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Empathic dysfunction in psychopathic


individuals
R. James R. Blair
Mood and Anxiety Disorders Program, National Institute of Mental Health
Correspondence concerning the article should be addressed to James Blair, Ph.D., Chief, Unit on Affective
Cognitive Neuroscience, Mood and Anxiety Disorders Program, National Institute of Mental Health, 15 K North
Drive, Room 206, MSC 2670, Bethesda, Maryland 20892–2670. Email: blairj@intra.nimh.nih.gov

1.1 Introduction
Psychopathy can be considered one of the prototypical disorders associated with
empathic dysfunction. Reference to empathic dysfunction is part of the diagnostic
criteria of psychopathy (Hare, 1991). The very ability to inflict serious harm to
others repeatedly can be, and is (Hare, 1991), an indicator of a profound dis-
turbance in an appropriate ‘empathic’ response to the suffering of another. The
goal of this chapter will be to consider the nature of the empathic impairment in
psychopathy.
First, I will consider the disorder of psychopathy and the definition of empathy.
Second, I will consider whether individuals with psychopathy are impaired in
‘cognitive empathy’ or Theory of Mind. Third, I will consider the cognitive and
neural architecture mediating ‘emotional empathy’. Fourth, I will consider
whether individuals with psychopathy are impaired in ‘emotional empathy’.

1.1.1 The disorder of psychopathy


The origins of the concept of psychopathy probably originate in the writings of
Pritchard (1837); see Pichot (1978). Pritchard developed the concept of ‘moral
insanity’ to account for socially damaging or irresponsible behaviour that was not
associated with known forms of mental disorder. He attributed morally objection-
able behaviour to be a consequence of a diseased ‘moral faculty’. While the notion
of a ‘moral faculty’ has been dropped, modern psychiatric classifications such as
the American Psychiatric Association’s Diagnostic and Statistical Manual (currently,
DSM-IV) make reference to syndromes associated with high levels of antisocial
behaviour: conduct disorder (CD) in children and antisocial personality disorder
(APD) in adults.
3
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4 ‘Dysempathy’ in psychiatric samples

Unfortunately, the psychiatric diagnoses of CD and APD are flawed. Partly


because they only focus on the presence of antisocial behaviour, these diagnoses
tend to identify highly heterogeneous samples. This heterogeneity is even acknowl-
edged in DSM-IV where two forms of CD are specified: childhood- and adolescent-
onset types. Because of their lack of precision, the diagnostic rate of CD can reach
16% of boys in mainstream education (American Psychiatric Association, 1994)
while the diagnostic rate of APD can reach over 80% in adult forensic institutions
(Hare, 1991). Unsurprisingly, therefore, diagnoses of CD and APD are relatively
uninformative regarding an individual’s prognosis.
The classification of psychopathy, in contrast, is informative. This classification
was introduced by Hare (1980; 1991) and has proved to be a useful predictor of
future risk (Hare, 1991). The classification involves both affective-interpersonal
(e.g. such as lack of empathy and guilt) and behavioural components (e.g. criminal
activity and poor behavioural controls) (Frick & Hare, 2001; Hare, 1991).
Psychopathy represents a developmental disorder. In childhood and adolescence,
psychopathic tendencies are identified principally by either the use of the
Antisocial Process Screening Device (Frick & Hare, 2001) or by the Psychopathy
Checklist: Youth Version. In adulthood, psychopathy is identified though use of
the Psychopathy Checklist – Revised (Hare, 1991).
As noted above, psychopathy can be considered one of the prototypical disor-
ders associated with empathic dysfunction. In this chapter, I will consider the
nature of the empathic impairment in psychopathy.

1.1.2 Defining empathy


Empathy has been defined as ‘an affective response more appropriate to someone
else’s situation than to one’s own’ (Hoffman, 1987; p. 48); it is an emotional
reaction in an observer to the affective state of another individual. This form of
definition of empathy will underpin this paper. Unfortunately, however, the term
empathy has been used in a variety of ways by a variety of authors (Hoffman,
1987). At least three different types of empathy can be considered. The differences
between these types are important to identify as they must implicate notably
different cognitive architectures. The three types of empathy are: (1) motor
empathy where the individual mirrors the motor responses of the observed
actor; (2) ‘cognitive’ empathy where the individual represents the internal mental
state of the other (effectively Theory of Mind); (3) an emotional response to
another individual that is congruent with the other’s emotional reaction. In this
chapter, I will briefly consider ‘cognitive empathy’, from here onwards referred to
only as Theory of Mind, and emotional empathy with respect to psychopathy
(a distinction will be made between the two forms outlined above later in the
paper). I will not consider motor empathy in this chapter.
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5 Empathic dysfunction in psychopathic individuals

1.1.3 Theory of Mind and psychopathy


Theory of Mind refers to the ability to represent the mental states of others,
i.e. their thoughts, desires, beliefs, intentions and knowledge (Frith, 1989).
Theory of Mind allows the attribution of mental states to self and others in
order to explain and predict behaviour.
The classic measure of Theory of Mind is the Sally-Anne task (Wimmer &
Perner, 1983). In this task, the participant is shown two dolls, Sally and Anne, and
a basket and a box. The participant watches as Sally places her marble in the basket
and then leaves the room. While Sally is out, naughty Anne moves Sally’s marble
from the basket to the box. Then she, too, leaves the room. Now Sally comes back
into the room. The participant is asked the test question: ‘Where will Sally look for
her marble?’. In order to pass this task, the participant must represent Sally’s
mental state, her belief that the marble is in the basket. Without this representa-
tion, the participant will answer on the basis of the marble’s real location, i.e. the
box. Most healthy developing individuals from the age of 4 years pass this task
(Wimmer & Perner, 1983).
In addition to being considered a form of empathy in its own right, the ability to
represent the mental states of others has been considered to be necessary for
‘emotional empathy’ to occur (Batson, Fultz, & Schoenrade, 1987; Feshbach,
1987). Within these positions, representations of the internal mental state of
another are assumed to act as stimuli for the activation of the affective, empathic
response (Batson et al., 1987). Feshbach (1987), for example, viewed empathy to
be a function of three processes: first, the cognitive ability to discriminate affective
cues in others; second, the more mature cognitive skills entailed in assuming the
perspective and role of another person; third, emotional responsiveness (i.e. the
ability to experience emotions) (Feshbach, 1987). According to Feshbach (1987),
‘empathy is conceived to be the outcome of cognitive and affective processes that
operate conjointly’ (p. 273).
There are no indications of Theory of Mind impairment in individuals with
psychopathy. Three out of four studies assessing the ability of individuals with
psychopathy on Theory of Mind measures have reported no impairment (Blair
et al., 1996; Richell et al., 2003; Widom, 1978). Only one study has reported
impairment and this used a rating scale that is not a typical measure of Theory
of Mind (Widom, 1976).
Blair et al. (1996) assessed the ability of individuals with psychopathy to
perform the Advanced Theory of Mind test (Happé, 1994). This is a story
comprehension measure that assesses understanding of mental states.
Individuals with autism, a population with known Theory of Mind impairment
(Frith, 1989), are impaired on this measure (Happé, 1994). However, the individ-
uals with psychopathy were not (Blair et al., 1996).
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6 ‘Dysempathy’ in psychiatric samples

Richell et al. (2003) examined the ability of individuals with psychopathy to


perform the ‘Reading the Mind in the Eyes’ task. In this task, participants must
judge the complex social emotion being displayed by an individual based on
information only from the eye region (Baron-Cohen et al., 1997). Individuals
with autism are impaired on this task (Baron-Cohen et al., 2001). However, again,
the individuals with psychopathy were not (Richell et al., 2003).
In addition to the above work with individuals with psychopathy, it is impor-
tant to note that even in the broader spectrum of antisocial individuals, there are
few data suggesting any link between Theory of Mind impairment and antisocial
behaviour. Hughes and colleagues did find some indication of Theory of Mind
impairment in their ‘hard-to-manage’ preschoolers relative to the comparison
group (Hughes et al., 1998). However, Happé and Frith found no impairment in
their children with emotional and behavioural difficulties (Happé & Frith, 1996).
Similarly a study of school bullies found no indications of Theory of Mind
impairment (Sutton et al., 1999). In addition, Sutton and colleagues also found
no relationship between Theory of Mind performance on the advanced Eyes task
and ‘disruptive behaviour disorder’ symptoms in children aged 11–13 years
(Sutton et al., 2000).

1.1.3.1 Summary
The profound empathic dysfunction reported in the clinical description of psy-
chopathy (Hare, 1991) does not involve Theory of Mind impairment. Individuals
with psychopathy are unimpaired on measures of Theory of Mind. Indeed, there
are no indications that any populations who show heightened levels of antisocial
behaviour are associated with Theory of Mind impairment.

1.2 Emotional empathy

Figure 1.1 represents a simple schematic of the cognitive processes that I consider
to underpin empathy. Here empathy is being defined as the emotional response
to another individual’s visual or vocal expression of emotion. This schematic
assumes that there may be at least two routes to the generation of an emotional
empathic response: one which relies on the ‘semantic processing’ of the expres-
sion and one which does not. This follows suggestions that information on the
emotional expressions of others can be conveyed either by a sub-cortical pathway
(retinocollicular–pulvivar–amygdalar) or by a cortical pathway (retinogeniculostriate–
extrastriate–fusiform) (Adolphs, 2002).
These two routes for expression processing mirror those previously suggested to
be involved in aversive conditioning (LeDoux, 2000). The sub-cortical route is
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7 Empathic dysfunction in psychopathic individuals

Emotional expression

Visual (or auditory) processing of expression

Semantic processing of expression

Orchestration of the emotional response

Empathic response
Figure 1.1. A schematic of the cognitive processes thought to underpin empathy. The dotted line refers
to the suggested (sub-cortical) route that bypasses the semantic processing of the expression

thought to provide coarse stimulus processing while the cortical route is thought
to allow more precise stimulus encoding and allow discrimination learning. The
cortical route would underpin the ‘semantic processing’ of the expression; i.e. it
would allow the expression to be named and would allow goal-directed behaviour
to be initiated in response to the expression (e.g. initiate helping behaviour to a
crying individual).
In Figure 1.1, there is reference to the systems involved in ‘the orchestration of
the emotional response’. I have stressed elsewhere that the facial expressions of
emotion each have a communicatory function, that they impart specific infor-
mation to the observer (Blair, 2003a). The systems involved in ‘the orchestration
of the emotional response’ are those systems which respond automatically to
the communicatory value of the expression. In short, an empathic response
is a translation of a non-verbal communicatory signal. Because of the different
implications of these communicatory signals, I have argued that they are
translated in several separable systems (Blair, 2003a). I will consider this com-
munication and the systems that orchestrate the response to this communication
below.
I have suggested that fearfulness, sadness and happiness are reinforcers that
modulate the probability that a particular behaviour will be performed in the
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8 ‘Dysempathy’ in psychiatric samples

future (Blair, 2003a). Indeed, fearful faces have been seen as aversive uncondi-
tioned stimuli that rapidly convey information to others that a novel stimulus is
aversive and should be avoided (Mineka & Cook, 1993). Similarly, I have sug-
gested that sad facial expressions also act as aversive unconditioned stimuli,
discouraging actions that caused the display of sadness in another individual
and motivating reparatory behaviours. Happy expressions, in contrast, are appe-
titive unconditioned stimuli which increase the probability of actions to which
they appear causally related.
The amygdala has been implicated in aversive and appetitive conditioning
including instrumental learning (LeDoux, 2000). It is thus unsurprising, given
the suggested role of fearful, sad and happy expressions as reinforcers, that neuro-
imaging studies, with a few exceptions, have generally found that fearful, sad and
happy expressions all modulate amygdala activity (see, for a review, Blair, 2003a).
The neuropsychological literature supports the neuroimaging literature as regards
the importance of the amygdala in the processing of fearful expressions. There
have been occasional suggestions that amygdala damage leads to general expression-
recognition impairment but these reports are typically from patients whose
lesions extend considerably beyond the amygdala (Rapcsak et al., 2000). Instead,
amygdala lesions have been consistently associated with impairment in the recog-
nition of fearful expressions (Adolphs, 2002; Blair, 2003a). Impairment in the
processing of sad expressions is not uncommonly found in patients with amygdala
lesions (Blair, 2003a). However, amygdala lesions rarely result in impairment in
the recognition of happy expressions although this may reflect the ease with which
happy expressions are recognized (Blair, 2003a).
Disgusted expressions are also reinforcers but are used most frequently to
provide information about foods (Rozin et al., 1993). In particular, they allow
the rapid transmission of taste aversions; the observer is warned not to approach
the food to which the emoter is displaying the disgust reaction. Thus, the sugges-
tion is that the disgusted expressions of others activate in particular the insula
allowing taste aversion [the disgust expression is the unconditioned stimulus
(US) that is associated with the novel food conditioned stimulus (CS)] to occur
(Blair, 2003a).
I have argued that displays of anger or embarrassment do not act as uncon-
ditioned stimuli for aversive conditioning or instrumental learning (Blair, 2003a).
Angry expressions are known to curtail the behaviour of others in situations where
social rules or expectations have been violated (Averill, 1982). Instead, they are
important signals to modulate current behavioural responding, particularly in
situations involving hierarchy interactions (Blair, 2003a). They appear to serve to
inform the observer to stop the current behavioural action rather than to convey
any information as to whether that action should be initiated in the future.
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9 Empathic dysfunction in psychopathic individuals

In other words, angry expressions can be seen as triggers for response reversal.
Orbital and ventrolateral frontal cortex is crucially implicated in response reversal
(Cools et al., 2002). Interestingly, similar areas of lateral orbital frontal cortex are
activated by angry expressions and response reversal as a function of contingency
change (Blair, 2003b).

1.2.4.2 Summary
In short, emotional expressions are non-verbal communications. Empathy is a
prime component of the translation of this communication within the observer.
This translation is potentially reliant on both cortical and sub-cortical routes.
These routes convey the communication to regions of the brain involved in
emotional processing (the amygdala, insula and orbital and ventrolateral frontal
cortex). These regions orchestrate a response to this communication; mediating
emotional learning about objects or food or initiating response reversal.

1.3 Psychopathy and emotional empathy


As noted in the introduction, there can be no doubt that psychopathy is associated
with empathic dysfunction. However, the question remains regarding the form of
this dysfunction. I outlined above that the empathic dysfunction in psychopathy
does not include impairment in Theory of Mind. What about emotional empathy?
In Section 1.2, I outlined a schematic of the empathic process. Currently, no data exist
regarding the two routes to the systems that allow the orchestration of the emotional
response. We do not know whether psychopathy is associated with dysfunction in
systems involved in face processing. However, one reason to believe that there is no
obvious general dysfunction in the systems involved in facial processing is that while
individuals with psychopathy are impaired in expression processing, their impair-
ment appears to be selective. Given this selectivity (see below), it is unlikely that there
is notable dysfunction in the systems involved in face processing.
Two main forms of paradigm have been used to index empathy in individuals
with psychopathy: skin conductance responses (SCRs) to empathy-inducing stim-
uli and the ability to recognize facial expressions. Three studies have examined
vicarious conditioning in individuals with psychopathy; i.e. the extent to which the
participant will learn an autonomic response to a stimulus associated with another
individual’s distress (Aniskiewicz, 1979; House & Milligan, 1976; Sutker, 1970).
Two of these three studies reported reduced vicarious conditioning in the indi-
viduals with psychopathy, the third did not.
Two studies have examined SCRs to sad faces in individuals with psycho-
pathic tendencies: one examined adults with psychopathy, the other children
with psychopathic tendencies (Blair, 1999; Blair et al., 1997). In these studies,
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10 ‘Dysempathy’ in psychiatric samples

the participants were presented with images of sad faces, threatening stimuli (e.g.
pointed guns but also including an angry face) or neutral stimuli (e.g. a book).
Both the adults with psychopathy and the children with psychopathic tendencies
showed reduced SCRs to the sad faces relative to their respective comparison
populations. Interestingly, both adults with psychopathy and the children with
psychopathic tendencies showed relatively appropriate SCRs to the angry face
amidst the threatening stimuli. This was the first indication that the empathic
impairment in individuals with psychopathy might be selective for particular
expressions.
Studies have examined the ability of individuals with psychopathy to recognize
the facial or vocal emotional expressions of others (Blair et al., 2001, 2002, 2004,
2006; Kosson et al., 2002; Stevens et al., 2001). In most of these studies, the children
with psychopathic tendencies/adults with psychopathy have been impaired in the
recognition of sad/fearful expressions. Typically, the children with psychopathic
tendencies have shown impairment in the recognition of sad expressions (Blair
et al., 2001; Stevens et al., 2001). However, this has not been found in the
adults with psychopathy (with one exception; Dolan, personal communication).
In all of the studies, except that of Kosson et al. (2002), the children with
psychopathic tendencies and the adults with psychopathy have been impaired in
the recognition of fearful expressions. Kosson et al. (2002) reported some difficulty
with the recognition of disgusted expressions (but only when the participants
were responding with the left hand). Blair et al. (2004) also found some impair-
ment in the adults with psychopathy for the recognition of disgusted expressions,
however this deficit was not present if the effect of intelligence quotient (IQ) was
co-varied out.
The above data suggest a relative selectivity in the empathic dysfunction shown
by individuals with psychopathy. Individuals with psychopathy are impaired when
processing fearful, sad (in adulthood if responsiveness is indexed by SCRs, in
childhood whether by SCR or recognition score) and possibly disgusted expres-
sions. No study has yet reported that individuals with psychopathy show impair-
ment in the processing of angry, happy or surprised expressions. The absence of
impairment for angry expressions is particularly interesting. Neurological patients
following lesions of orbital and ventral frontal cortex or psychiatric conditions
which are thought to detrimentally affect orbital and ventrolateral regions, such as
childhood bipolar disorder or intermittent explosive disorder, all show general
difficulties with processing expressions but their difficulty is particularly marked
for angry expressions (Best et al., 2002; Blair & Cipolotti, 2000; Hornak et al., 1996;
McClure et al., 2003).
In the Section 1.2, I suggested that there were at least three systems responsible
for orchestrating responses to expressions; i.e. the core component of empathy
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11 Empathic dysfunction in psychopathic individuals

(Blair, 2003a). One system responsive to the aversive and appetitive uncondi-
tioned stimuli of fearful, sad and happy expressions and consequently modulating
the probability that any stimulus associated with these expressions will be avoided
or approached in the future. A second system responsive to the aversive uncon-
ditioned stimulus of a disgusted expression will reduce the probability that any
stimulus (particularly food) associated with this expression will be avoided in the
future. A third system is particularly responsive to displays of anger and embar-
rassment which modulates on-going social interactions (eliciting responses
according to the hierarchy level of the communicator amongst other factors).
I claim that individuals with psychopathy have dysfunction primarily in the
first system (that responsive to fearful, sad and happy expressions). They may
also have dysfunction in the second system (that responsive to disgusted expres-
sions). However, in the absence of additional data that possibility will not be
considered here.
As noted above, the primary neural system responsible for orchestrating an
emotional response to fearful, sad and happy expressions is the amygdala (see
Blair, 2003a). This suggests amygdala dysfunction in psychopathy. There are
considerable data in line with this suggestion (Blair, 2003b). Thus, individuals
with psychopathy show reduced amygdaloid volume relative to comparison indi-
viduals and reduced amygdala activation during emotional memory and aversive
conditioning tasks. Human and animal neuropsychological work has informed
us that the effects of amygdala lesions include impairment in: (1) aversive con-
ditioning; (2) the augmentation of the startle reflex to visual threat primes; and
(3) passive avoidance learning. If psychopathy is associated with amygdala dys-
function, the neuropsychological approach would predict that individuals with
psychopathy are impaired in the above tasks. Considerable data show that they are
(see, for a review, Blair, 2004).
While individuals with psychopathy are impaired in the processing of fearful
and sad expressions, they show no impairment for the processing of happy
expressions (Blair et al., 2001, 2002, 2003b, 2006; Kosson et al., 2002; Stevens
et al., 2001). While this is consistent with the neuropsychological literature
documenting the consequences of amygdala lesions, it is less consistent with the
neuroimaging literature (see above) which suggests a role for the amygdala in the
processing of happy expressions. Of course, the absence of impairment for happy
expressions in individuals with psychopathy might reflect the ease with which they
are recognized (i.e. an intact amygdala is not necessary for naming).
However, a more interesting possibility is that this absence of impairment
reflects the selectivity of their impairment. The amygdala is involved in the
formation of stimulus–reward and stimulus–punishment associations; animals
with amygdala lesions show impairment in both reward- and punishment-related
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12 ‘Dysempathy’ in psychiatric samples

behaviour (Baxter & Murray, 2002). Yet, the impairment in individuals with
psychopathy is far more marked for processing dependent on stimulus–punishment
associations than for stimulus–reward associations (Levenston et al., 2000). Thus,
whereas individuals with psychopathy do not show augmentation of the startle
reflex following a negative visual prime relative to comparison individuals, they do
show a comparable reduction in startle reflex following a positive visual prime
relative to comparison individuals (Levenston et al., 2000). Moreover, in
a decision-making study, individuals with psychopathy showed particular diffi-
culty, relative to controls, when choosing between stimuli associated with different
levels of punishment. Their impairment in choosing between stimuli associated
with different levels of reward was far less marked (K. S. Peschardt, A. Leonard,
J. Morton, & R. J. R. Blair, Differential stimulus–reward and stimulus–punishment
learning in individuals with psychopathy. Submitted for publication). I argue that
happy faces are appetitive unconditioned stimuli. In other words, the absence of
impairment in individuals with psychopathy for happy expressions might also
reflect the selectivity of their impairment for the processing of punishment
information as opposed to reward information.

1.3.4.3 Summary
I assume that individuals with psychopathy have no impairment in the systems
which convey facial expression information to those neural systems that are
involved in orchestrating an emotional response to these expressions. This
assumption is made because individuals with psychopathy show considerable
selectivity in their facial-expression-processing impairment. They are not
impaired for all expressions. They are not impaired when processing angry,
surprised or happy expressions. They are, however, impaired when processing
fearful, sad and, possibly, disgusted expressions. This impairment is likely related
to the amygdala dysfunction seen in patients with this disorder.

1.4 Conclusion
Empathic dysfunction is one of the major features of psychopathy. The goal of this
chapter was to consider the nature of this empathic dysfunction. Two main forms of
empathy were considered: ‘cognitive empathy’ or Theory of Mind and ‘emotional
empathy’. Considerable work indicates that there is no Theory of Mind impairment
in psychopathy. Moreover, it also appears clear that Theory of Mind impairment is
not associated with more general populations of antisocial individuals.
Emotional empathy can be considered the results of the translation of the
non-verbal communications that are the emotional expressions of others. It is
potentially reliant on both cortical and sub-cortical face processing routes. These
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13 Empathic dysfunction in psychopathic individuals

routes convey the communication to regions of the brain involved in emotional


processing (the amygdala, insula and orbital and ventrolateral frontal cortex).
These regions allow a dedicated response to the facial expressions of others. For
example, fearful and sad expressions, processed by the amygdala, initiate emo-
tional learning. In contrast, angry expressions, primarily processed by ventro-
lateral prefrontal cortex, initiate the termination of on-going behaviour.
Individuals with psychopathy have a relatively selective empathy deficit. They
are impaired in the processing of fearful, sad and possibly disgusted expressions.
Impairment in the processing of particularly fearful expressions is a common
consequence of amygdala lesions. Patients with psychopathy show many other
impairments associated with amygdala dysfunction. In short, it appears likely that
their reduced responsiveness to the fearful and sad expressions of others is related
to their more general amygdala dysfunction.
I, and others, consider the empathy dysfunction seen in individuals with
psychopathy to be at the heart of the disorder (Blair, 1995). Individuals who
are indifferent to the fear and sadness of others are individuals who are
difficult to socialize through effective socialization practices such as empathy
induction. Empathy induction involves the socializer focusing the attention of
the transgressor on the distress of the victim (and presumably heightens the
salience of the aversive stimulus of the victim’s distress). While the greater use of
empathy induction and other positive forms of parenting reduce the probability
of antisocial behaviour in healthy children, they have no significant effect on the
probability of antisocial behaviour in children with psychopathic tendencies
(Wootton et al., 1997). In other words, if we could find means to increase the
empathic reaction of children with psychopathic tendencies, we might be able to
considerably improve the prognosis of this disorder. The investigation of such
means is one of the main foci of our research at the moment.

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