Pmg.
Netm-Psycha@wmaco1.
& Broi. Psyckrat. Copyright Printed
2000,
Vol. 24, pp.
Q 2000
Elsevier
m the USA.
All rights
0278.5846/00/$-see
ELSEVIER
1277-1288 Saence front
PII: SO27S-5846(00)00143-3
RELATIONSHIP
BETWEEN ATTITUDINAL P300 LATENCIES
HOSTILITY
AND
ALYSON J. BOND AND SUSAN M. SURGUY
Section of Clinical Psychopharmacology,
Institute of Psychiatry, Kings College, London, UK
(Final form, October 2000)
Abstract
Bond, Alyson J. and Susan M. Surguy: Relationship between attitudinal hostility and P300 latencies. Prog. Neuro-Psychopharmacol. & Biol. Psychiat 2ooo,ZL PP. 1277-1288. 02000 Elwier Science Inc
1 The purpose of the present study was to determine whether components of the P300 were related to aggression in a normal population. 2. Event-related potentials were recorded from midline sites during a standard pure tone auditory oddball task. 3. Findings indicated significantly prolonged P300 latencies to target stimuli in subjects with higher total aggression and attitudinal hostility scores on the BDHI. 4. The relationship between P300 latency and aggression extends findings in specifically aggressive populations. P300 amplitudes may only be reduced in samples displaying violent or assaultive behaviour.
Kevwords: aggression, attitudinal hostility, event-related potentials, P300
Abbreviations: Barratt Impulsiveness Scale (BIS-1 l), Buss Durkee Hostility electro-oculogram (EOG), event-related potential (ERP), reaction time (RT).
Inventory
(BDHI),
Introduction
Event-related potentials (ERPs) have been studied extensively
as a measure of brain functioning
related to cognitive and perceptual processing (Donchin, 1979). The P300 wave, in particular, is a 1277
Inc.
reserved matter
1278
useful
A.J. Bond and S.M. Surguy
way
of studying
cognitive
measure
stimulus
process
a stimulus,
lower
and Kutas,
1983)
(Hillyard
P300
evaluation
abnormalities
resource
time while
being
been
in
several
less
1993, Kutcher
et al., 1989; Pfefferbaum
et al., 1984) in which
from normal.
Attempts
made
have also been
to commit
Long latency
1988).
have
been
However,
discriminate
between
The rare stimulus P300
relationship (Kiehl
students
1999)
such
The current
(Patton
population.
et al., 1995)
associated
with P300
participant
were recorded
paradigm.
changes
et
aggressive
problems acts (Gerstle
whether
the Buss Durkee
A secondary
aggressive
from three midline
behaviour
and Stanford,
1997)
using
or acts who
and
amplitude
(Raine
non-target
oddball
alcoholics
and Hesselbrock,
components Hostility
had to
tasks
task,
stimulus. have shown The
violence.
as psychopathic with
a history
if impulsivity,
components,
populations
(Barratt
1999)
and college 1999).
to
Buss and Durkee, measured
as impulsivity
et al., 1997).
to a standard
of
in less severe
and Stanford,
(BDHI:
with P300
scalp sites, in response
P300
of the P300 wave are related
Inventory
et
and Venables,
of physical
et al., 1998; Mathias
1999).
is the oddball
It has also been confirmed
(Bauer
and
(Drake
the participants
are classified
in
differ
to psychopathy
and a frequent
Studies
et al,
1994).
violent
in which
aim was to investigate
had any relationship
and/or
to
dementia,
(McFarlane
The usual convention stimulus
et al., 1988).
to investigate
in some
task
offenders
al.,
disorder
of psychopaths
aggression
imprisoned
conduct
questionnaire,
(Mathias
stimuli.
with
(Barratt
with
aggressive
a rare target
(Branchey
study was designed
1957), in a normal
oddball
crime
habitually
20% of the trials.
in currently
to impulsive,
scores on an aggression
BIS-11
on about
impulsive
as teenagers
admitting
between
to be associated
shown or
non-target
functioning
and Siegel,
displaying
performance
cognitive
of the P300
(Mirsky
in one sample
a continuous
different
is presented
for violent
populations
as enhanced
discrimination
amplitudes
et al.,
as impulsively
used
multiple
has been
imprisonment
described
this study
which only requires
reduced
crimes
to
available
including
the latency
to link components
and aggressive
classified
stress
is considered
resources
disorders
and post-traumatic
P3OOs have been found in prisoners
al., 1988) and in subjects amplitudes
violent
efficient
clinical
depression,
of the P300
to the neural
with
schizophrenia,
with the tendency
disorder,
latency
is related
associated
reported
personality
The
the amplitude
amplitude
have
allocation.
ERPs
auditory
with the has been of each pure tone
Attitudinal
hostility and P300 latency
1279
Methods
Participants Participants
were 28 paid male volunteers from the general population aged from 18 with 45 years set as
the upper limit, because participants
characteristics
were taking medication,
or past history of psychiatric All participants
of the P300 wave change
after middle
had a history of head injury or substance
disorder,
any significant
were tested in the morning,
age.
None of the
abuse, had any current
medical history nor any hearing
3 hours after any food intake
was obtained and the study was approved by the Institutionai
disabilities.
Written informed
consent
Ethical Committee.
Stimuli The auditory randomly
oddball
presented
paradigm
with the probability
intensity of 70 dB, binaurally. 120ms, (tone envelope: microswitch
consisted
of two tones
of 0.2 and 0.8, target and non-target
The inter-stimulus
rise/plateau/fall,
of lkI-Iz and 2kHz (target)
that were
respectively,
at an
interval was 2s and each tone was presented
10ms/100ms/10ms).
with the index finger of their preferred
Participants
were required
hand when the target stimulus
for
to press a
was presented.
The mean reaction time (RT) in ms was recorded. Data Acauisition Potentials
were
recorded
with silver/silver
midline Fz, Cz and Pz sites according AZ (earlobes)
and an Fpz ground.
chloride
surface
to the International
Electra-oculogram
were kept below SWZ and approximately
was amplified
placed
lo-20 system referenced
(EOG) activity was recorded
placed above and below the left eye, to allow elimination impedances
electrodes
of eye movement
equal at all sites.
artefacts.
The amplified
to linked Al and with electrodes Inter-electrode
The electroencephalogram
50,000 times and the EOG 5,000 times with a filter bandpass
5OHz notch filter was used to eliminate mains interference.
at the standard
of 0.1 - 100 Hz and a
signals were digitized
and
sampled every 2ms, from 1OOms before the stimulus to 1 lOOms after, time locked to the stimuli. Ouestionnaires The BDI-II (Buss and Durkee, score (max=75), and attitudinal
motor aggression
1957) was used to assess trait hostility factor (assault, verbal hostility,
hostility factor (resentment
and suspicion)
and aggression.
irritability
were calculated
and indirect
The total hostility)
for each participant.
total score from the BIS-11 (Patton et al., 1995) was used to measure impulsivity
The
1280
A.J. Bond and SM. Surguy
Procedure Participants were asked to fill in the questionnaires. was to be recorded in response to different tone stimuli.
They were informed that their brain activity The electrodes were then attached and they
were seated in a chair with head supports, to avoid electromyography attenuated cubicle with low ambient light, 120cm from the monitor.
contamination,
in a sound
Prior to the test, they were given
a trial block to familiarise them with the procedure, to check the integrity of the electrophysiological signal, and to ensure they were able to hear the two tones and discriminate between them. They were instructed to place the index finger of their preferred hand over the response button and asked to respond to the rare tone only. Data Analysis
The digitized data was converted to microvolts and plotted, positive values down according to convention.
Responses to each stimulus set were averaged and responses contaminated
excluded from the averages.
The P300 was taken as the major positive peak occurring between 250
and 450ms. Latency was measured from stimulus presentation, this positive peak to the following volunteers
and so the relationship
participants was investigated
by EOG
negative
peak.
Oms, to the peak, and amplitude from
The study population
between the key variables
consisted
and the questionnaire
first using multiple linear regression analysis.
individual scores to see whether two groups could be discriminated.
of healthy scores of all
We then examined the
A median split was performed
on the BDHI total scores to produce a high and a low scoring group. Univariate ANOVAs were used to compare groups on RT and the BIS- 11. Mulivariate ANOVAs were performed on the amplitudes and latencies of the P300 wave. These analyses included a between subjects factor of group (high vs low BDHI) and within subjects factors of Condition (target vs non-target)
and Site (frontal, central
and parietal). The BIS-11 was similarly analysed as an independent measure.
Results
The characteristics of the total sample and the two groups formed by the median split are shown in Table 1. The groups did not differ on age. The scores for the BDHl and the BIS-11 are shown for the total sample and for the high and low groups.
The sample fell easily into two groups with 14
subjects scoring 32 or below and 14 subjects scoring 35 or above on the BDHl total. low aggression groups differed significantly
on the BIS-11 (F1,26 =18.65, p
The high and
Attitudinal
hostility and P300 latency
1281
Table 1 Mean Ages and Scores on Hostility and Impulsivity
for the Total Sample and for the High Scorers
(35 or above) and Low Scorers (32 or below) on the BDHI Total High Scorers (N=14) Mean SD
Low Scorers (N=14) Mean SD
Total Sample (N=28) Mean SD
Age
27
5
31
7
29
BDHI Total Motor Attitudinal
43.6 27.1 9.2
7.6 4.3 3.8
26.7 17.6 4.3
4.2 4.5 2.3
35.2 22.4 6.7
10.5 6.5 4.0
BIS-11
64.9
14.7
42.9
11.5
53.9
17.1
The mean RT, latencies and amplitudes
of the P300 to the target stimuli at each electrode
shown in Table 2. There were no significant F1,26 = 0.45; p = 0.51; BE-II:
6
differences
on RT performance
F ~6 = 0.59; p = 0.45).
site are
between groups (BDHI
There were no significant
effects on the
amplitude of the P300 between groups (BDHI: F 1.26= 0.99; p = 0.33; BIS-11: Fr,26 = 0.93; p = 0.35) between target and nontarget
stimulus conditions
(BDHI: F 1.26= 1.21; p = 0.28; BIS-11: F1,26= 1.20;
p = 0.28) between electrode
sites (BDHI: F ~6 = 1.26; p = 0.29; BIS-11: Fz,J~ = 1.26; p = 0.29) nor
any significant interactions.
Table 2 Reaction Times, Latencies and Amplitudes of P300 to Target Stimuli (Rare Tones) for the Total Sample and the High (35 or above) and Low (32 or below) Scorers on the BDHl Total
High Scorers
Low Scorers
RT
375.8
89.8
3548
74.5
365.3
Fz Latency Fz Amplitude
340.1 19.8
34.3 14.4
315.4 18.7
33.2 12.5
327.8 35.4 19.2 13.2
Cz Latency Cz Amplitude
340.5 33.8 19.7 14.2
314.3 21.6
32.3 12.3
327.4 20.7
35.1 13.1
Pz Latency Pz Amplitude
341.0 14.8
314.4 32.6 16.7 11.7
327.7 15.8
34 6 10.0
32.3 8.3
Total Sample 81.6
1282
A.J. Bond and S.M. Surguy
For the P300 latency, target
conditions
electrode
(BDHI:
sites (BDHI:
interactions. components
there were no significant
significant
in either stimulus
There was a significant
condition
Fi,s6 = 0.05; p = 0.83; BIS-11:
F2,26 = 1.34; p = 0.27; BIS-11:
No further
4.65; p < 0.04).
overall
differences
were
A representative
= 0.70; p = 0.41) or electrode
p < 0.04) but no interaction were longer at all electrode was no significant on latencies
and nonthe
F 2.26 = 1.33, p = 0.27) nor any significant for the BIS-11
between recording
the high and low aggressive from one volunteer
and any of the P300
position
position
in the high aggressive
tone condition,
nor any significant
Latency
on latency (F1,26 = for the rare tone
and stimulus
condition
The high aggressive
group in the rare tone condition
group and electrode
conditions
groups
(Fz,sz = 0.81, p = 0.45).
than the low aggressive between
between
groups
in each group
(FQC
group
had
(F1,26 = 4.87;
(F2,52 = 1.09; p = 0.34) i.e. latencies
group compared
effect of group (Fi,zh = 1.95; p = 0.17) or electrode
in the frequent
the target
condition.
difference
longer latencies
between
F 1,s~ = 0.04, p = 0.84) or between
found
is shown in Fig 1. There were no interactions
significantly
differences
position
interaction
with the low.
There
(Fz,sz = 0.67; p = 0.52)
(Fz,sz = 1.46, p = 0.24).
(ms)
Fig 1. Event related responses to target stimuli (rare tones) in one volunteer scoring low (. .) on the BDHI total score.
scoring high (-)
and one
Attitudinal hostility and P300 latency
1283
The regression analysis showed a significant relationship between total BDHI scores and the P300 latencies to rare tones at Fz (F1,26 = 3.92; p < O.OS),Cz (F1,26 = 4.62; p < 0.05) and Pz (F1,26 = 4 64; p < O.OS),(Pig 2).
.
400 -
a
0 a
z 350 E .p P 300 Y 3 250 -
150 I 15
l
0
l l
a .=
‘. .
l
0
l
.
l
t 25
35
1
t
,
45
55
65
Total BDEU Scores
Fig 2 Values for P300 latencies to rare tones at Pz plotted against BDHI total scores for all participants (N=28), with regression line.
There were also significant relationships between attitudinal hostility scores and the P300 latency. Those with higher scores had longer latencies in the rare tone condition (Fr,ac = 9.42; p = 0.005) but there was no interaction with electrode position (F2,52= 1.OO;p = 0.37). Regression analysis showed a significant relationship between attitudinal hostility scores and latencies at Fz (F1,26 = 6.16, p < 0.02), Cz (F1,26 = 6.64; p < 0.02) (Fig 3) and Pz (F1,26 = 3.96; p < 0.05). There was no significant relationship between motor aggression scores and P300 latencies (Fr.26= 1.Ol, p = 0.32) and the regression analysis showed no significant results.
1284
A.J. Bond and S.M. Surguy
450
1
0
250
200 m
0
5
10 BDHI
15
Attitudinal
Fig 3 Values for P300 latencies to rare tones at Cz plotted for all participants (N=28), with regression line
20
Scores
against
BDHI
attitudinal
hostility
scores
Discussion
The principal to rare tones
finding
and scores
of the present
study was the significant
on the BDHI.
There
relationship
were no differences
between
between
P300 latencies
the frontal,
central
and
parietal sites.
&gression
High prolonged
and P300 Parameters
scores
on the
total
P300 latencies
on the BDHI,
BDHI
and
at all 3 midline
in particular
stimuli than those with lower
resentment scores.
on the sites.
attitudinal This suggests
and suspicion, This confirms
take
findings
hostility
factor
that those longer
were
participants
to evaluate
in specifically
associated scoring
infrequent
aggressive
with higher random
populations.
Attitudinal hostility and P300 latency
Drake et al. (1988) found prolonged in violent compared
prescribed
latencies to target stimuli, using an auditory oddball paradigm,
with non-violent
prison, they were carefully medication.
inmates and controls.
screened.
Although Drake’s subjects were all in
They had no history
of head injury and were not being
They were also of a similar age to our subjects.
oddball paradigm, Mathias and Stanford (1999) found prolonged students preselected
No significant
for impulsive aggression
relationships
amplitude between impulsive
participants
compared to nonaggressive
were found between amplitudes
participants
selected
et al., 1998; Mathias
in these studies were specifically
acts or destruction for Intermittent
Explosive Disorder (DSM-IV,
extreme or psychiatrically
American Psychiatric
serious assaultive
Association,
criteria used
1995). In addition,
in study populations
may account
and found that amplitudes
The most significant
difference
between scores on the BDHI and the P300 amplitude. of psychopathology
with no
et al (I 988)
Supporting evidence comes from Branchey
disturbed group.
with severity
aggressive
by the presence of head injury in almost half the
were lower in all patients with
was found for patients who had been jailed in
the past for crimes involving physical violence and a significant
been associated
the impulsive
effects in the current study, which used a normal population
who looked at P3OOs in male alcoholics problems.
with non-aggressive
and in fact met the diagnostic
group (Gerstle et al., 1998). The difference
for the absence of amplitude
were found to have
compared
However,
in
In two recent studies,
selected as having recently displayed
in one study, the results may have been confounded
psychiatric
1999).
of property on a number of occasions
impulsive aggressive
sites, or difference
from a college student population,
and Stanford,
using a visual
students.
at the different
P300, in an auditory or visual oddball paradigm,
controls (Gerstle,
Likewise,
latencies to target letters, in college
the sites, and scores on the BDHI in the present study.
aggressive
lower amplitude
1285
negative correlation
was also found
in P300 amplitudes
have generally
Reductions or behavioural
problems.
However,
increased
P300 amplitudes have been shown in panic disorder patients (Clark et al., 1996) and in posttraumatic stress disorder patients comorbid for panic disorder (Metzger et al., 1997). This has been associated with the stimulus overreactivity
Distinction
characteristic
between Tvpes of Aggression
No relationship
was found between either the motor aggression
BDHI and the P300 in the present study. different amplitude
of this type of anxiety.
components
It may be that different forms of aggression
of the P300 wave: assaultiveness
and attitudinal
hostility
factor or the irritability scale of the
to prolonged
and irritability
latency.
More
are related to
being related
severe
populations
to reduced or those
1286
A.J. Bond and S.M. Surguy
preselected
for impulsive,
aggressive
al., 1988), even when selected Stanford,
1999)
adult normal
because
subjects,
current assaultive of our subjects impulsive
subjects
such as the present
scored
would then be likely to show both effects
one, is unlikely
in some previous
subjects
such as college
to include
(Gerstle
(Drake
(Mathias
However,
decrements. the cut-off
et and
a study in
many participants
scale of the BDHI,
studies
students
of aggression.
reveal P300 amplitude
more than 8 on the irritability
the mean amplitudes
sample
with both types
and may not therefore
groups
1999). Interestingly, in the control
they include
behaviour
aggressive
behaviour
from a high functioning
displaying In fact, none
chosen
et al., 1998; Mathias
for the
and Stanford,
to rare tones in this study were more similar to those found
of these studies.
Conclusions
Aggression, population. findings
in particular
attitudinal
The P300 was elicited extend
relationships
results
were
from
found
hostility, in response
more
with
P300
severely
appears
to be related to P300 latencies
to rare tones during aggressive
amplitudes
an auditory
populations.
because
of low
oddball
in the general task.
It is hypothesised rates
These that
of assaultiveness
no
in this
population.
Acknowledgements
We are grateful with computer
to David Allen for help with running
programming
and technical
the experiment
and to Jeff Dalton
for help
assistance.
References
AMERICAN PSYCHIATRIC ASSOCIATION Mental Disorders, 4’h ed., APA, Washington. BARRATT, E. S., STANFORD, Neuropsychological and cognitive Psychiatry, 41. 1035-1044.
(1995) DC.
M. S., KENT, psychophysiological
Diagnostic
and
Statistical
Manual
of
T. A. and FELTHOUS, A. (1997) substrates of impulsive aggression. Biol.
Attitudinal
BALER, L. 0. and HESSELBROCK, problems: implications for substance 272. BRANCHEY, disordered
hostility
1287
and P300 latency
V M. (1999) P300 decrements in teenagers with conduct abuse risk and brain development. Biol. Psychiatry, 46: 263-
M. H., BUYDENS-BRANCHEY, L. and LIEBER, C S. (1988) P3 in alcoholics regulation of aggression. Psychiatry Res., 2: 49-58
BUSS, A. H. and DURKEE, A. (1957) An inventory Consult Psychol., 11: 343-349.
for assessing
different
with
kinds of hostility.
J
CLARK, C R., McFARLANE, A. C., WEBER, D. L. and BATTERSBY, M. (1996) Enlarged frontal P300 to stimulus change in panic disorder. Biol. Psychiatry, 39: 845-856. DONCHIN, E (1979) Event-related potentials: A tool in the study of human information In: Evoked Brain Potentials and Behaviour, H. Begleiter (Ed), pp. 13-89, Plenum York.
processing. Press, New
DRAKE, M. E. JR., PAKALNIS, A., BROWN, M. E. and HIETTER, S. A. (1988) Auditory event related potentials in violent and nonviolent prisoners. Eur. Arch. Psychiatry & Neural. Sci., 238: 7-10. GERSTLE, J. E., MATHIAS, C. W. and STANFORD, impulsive aggression. Prog. Neuro-Psychopharmacol HILLYARD, S A. and KUTAS, Psychol., 34: 33-61.
M.
M. S. (1998) Auditory P300 and self-reported & Biol. Psychiat., 22: 575-583.
(1983) Electrophysiology
of cognitive
processing.
Annu. Rev.
KIEHL, K. A., HARE, R. D LIDDLE, P. F. and MCDONALD, J. J. (1999) Reduced ~300 responses in criminal psychopaths during a visual oddball task Biol. Psychiatry, 45: 1498-1507. KUTCHER S. P., BLACKWOOD, D H. R., GASKELL, D. F., MUIR, W. J. and ST CLAIR, D. M. (1989) Auditory P300 does not differentiate borderline personality disorder from schizotypical personality disorder. Biol. Psychiatry, 26 766-774. MATHIAS, C. W. and STANFORD, M. S. (1999) P300 under standard and surprise conditions in self-reported impulsive aggression. Prog. Neuro-Psychopharmacol. & Biol. Psychiat., 21: 10371051. MCFARLANE, A. C., WEBER, D. L and CLARK, C. R. (1993) Abnormal posttraumatic stress disorder. Biol. Psychiatry, 34: 3 1 l-320.
stimulus
processing
in
METZGER, L. J., ORR, S. P., LASKO, N. B. and PITMAN, R. K. (1997) Auditory event-related potentials to tone stimuli in combat-related posttraumatic stress disorder. Biol. Psychiatry, $2 1006-1015. MIRSKY, A. F. and SIEGEL, A. (1994) The neurobiology of violence and aggression. In: Understanding and Preventing Violence, Vol. 2, Biobehavioral Influences, A. J. Reiss Jr., K. A Miczek and J. A. Roth, (Eds.), pp. 59-173, National Academy Press, Washington DC. PATTON, J. H., STANFORD, M. S. and BARRATT, Impulsiveness Scale. J. Clin. Psychol., 2: 768-774.
E S (1995) Factor structure
of the Barratt
1288
A.J. Bond and SM.
Surguy
PFEFFE~AUM, A., WENEGRAT, B. G. and FORD, J. M. (1984) Clinical application of P3 component of event-related potentials II. Dementia, depression and schizophrenia. Electroen. & Clin. Neuro., 59: 104-124. RAINE, A. and VENABLES, P. H. (1988) Enhanced P3 evoked times in psychopaths. Psychophysiology, 25: 30-38.
Inquiries
and reprint requests
should be addressed
Dr Alyson Bond Section of Clinical Psychopharmacology Institute of Psychiatry De Crespigny Park London SE5 8AF I.K Tel +44 (0)20 7848 037 1 Fax +44 (0)20 7252 543 7 E-mail a.bond(ia.iou.kcl.ac.uk
to:
potentials
and longer
P3 recovery