Download Brain Abnormalities in Murderers

Brain Abnormalities in Murderers !
Indicated by Positron Emission Tomography!
!
!
!
!
!
by Adrian Raine, Monte Buchsbaum, and Lori LaCasse!
!
Murderers who plead not guilty by reason of insanity (NGRI) are thought to have
brain dysfunction however, there have been no previous studies reporting direct
measures of both cortical and subcortical brain functioning in this specific group.
Positron emission tomography (PET) brain imaging was conducted on 41
murderers pleading NGRI and 41 control subjects. Murderers were characterised
by reduced glucose metabolism in the prefrontal cortex, superior parietal gyrus,
left angular gyrus, and the corpus callosum. There were also abnormal
asymmetries of activity (left hemisphere lower than right) in the amygdala,
thalamus and medial temporal lobe. These findings provide initial indications of a
network of abnormal cortical and subcortical brain processes that may cause a
predisposition to violence in murderers pleading NGRI. !
Introduction!
It has long been suspected that brain dysfunction can predispose someone to violent behaviour.
Whilst previous studies have shown that violent offenders have poorer brain functioning than
normal control subjects, it has not yet been possible to localise which specific brain areas are
dysfunctional. However, past research which looks at criminals with brain injuries does provide
clues as to which areas of the brain are associated with violence and so we can expect the
following areas to be dysfunctional in murderers; the prefrontal cortex, the left angular gyrus, the
amygdala, the hippocampus, the hypothalamus and the corpus callosum (which is responsible for
coherence between the two hemispheres, and dysfunction of which can cause hemispheric
asymmetries of function. Conversely, no dysfunction is expected in other brain areas (e.g. the
midbrain, the cerebellum) which have been implicated in other psychiatric condition but have not
been related to violence. One particularly important group of violent offenders consists of those
who commit murder and plead not guilty by reason of insanity (NGRI). Although it is thought that
such individuals have localised brain impairments, there has been no previous brain imaging
research on this important population. !
!
!
Methods!
!
Subjects!
The experimental group consisted of 41 subjects tried in the state of California (39 men, 2 women)
with a mean age of 34.3 years who had been charged with either murder or manslaughter.
Subjects were referred to the University of California to obtain evidence using PET scanning for a
NGRI defence or they had been found guilty and were referred to obtain information that may
reduce their sentence. Reasons for referral included history of head injury or brain damage. A
control group was formed by matching each murderer with a normal subject of the same sex and
age who was tested using identical PET imaging procedures in the same laboratory. The mean age
of the 41 controls (39 men, 2 women) was 31.7. They had been screened for health with a physical
exam, a psychiatric interview and their medical history was checked.!
!
PET Task Procedure!
The radioactive tracer (fluorodeoxyglucose) was injected into the the subject and taken up by the
brain for a 32 minute period during which the subject completed a continuous performance task
(CPT). The subject was then transferred to a PET scanner where the brain was scanned in 10 mm
horizontal slices as shown in Figure 1. !
1997;42:495-508
Precentrol
Postcentral
I
edure
amarginal
general PET scanning procedures and
Middle f ro~t~,,~.~
erior parietal Iobule
y be found in !Buchsbaum et al (1990).
r / :::::::::::::::::::::: ~.ngular gyrus
Superior
~iiiiii~i~
deoxyglucose (FDG) tracer was injected
lii!!::::~!~ii.::'~Jf/lll//-----"Jl~l lateral occipital
frontal \ ~ i i i : : i i : : : : ~ I
the test room and taken up by the brain
i~ F..iiiii~i~g,7//A:,.~!I =================================
~J----18
I I::::::::::::::::::::::::: ' lii::~:,i::::::ili::::~::~ii~i[¢"/A[ "~d__19
ain metabolic rate for a 32-min period
)'liii::::iY - l~'i::ii::i::iiiiiiN ~,1d--17
i i ~ .J~Ti~/i!iiiiiiiiiiiii~ ~1~ 17
subject completed the continuous periii!~...r~///~
PT; Nuechterlein et al 1983). A degraded
liiii::::::iiii::::~V////////J[ - ~
kl[i::iiiiw/////~r
of the CPT was employed as the frontal
ecause it has been shown to produce
Inferior frontal
!
ve glucose metabolic rates in the frontal
~ferior temporal
ontrols, in addition to increases in fight
Superior temporal
Posteri,or temporal
etal lobes (Buchsbaum et al 1990). The
1. Lateral
10 stackedslices
slices showing
showing surface
Figure 1.Figure
A lateral
view view
of 10ofstacked
the prefrontal
ion performance measure of d' reflects
superior, middle, and inferior cortical prefrontal areas, precentral
cortex,
and
temporal,
parietal,
and
occipital
areas.
n accuracy across the 32-min period
frontal cortex, and temporal, parietal, and occipital areas from
uraman 1982; Nuechterlein 1991). Splitcortical peel analysis. The top slice corresponds to slice #2, or
80% of head height in the brain atlas of Matsui and Hirano
r the task is high (r = .843, p < .001).
(1978).
etails are reported in Buchsbaum et al
!
!
!
!
!
!
!
!
!
!
!
!
Results!
!
values (averaged across slices) for each hemisphere
efore the FDG injection, subjects were
were extracted: superior frontal gyrus, middle frontal
als on the CPT.
Thirty Regions!
seconds before
Cortical
gyms,
and inferior
gyms (see
Figure
1).
k was started so
initial task novelty
Asthat
anticipated,
the group of 41 murderers
hadfrontal
significantly
lower
glucose
metabolism relative to
Bilateral
temporal
(superior,
middle,
inferior,
and
G labeled. After
32
min
of
FDG
uptake,
controls in both the lateral and medial prefrontal cortex in both hemispheres (see Figure 2). !
500
BIOL
PSYCHIATRY
,at. R a i n e et al
posterior), parietal (postcentral, supramarginal, superansferred to the
PET
scanner
! adjacent1997;42:495-508
rior
parietal
lobule,
and
angular
gyrus),
and
occipital
ually molded, thermosetting plastic head
(area 19, area 17 superior, area 17 inferior, and area
o hold the head still during the scan. Ten
18) measures averaged across slices were also taken
ntervals parallel to the canthomeatal line
L A T E R A L P R E(see
F R O NFigure
T A L 1).
CORPUS CALLOSUM
cans started at the level of 80% of head
e canthomeatal line (vertex to canTechnique (medial areas). Medial cortical
CONTROLS Box
1 MURDERERS
~ C O N Tand
ROLS
1MURDERERS
sually 12-14 cm) and step downward at
subcortical regions of interest were located on PET
R
R
slices by reference to stereotaxic
coordinates as
E 114
E o7were identified using
two techniques as
L
L (1989). A 3 × 3 pixel
detailed in Buchsbaum et al
A 1.18
A
region of interest box wasT placed
on cortical and
T
065
I
I 112
subcortical structures at each
level, according to a
Technique (lateral Vareas). Surface cortical
V
standard list (see Figure 2).E As06each pixel measured
E 111using a modificanterest were measured
2 × 2 ram, the size of the region of interest box was
G
G
original cortical peel
technique (Buchs11
L
approximately one full-width
half-maximum. PreL
1990) with theU four lobes and four
U o.e5
frontal
measures
extracted
from
each slice level
C 1.o9
C
ubdivisions of each
identified stereotac(given
as
a
percentage
of
the
distance
from the
0
O
hsbaum et al 1989).
This technique has
S 1.De
S o6
external
auditory
meatus
to
the
top
of
the
LEFT
LEFThead)
RIGHT
RIGFT
E
E
y at least nine different
PET groups,
and
according
to
a
brain
atlas
(Matsui
and
Hirano
1978)
HEMISPHERE
HEMISPHERE
ts advantages for facilitating intrasubject
(see Figure 2) were as follows: superior frontal gyrus
ect differences may be found in Harris et
(average of 80%, 74%, 68%, and 61% slice levels as
bsolute glucose values for each region
of
M E D I A L P R E Fshown
R O N T A Lin Figure 2), anterior medial frontal Pgyrus
ARIETAL CORTEX
e expressed as a measure relative to all
(68% level), medial frontal gyms (average of 61%,
s contained in that slice. Relative~ Crather
ONTROLS
1 M54%,
URDER
E R S47% levels), and orbital gyrus (21%
~ C Olevel).
NTROLS
1MURDERER8
and
te metabolic rates were used because
R
To assess stereotaxic error dueRE to1.22individual differences
s are more widely
reported, have the
E 1.25
in
structure
location
within
the
plane,
we evaluated the
L
L brain metabolic rate,
of removing whole
A
A 1.23
stereotaxic
frame
based
on
the
brain
outline.
Stereotaxic
ely to be related Tto function in specific
T 1.17i
I
error
could
place
boxes
in
the
caudate
into
the
ventricle,
I and Mintum 1989),
ical systems (Fox
V
V 1.21
thereby
diluting
metabolic
rates
with
cerebrospinal
zero
eater reliability within
subjects over time
E
E 1.12"
rates,
but
confidence
limits
based
on
application
of
the
al 1991). The following
three prefrontal
G 1.19
G
L
L
U
1.17
S
116
C
O
E
U
C
O
RIGHT
LEFT
HEMISPHERE
Figure 3. Relative glucose metabolic rates for murders and
controls
in lateral prefrontal
cortex (above)
andfor
medial
prefrontal
Figure
2. Relative
glucose metabolic
rates
murderers
cortex (below). Murderers have significantly lower lateral (p <
and
controls
in the lateral
and medial
cortex.
.02)
and medial
(p < .02)
prefrontalprefrontal
functioning
in both
hemispheres.
Subcortical Regions
CORPUS CALLOSUM. Murderers had bilaterally lower
glucose metabolism in the corpus callosum than controls
S
E
1.o7
1.02-
POST-CENTRAL SUPRAMARGPNAL
ANGULAR
SUPERIOR
GYRUS
Figure 4. Relative glucose metabolic rates for murderers and
controls
the corpus
callosum
and parietal
cortex.
Murderers
Figure 3.inRelative
glucose
metabolic
rates
for murderers!
have lower activity in the corpus callosum bilaterally (p < .001),
and controls in the corpus callosum and the parietal !
in the superior parietal gyri bilaterally (p < .05), and also in the
cortex.!
left
angular gyrus (p < .06).
activity, but relatively greater fight amygdala activity. A
laterality coefficient (computed using the formula left fight/left + right) indicated that murderers had relatively
!Murderers had significantly lower parietal glucose metabolism than controls, especially in the left
angular gyrus. As indicated in Figure 3, murderers had significantly lower glucose especially in the
left and right superior parietal gyri. Murderers were identical to controls on temporal lobe glucose
metabolism. Murderers were found to show significantly higher occipital lobe glucose metabolism
than controls. !
!
!
Subcortical Regions!
Murderers have bilaterally lower glucose metabolism in the corpus callosum than controls.
Murderers showed an abnormal asymmetry of activity with reduced left and increased right
amygdala activity relative to controls. Murderers showed an abnormal asymmetry of activity with
reduced left and increased right activity in the hippocampus. Murderers showed an abnormal
asymmetry consisting of relatively greater right thalamic activity. !
As predicted, there were no significant differences for the amount of midbrain and cerebellum
activity between murderers and controls. !
!
Groups did not differ on any aspect of behavioural performance on the CPT. !
!
!
Discussion!
!
The key findings from this study are that murderers pleading NGRI are characterised by;!
• reduced glucose metabolism in the prefrontal cortex, the parietal cortex, and the corpus
callosum.!
• abnormal asymmetries of activity (left hemisphere lower than right) in the amygdala, thalamus,
and the hippocampus. !
!
Biosocial Pathways from Brain Deficits to Violence!
A key question is how these multisite deficits can translate into violence via neuropsychological,
cognitive and social pathways. Regarding prefrontal deficits, damage to this brain region can result
in impulsivity, loss of self-control, immaturity, and the inability to modify behaviour, which in turn
facilitates aggressive behaviour. !
The amygdala, hippocampus, and prefrontal cortex make up part of the limbic system which
governs the expression of emotion, while the thalamus relays inputs from subcortical structures to
the prefrontal cortex. The hippocampal formation is thought to modulate aggression through its
action on the lateral hypothalamus and together with the prefrontal cortex, forms the
neurobiological basis of Gray’s Behavioural Inhibition System, which is theorised to be
dysfunctional in violent and psychopathic individuals. !
The hippocampus, amygdala, and thalamus are also important for learning, memory and
attention; abnormalities in their functioning may relate to deficits in forming conditioned emotional
responses and a failure to learn from experience, a trait which is often displayed by violent
offenders. The amygdala additionally plays a role in the recognition of emotional and socially
significant stimuli, with destruction of the amygdala in animals resulting in a lack of fear and in
humans in a reduction in autonomic arousal; thus abnormalities in the amygdala could be relevant
to a fearlessness theory of violence based on psychophysiological findings of reduced autonomic
arousal in offenders. !
The parietal cortex is involved in the integration of sensory input and the formation of abstract
concepts and may contribute to the deficits in cognitive and social information processing observed
in violent offenders. If the angular gyrus is damaged or experiences a reduction in glucose
metabolism, the individual may experience reduced verbal, arithmetic and reading ability. Such
cognitive dysfunctions could predispose to educational and occupational failure, which in turn
could predispose to crime and violence. Learning deficits have been found to be common in violent
offenders who also have low verbal IQs. !
This study provides the first direct evidence supporting the long-held notion that dysfunction in
the corpus callosum may cause a predisposition to violence. Callosal dysfunction and the resulting
lack of inter hemispheric integration could contribute to the abnormal asymmetries of function and
reduced integration previously observed in antisocial and violent groups. Another potential
implication of poor inter-hemispheric transfer is that the right hemisphere, which is involved in the
generation of negative emotions, may experience less regulation and control by the inhibitory
processes of the left hemisphere, a factor that may contribute to the expression of violence in
predisposed individuals. Rats who are stressed during their early life show increased activity in the
right hemisphere when killing mice. Severing the corpus callosum in rats leads to an increase in
mice-killing, indicating that the left hemisphere acts to inhibit the right hemisphere-mediated killing
via an intact corpus callosum. It has been observed that split-brain patients experience poor
emotional expression and an inability to grasp the long-term implications of a situation. These traits
are commonly found in violent offenders, further implicating the role of the corpus callosum in
inhibiting aggression. However it should be noted that findings from animal research cannot be
directly extrapolated to humans. Furthermore, callossal dysfunction itself is unlikely to cause
aggression; instead it may contribute to violence in those with limbic and cortical abnormalities. !
The findings of this study suggest that the neural processes underlying violence are complex and
cannot be reduced to single brain mechanisms causing violence in a direct causal fashion. Instead,
violent behaviour probably involves disruption of network of multiple interacting brain mechanisms
that predispose to violence in the presence of other social, environmental, and psychological
predispositions. Nevertheless, attempts to ‘connect’ findings from the individual brain sites in this
study must proceed cautiously, because there are brain mechanisms relevant to aggression (e.g.
the hypothalamus) that could not be imaged in this study. For this reason, this study cannot provide
a complete account of the neurophysiology of violence in this specific and selected subgroup of
violent offenders, although it is felt that it both provides evidence that murderers pleading NGRI
have different brain functioning compared to controls, and also gives initial suggestions as to which
specific neural processes may predispose to their violent behaviour. !
!
!
Conclusions!
!
First, it is important to document that these findings cannot be taken to demonstrate that violence
is determined by biology alone; clearly, social, psychological, cultural, and situational factors also
play important roles in predisposing to violence. Second, these data do not demonstrate that
murderers pleading NGRI are not responsible for their actions, nor do they demonstrate that PET
can be used as a diagnostic technique. Third, these findings do not establish causal link between
brain dysfunction and violence. Fourth, findings cannot be generalised at the present date from
NGRI murder cases to other types of violent offenders. What these findings do document is that as
a group, murderers pleading NGRI have statistically significant differences in glucose metabolism
in certain brain regions compared to control subjects. They also suggest that reduced activity in the
prefrontal, parietal, and callosal regions of the brain, together with abnormal asymmetries of
activity in the amygdala, thalamus, and hippocampus, may be one of many predispositions toward
violence in this specific group. As with all initial findings, future independent replication, refinement,
and extension are greatly needed. !
!
!