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International Journal of Law and Psychiatry 32 (2009) 266–271

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International Journal of Law and Psychiatry

Aggression, psychopathy and brain imaging — Review and future recommendations


Katarina Wahlund ⁎, Marianne Kristiansson
Karolinska Institutet, Stockholm, Sweden

a r t i c l e i n f o a b s t r a c t

Keywords: Violent behavior appears to result from a complex web of interacting genetic as well as environmental
Aggression factors. Psychopathy is a strong predictor for relapse in violent acts. The current review shed light on rapidly
Psychopathy expanding knowledge in brain imaging related to violent behavior and psychopathy. A literature search was
Brain Imaging performed in PubMed, Cochrane and PsycInfo combining the key words: mentally disordered offender/
fMRI aggression/violence/ crime/forensic psychiatry/brain imaging neuroimaging/fMRI/MRI/PET/SPECT/lack of
empathy/psychopathy and antisocial personality disorder. The reviewed material, which consisted of 48
articles, indicates a rather strong consensus on the connection between dysfunctional parts of the frontal and
temporal lobes and violent antisocial behavior and psychopathy. In future studies, it would be useful to focus
on the limbic system and to investigate which parts of the frontal lobes and cerebral networks that are of
interest in the psychopathic personality. Moreover, the reviewed material highlights some of the
methodological difficulties in this area of research such as selection bias in the recruitment of patients,
inadequate matching of control subjects, and sometimes incongruous results. In the future we hope that
brain imaging can be used to map biological deviations in different offenders in order to try to learn more
about the different mechanisms behind violent behaviors.
© 2009 Elsevier Ltd. All rights reserved.

1. Introduction probably be more interesting to consider functional differences, such


as intentions and motives that control and trigger different types of
Earlier studies have pointed to a complex web of biological and offenders. Such differences could be explored with regards to factors
social risk factors underlying antisocial and violent behavior (Raine, such as impulse control and lack of empathy. Criminal investigative
2002). Whether these risk factors eventually lead to antisocial and analyses (Hazelwood & Warren, 2000; Meloy, 2000) and case studies
violent behavior in any single individual depends on a large set of (Kristiansson, 1995), have already suggested differences in motives
possible interactions, which are still largely in need of further research and triggers underlying violent behavior.
(Raine, 2002). Specific traits in the personality may, regardless of
diagnosis, be related to violent behavior. Accordingly, there are dif- 2. Aggression
ferent motives and different triggers for violent behavior such as
hatred, jealousy, perceived insult, fantasy, distortions of reality or Quite commonly throughout the literature, aggression is subdivided
the urge to gain money or dominance. Despite a strong consensus on into affective (also called reactive) or predatory (also called proactive)
the complex causes of violent behavior, general psychiatry and for- aggression (McEllistrem, 2004; Meloy, 1988, 2006). Affective aggression
ensic psychiatry are often limited to referring violent behavior to is the mammalian response to a threatening situation and is therefore
specific psychiatric diagnoses defined in the diagnostic manual DSM- not inappropriate per se. It is enacted instantly as a direct response to
IV (American Psychiatric Association, 1994, 2000). According to DSM- provocation, such as during a verbal argument that turns into a physical
IV, subjects have to fulfill a number of criteria in order to receive a fight. Physiologically, affective aggression is preceded by intense auto-
certain diagnosis, and even then, two subjects assigned the same nomic arousal manifested by pounding heart, racing pulse, shallow
diagnosis could present very differently, since they may not share the breathing, elevated blood pressure, and muscle tension, preparing the
same criteria. To illustrate this; in order to be assigned the diagnosis body for fight or flight.
Borderline Personality Disorder (BPD), a subject has to fulfill five out Predatory aggression, on the other hand, is usually more planned
of nine different criteria. In practice therefore, two BPD patients may and goal directed and is not preceded by heightened autonomic
only really share one of the specified criteria. Therefore, it would arousal. It can be a response to provocation, but it is not acted out
directly, rather as revenge after a clear cool off period. In animals,
predatory aggression and violence is used to hunt prey for food and
⁎ Corresponding author. Department of Clinical Neuroscience, Division of Forensic
Psychiatry, Karolinska Institutet, Box 4044, S-141 04 Huddinge, Sweden. Tel.: +46 607
survival. Humans can show lack of empathy and compassion and hunt
15 39; fax: +46 8 711 71 41. one another in order to obtain rewards such as money, sex, or power.
E-mail address: katarina.wahlund@ki.se (K. Wahlund). Predatory aggression is often associated with crimes such as serial

0160-2527/$ – see front matter © 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ijlp.2009.04.007
K. Wahlund, M. Kristiansson / International Journal of Law and Psychiatry 32 (2009) 266–271 267

murders or rape (Silva, Leong, & Ferrari, 2004). It has been suggested 4. Brain imaging
that predatory aggression is strongly connected specifically to psy-
chopathy (Barratt & Felthous, 2003; Barratt, Stanford, Dowdy, Lieb- Currently, brain imaging techniques offer the possibility not only to
man, & Kent, 1999; Blair, Mitchell, Blair, 2005; Cornell et al., 1996; measure brain volumes, but also to study neuronal processing behind
Williamson, Hare, & Wong, 1987). Importantly however, psychopaths specific actions through observation and measurement of brain activity
are thought to act on impulse as well, which is reflected by the during emotional and cognitive processing. Computer tomography (CT)
impulsivity item and the poor behavior control item in the Psycho- and magnetic resonance imaging (MRI) are the most common ways
pathy Checklist Revised (PCL-R) (Hare, 2003, 1991). Subjects with of imaging the brain. In structural studies, various techniques such as
Aspergers syndrome sometimes also act in a predatory way, for in- segmentation, manual outline, semi-automatic combination of manual
stance by stalking other people, maybe as a means of “communica- and automatic segmentation, and stereotachtichal cavalieri principal
tion” (Stokes, Newton, & Kaur, 2007). (Barta, Dhingra, Royall, & Schwartz, 1997), can be used, in order to study
volumes in different areas of the brain. Brain functioning can be studied
3. Psychopathy using different techniques such as positron emission tomography (PET),
single photon emission computed tomography (SPECT) or functional
The present review will discuss contemporary research in brain magnetic resonance imaging (fMRI). PET is a nuclear medical imaging
imaging on offenders, with a specific focus on psychopathy. Psycho- technique which produces a three-dimensional image or map of
pathy is a strong predictor of relapse in violent offences (Dolan & functional processes in the body. The system detects pairs of gamma
Doyle, 2000) In 1809, psychopathy was first introduced as a concept rays emitted indirectly by a positron-emitting radioisotope, which is
by Phillippe Pinel who introduced the term: ”Mania sans délir”; introduced into the body on a metabolically active molecule. SPECT is a
“Insane without delirium”. The concept was further developed by nuclear, tomographic imaging technique that enables the study of
Cleckley in 1976 in the book “the Mask of Sanity”, (Cleckley, 1976). perfusion in the brain, either in resting state or during an active task. An
Currently, psychopathy does not exist as a DSM-IV diagnosis indirect measurement of brain activity is obtained by fMRI, utilizing the
(American Psychiatric Association, 1994, 2000). Quite often however, hemodynamic response, related to neural activity in the brain, the so
it is confused with antisocial personality disorder (APD), which is a called Blood Oxygen Level Dependency, BOLD-technique (Ogawa et al.,
defined diagnosis in DSM-IV (American Psychiatric Association, 1994, 1993).
2000). Although there are some overlapping items between the two
diagnoses, they are not interchangeable i.e. not all individuals with 5. Aim of the study
antisocial personality disorder are considered psychopaths. Psycho-
pathy is commonly assessed by use of the Psychopathy Checklist The aim of the present review is not to be a meta-analysis, but to
Revised, (PCL-R), developed by Robert Hare (Hare, 2003, 1991). PCL-R provide a glimpse of the research field on psychopathy and brain
consists of two major parts; factor one and factor two. In factor one, imaging to date, this serving as a basis for discussion of the difficulties
personality traits such as superficial charm, grandiose sense of self- that face researchers in this field. Furthermore, the review aims to
worth, shallow affect, lack of remorse, and lack of empathy are scored. provide suggestions for future areas of research.
In factor two, behavior and life style such as impulsivity, poor be-
havioral control, parasitic lifestyle, juvenile delinquency, and criminal 6. Methods
versatility is scored. PCL-R has been criticized for mixing personality
traits with lifestyle and behavior. In reference to the PCL-R, some A literature search was performed in PubMed, Cochrane and PsycInfo
authors subdivide psychopaths into primary and secondary psycho- by combining the following key words: mentally disordered offender/
paths. The primary psychopaths have more pronounced psychopathic aggression/violence/crime/forensic psychiatry/brain imaging/neuroi-
personality traits scoring high on factor one, and the secondary maging/ fMRI/MRI/PET/SPECT/lack of empathy/psychopathy and
psychopaths are displaying antisocial behavior and lifestyle, scoring antisocial personality disorder. The search yielded 58 articles, eight
higher on factor two (Lykken, 1995; Skeem, Johansson, Andershed, books, and two dissertations. From that material, only articles written in
Kerr, & Louden, 2007). English were reviewed. Any studies focusing on topics outside our area
Lack of empathy is one of the characteristics of psychopathy. There of interest (studies of children or studies using methods other than brain
are many different aspects of empathy but it has been suggested imaging) were excluded. In all the articles included, the reference lists
that psychopaths specifically lack affective empathy specifically (Blair were searched and some additional references were added. The final
et al., 2005; Blair, 2006). Affective empathy constitutes non-conscious material consisted of 48 articles divided into three categories; review
physiological reactions such as the fight or flight reaction, character- articles, structural studies and functional studies.
ized by autonomic arousal, which is controlled by the amygdala. The
amygdala is situated in the medial temporal lobe just in front of the 7. Results
hippocampus, and it is involved in emotional regulation, particularly
of unpleasant emotions (Gross, 2007). A dysfunctional amygdala has 7.1. Previous review articles
been suggested as one of the core neural correlates of psychopathy
(Blair et al., 2005; Blair, 2003, 2006). Impairments in the amygdala In the 12 review articles included, results suggested smaller brain
could lead to deficient emotional learning, which in turn could be one tissue and decreased activity in the frontal lobes in individuals with
of the reasons behind the development of psychopathy (Blair, 2003, antisocial and violent behavior (Anckarsater, 2006; Bassarath, 2001;
2006; Blair, Peschardt, Budhani, Mitchell, & Pine, 2006). In addition, a Brower & Price, 2001; Hoptman, 2003; Pridmore, Chambers, &
rather large set of studies have shown that individuals with psy- McArthur, 2005). There were also findings indicating that deviations
chopathy fail to react to threatening stimuli (Birbaumer et al., 2005; in the temporal lobes and in the limbic system are more closely con-
Patrick, Bradley, & Lang, 1993; Patrick, Cuthbert, & Lang, 1994; Raine, nected to psychopathic traits (Anckarsater, 2006; Blair, 2003; Dolan,
1996; Raine, Lencz, Bihrle, LaCasse, & Colletti, 2000). It has been 2002; Kiehl, 2006). Blair suggested, in his review article from 2006, that
suggested that this could be due to a dysfunctional or slow auto- the reason why psychopathic individuals fail to avoid actions that harm
nomic nervous system or an inhibitory mechanism stemming from others is a disrupted ability to form the stimulus-punishment associa-
other parts of the brain. Aside from the amygdala, frontal lobe dys- tions, necessary for successful socialization (Blair, 2006). The distur-
function has been suggested in psychopaths (Gorenstein, 1982; Raine, bance in the limbic system, the insensitivity to punishment, and the
2002). extreme sensitivity to reward were further discussed in the latest review
268 K. Wahlund, M. Kristiansson / International Journal of Law and Psychiatry 32 (2009) 266–271

by van Honk and Schutter (2006). In this review, the authors proposed a alities constitute a greater predisposition to violence in this group
neurobiological construct of emotional processing in primary psycho- (Raine, Phil, Stoddard, Bihrle, & Buchsbaum, 1998). Furthermore, the
pathy. They concluded that different models such as the low fear mo- murderers were subdivided according to what type of violence they
del, the somatomarker hypothesis and the violence inhibition model had used; affective or predatory violence. The latter group showed a
probably coexist and influence each other (van Honk & Schutter, 2006). pattern in glucose metabolism more similar to the healthy controls
while the impulsive group showed less metabolism in the prefrontal
7.2. Structural studies regions but an increased metabolism in sub cortical regions (Raine,
Meloy et al., 1998).
The eleven structural studies that were included pointed to dif- Two of the SPECT-studies were performed in the resting state and
ferences in brain tissue in the frontal lobes, the temporal lobes, corpus they showed that there might be a hypo perfusion in the frontal lobes of
callosum and amygdala in antisocial and psychopathic individuals alcoholics with antisocial personality disorder (Kuruoglu et al., 1996)
compared to controls. However, the results from these studies have but also in subjects that had committed violent offences (Kuruoglu et al.,
come to different conclusions. Some studies showed brain tissue loss in 1996; Soderstrom et al., 2002). In the third SPECT-study, a group of
the temporal lobes in violent patients (Laakso et al., 2001; Tonkonogy, psychopathic patients and a group of non-psychopathic patients from an
1991) and in antisocial patients (Barkataki, Kumari, Das, Taylor, & inpatient substance abuse program were scanned while performing a
Sharma, 2006; Laakso et al., 2001; Tonkonogy, 1991). Results from semantic task. The groups were compared to one another and to a
some studies presented brain tissue loss in the frontal areas (Raine healthy control group. The results showed an increased blood flow in the
et al., 2000), while yet other studies failed to show any differences at all psychopaths in relation to the non-psychopathic patients and control
between psychopaths or subjects with antisocial personality disorder subjects. This was interpreted as a greater demand on the psychopath's
compared to healthy controls (Dolan, 2002; Dolan, M., Deakin, W.J., brains when processing emotional words (Intrator et al., 1997).
Roberts, N., & Anderson, I., 2002; Dolan, M.C., Deakin, J.F., Roberts, N., & Studies using fMRI have also revealed impairments in performing
Anderson, I.M., 2002; Laakso et al., 2002). In a recent study from 2007, semantic tasks in criminal psychopaths. Individuals with a high degree
Narayan studied cortical thickness in violent patients with schizo- of psychopathy have been shown to need more time to solve semantic
phrenia and/or antisocial personality disorder in comparison to healthy tasks with abstract and concrete words compared to control subjects
control subjects. Violence was associated with cortical thinning in the (Kiehl et al., 2004). Some studies have investigated healthy individuals
medial inferior frontal and lateral sensory motor cortex, particularly in who rated high on Psychopathy Personality Inventory (PPI), a checklist
the right hemisphere, but only subjects with a coexisting antisocial developed for psychopathic traits in the normal population (Lilienfeld
personality disorder exhibited cortical thinning in inferior mesial frontal & Andrews, 1996). Results from these studies have shown that subjects
cortices (Narayan et al., 2007). In another study by Raine et al. (2003), with a high degree of psychopathic traits had a significantly different
the authors compared the corpus callosum in subjects with antisocial pattern of neural activity when processing a recognition task
personality disorder and high degree of psychopathy, recruited from demanding affective processing (Gordon, Baird, & End, 2004). In a
society, with healthy controls. They found an increased estimated cal- study by Kiehl et al. (2001), it was suggested that the deficient affective
losal white matter volume, increase in length, and reduction in callosal processing in psychopaths might result from deficient or weakened
thickness in the psychopathic individuals compared to the controls input from the limbic structures in psychopathic subjects. (Kiehl et al.,
(Raine et al., 2003). In another study “successful psychopaths”, who had 2001). In contrast to that suggestion, other studies have shown in-
not been convicted were compared to “unsuccessful psychopaths” who creased activity in limbic structures, such as the amygdala, when
had been convicted. The authors found that the “unsuccessful psy- psychopaths viewed emotional pictures (Muller et al., 2003). A recent
chopaths” had reduced prefrontal grey substance (22%) but also a higher study showed differences between psychopathic subjects and control
asymmetry in anterior part of the hippocampus in comparison to the subjects when processing facial emotions; the psychopaths showed
“successful psychopaths” and healthy controls (Raine et al., 2004; Yang, significantly lower activation in fusiform and extrastriate cortices
Raine, Lencz, Bihrle, LaCasse et al., 2005). In another study, pathological when processing happy as well as neutral and fearful faces. The
liars were compared to antisocial individuals and healthy controls. The response pattern was affected by the emotion type, however; when
results suggested that the pathological liars had 22–26% increased white processing fearful faces, the healthy controls showed increased activ-
substance in the frontal lobes although the prefrontal grey matter/white ation, while the psychopaths showed decreased activation in the
substance was reduced with 36–42% in comparison to both controls fusiform gyrus (Deeley et al., 2006). In a study on subjects with
groups (Yang, Raine, Lencz, Bihrle, Lacasse et al., 2005). antisocial personality disorder and healthy control subjects using a
differential aversive classical conditioning paradigm applied with
7.3. Functional studies odors as unconditioned stimuli and faces as conditioned stimuli,
differential effects during acquisition were found in the amygdala and
Twenty one functional studies, using the different techniques briefly dorsolateral prefrontal cortex. The controls showed signal decrease
introduced in previous section (PET (7), SPECT (3) and fMRI (11)) were while the patients' signals increased. This might seem to be an un-
included. expected result, but the authors hypothesized that the increase in
Various PET-studies have shown lower glucose metabolism in the signal in the antisocial subjects might be due to an additional effort
temporal lobes and frontal lobes of violent patients, both in the put in by these individuals to form negative emotional associations
prefrontal and orbitofrontal cortex (Goyer et al., 1994; Seidenwurm, (Schneider et al., 2000). In two other studies, also using aversive dif-
Pounds, Globus, & Valk, 1997; Volkow et al., 1995). Using PET during a ferential conditioning, psychopathic subjects did not show the same
continuous performance task, Raine at al. tested the hypothesis that a activation in the limbic-prefrontal circuit as control subjects (Birbaumer
group of violent offenders, charged of murder but pleading not guilty et al., 2005; Veit et al., 2002).
by reason of insanity or incompetent to stand trial, would show pre- Kumari et al. investigated working memory in schizophrenic sub-
frontal dysfunction. In comparison to a control group, the murderers jects, subjects with antisocial personality disorder and healthy con-
showed significantly reduced glucose metabolism in the medial and trols. The antisocial subjects showed activation deficit in the left frontal
lateral prefrontal cortex (Raine, Buchsbaum, & LaCasse, 1997; Raine gyrus, anterior cingulated, and precuneus compared to the healthy
et al., 1994). Based on these results, the murderers were further divided controls (Kumari et al., 2006). A go/no-go task was performed by
into two groups on basis of early psychosocial deprivation. Murderers violent schizophrenic patients with a co-morbidity of APD and sub-
without any clear psychosocial deficits had significantly lower glucose stance abuse disorder compared to a group of violent schizophrenic
metabolism, indicating, according to the authors, that brain abnorm- patients with no co-morbidity. The aim of the study was to verify the
K. Wahlund, M. Kristiansson / International Journal of Law and Psychiatry 32 (2009) 266–271 269

hypothesis that the group with co-morbidity would present a different cingulate gyrus (Vollm et al., 2006). Future fMRI studies applying
pattern of prefrontal functioning to that of the group with only connectivity analysis may increase our knowledge of the cerebral
schizophrenia The results did support the main hypothesis; the group networks that are important for empathic ability.
of schizophrenic patients with APD and substance abuse had signifi- Is empathic ability innate, and is it possible to train empathic
cantly less activation in the frontal basal cortices during the go/no-go capacity? With so called real time fMRI, the BOLD-response can be
task compared to the patients solely presenting with schizophrenia. The followed, and it is possible to give the subject direct feedback. Using
same group also showed significantly higher activation in frontal motor, these kinds of techniques, some researchers have investigated healthy
premotor and anterior cingulated regions compared to the group of subjects as they provoke their own feelings. In one study, subjects
patients solely presenting with schizophrenia (Joyal et al., 2007). In were able to activate their amygdala by deliberately thinking of
another study, healthy controls, which had performed self assessment something sad (Eippert et al., 2007; Posse et al., 2003; Weiskopf et al.,
PPI (Lilienfeld & Andrews, 1996), were tested with a game, Prisoner's 2004). In Germany this technique has also been used on psychopaths
Dilemma. This is a decision-making task in which one decides whether (Eippert et al., 2007). Could this be a useful future tool to train off-
or not to cooperate, and in which optimal decisions can be made on enders in empathic processing?
either emotional or cognitive grounds. The findings in the study sug-
gested that, while subjects scoring low on PPI had emotional biases 10. Ethical considerations
toward cooperation that could only overcome by cognitive effort,
subjects scoring high on PPI had an opposite bias toward defection that What impact could brain imaging techniques have and what
likewise could only be overcome by cognitive effort (Rilling et al., 2007). applications could a better understanding of brain functioning lead
to? Could brain images be used as evidence in court sessions, and
8. Conclusion could diminished responsibility be argued for on the basis of deviant
emotional processing? This is a delicate matter. It is important to keep
In conclusion, results from the present review suggest some, in mind that although we have sophisticated brain imaging techni-
possibly modest, relationship between deviant brain structure and ques, this field is quite new and the methods have many limitations.
function of the frontal and temporal lobes and violent, antisocial We still don't know exactly what activation in fMRI means. Sometimes
behavior, and psychopathy. In the future, it would be useful to focus on activation can be increased activation of inhibitory systems. It is also
the role of the limbic system and to investigate which parts of the important to remember that e.g. fMRI is an indirect measure of
frontal lobes and cerebral networks (e.g. fronto-limbic ones) that are neuronal activity. In the future more direct methods can hopefully be
of interest in the psychopathic personality. used, such as magnetoencephalography (MEG).
The results from the literature strongly suggest that current
9. Discussion knowledge of mechanisms resulting in antisocial behavior and
psychopathy is scarce, but hopefully, in the future, we will be able to
Brain imaging research on psychopaths struggles with some major learn more with the help of brain imaging techniques. In summary, we
limitations such as difficulty with selection of patients (Abbott, 2001), need to know much more before we can draw firm conclusions on
small study groups (Brower & Price, 2001; Pridmore et al., 2005) and antisocial and psychopathic traits from brain imaging data.
difficulties in finding adequately matching control subjects (Pridmore
et al., 2005). One crucial difference between studies is that some 11. Future directions
investigate psychopaths and others investigate violent subjects in gen-
eral. Likewise, in some studies, convicted offenders are being studied, It might be time to look beyond the DSM-IV and focus more on the
and in others, non-convicted subjects with psychopathic traits are being complex correlates of specific functional divergences such as lack of
studied. Another marked difficulty relates to the diagnostic definition empathy and lack of impulse control. In risk assessment and in
of included subjects; not all studies are fully clear on how their in- rehabilitation maybe it would be better to describe degree of im-
cluded subjects have been diagnosed. Diagnoses are often mixed and pulsivity and deficiency of empathy in psychopathic offenders rather
few studies are able to correct for any co-morbidity. Schizophrenic than simply categorizing subjects as having a personality disorder.
patients for instance, tend to present with high degrees of psychopathic Today, fMRI is used in research to expand the knowledge on deviant
traits such as shallow affect and lack of empathy, which makes it difficult neuronal activity and reactivity in violent offenders assigned various
to determine if these traits are expressions of the schizophrenic disease diagnoses compared to controls. In the future maybe imaging tech-
or rather reflect psychopathic co-morbidity. The selection of control nique could be a complementary tool to routine clinical practice and
subjects is also critical. Commonly, the control group consists of non risk assessments and to evaluate rehabilitation. It is important to keep
criminal healthy individuals recruited from the society, while the patient in mind however that brain imaging only is an assisting tool, also
group may consist of offenders sentenced to life in prison. limited by generalization.
In research, as well as in clinical practice, it may be important to not
consider psychopaths as a homogenous group. In the future, it is likely Acknowledgements
that researchers more commonly will make a distinction between cer-
tain subtypes of psychopaths; primary, more calculated and controlled We are grateful to Karolina Sörman and Kristina Sygel for excellent
psychopaths who often use predatory violence, and secondary, more help with language revision.
impulsive psychopaths who often commit affective violence (Skeem
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