodological limitations, warrants further inves- administration may produce long-term changes in the
tigation. This positive finding mirrors that found in the psychological development of the youth with CU traits
ASDs (83). The authors note that one identified SNP, SNP (90). Another ripe avenue for research is an investigation
rs2254298, is associated with limbic structure volumes in of the potential for periodic administration of oxytocin
select adults (84, 85) and provides an interesting correlate during key psychosocial points in these youths’ lives, i.e.,
with the aforementioned social cognition deficits. in therapeutic settings (91). It is possible that such inter-
Epigenetic modifications are an alternate means ventions may assist in overcoming the traditionally severe
through which youth with CU traits may diverge from treatment refractoriness of this population to psychother-
healthy youth (76). One important means of epigenetic apeutic interventions, likely related to the impediment
modification is the methylation of CpG islands in the that their social cognitive deficits present to these youth
promoter regions of various genes, which significantly to connect with their therapists.
reduces gene expression. The oxytocin receptor gene Whereas exogenous administration of standard syn-
has been studied and found to show a 70% reduction in thetic oxytocin is the most direct avenue of future investi-
activity when its promoter was methylated (86). A sig- gation, there are of course alternate means of modifying
nificant association was found between pre-adolescents the oxytocin system biology in a therapeutic fashion. For
and adolescents with CU traits and promoter methyla- example, variants of synthetic oxytocin (92) may produce
tion, whereas no such association was found in children divergent effects. Consideration and investigation on the
with CU traits (75). This suggests that adolescents but not effects of the common practice of oxytocin application

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Rice and Derish: Oxytocin and callous-unemotional traits      199

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