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Frontal reactivity and sensation seeking an ERP study in skydivers
Prog. Nwo-PsycJxophcmnacwL
& BioL
Psychic&.
1999, Vol. 23, pp. 447463 1999 Ekvier Science Inc.
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AU rights reserved
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ELSEVIER
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FROIUTAL REACTMTY
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1
AND SENSATION SEEKING AN ERP STUDY IN SKYDIVERS
ANNICK PIERSON, JACQUES LE HOUEZEC, ARNAUD FOSSAERT, STEPHANIE DUBAL and ROLAND JOUVENT CNRS UMR 7593, H6pital de la Salp&i&e, Paris, France
(Final form, March 1999)
Abstract Pierson Annick, Jacques Le Houezec, Amaud Fossaert, StP;phanie Dubal and Roland Jouvent: Frontal Reactivity and Sensation Seeking: An ERP Study in Skydivers. Prog. Neuro-Psychopharmacol. & Biol. Psychiat. 1999,2& pp. 447463.81999 ElsevierScienazInc. 1.
2. 3.
4.
In the line of Zuckerman’s studies on sensation seeking and optimal level of arousal, the authors hypothesized that high sensation seeking might be used to compensate for anhedonia due to basal arousal deficit. A population of interest was found with parachutists practicing skydiving, generally described aa very high sensation seekers. After clinical assessment of emotional and affective components, amplitudes of the frontal P3 of the ERP were used as indices of arousal. Skydivers presented more negative symptoms (anhedonia and blunted-affect) than controls. This was observed in isolation from any depressive episode, which would suggest the presence of emotional deficit as a trait. As expected, skydivers presented more sensation seeking than controls. These two results taken together could indicate that sensation seeking is an adaptive reaction to anhedonia. ERP results showed that l?ontal P3 amplitudes were larger in skydivers than in controls, whereas in a previous study we showed the opposite in depressed patients with a similar emotional deficit. This could indicate that the frontal P3 amplitude does not reflect the emotional deficit per se. We suggest that it rather reflects the capacity to use some behaviors which improve automatic attentional processes in order to obtain arousing stimulation that could counterbalance the emotional deficit. Depressions with emotional deficit might be due to the lack of such a capacity.
Kev_words: emotional deficit, ERP, frontal reactivity, negative symptoms, orienting reflex, personality, sensation seeking. Abbreviations: Abram+Taylor blunted-affect scale (AT), Cchelle d’humeur depressive - depressive mood scale (EHD), 6chelle de ralentissement dkpressif - depressive retardation scale (ERD), event related potentials (E&P), Hamilton rating scale for depression (I-IRSD), Montgomery and Asberg depressive rating scale (MADRS), orienting reflex (OR), reaction time (RT), t&personality questionnaire (TPQ).
A. Pierson et
448
al.
Introduction Sensation
seeking was described
novel and complex sensations the sake of experience”. physiological perspective,
by Zuckerman
and experiences
Zuckerman
basis for the sensation
(1979) as a “trait defined by the need for varied,
and the willingness
et al (1972) asserted
to take physical and social risks for
that the optimal
seeking trait. Such an approach
is in keeping with a biological
being based upon Berlyne’s (1950) and Hebb’s (1955) concept
arousal and upon Eysenck
and Eysenck’s
later theory
hypothesis was that certain personality traits (extraversion chronic under-arousal
which makes these individuals
level of arousal is the
incorporating
of an optimal level of
this same notion.
Eysenck’s
for the case in question) may be explained by
seek sources of stimulation
so as to increase their
arousal to an hedonic point (Eysenck and Eysenck 1978). Following between
along the same lines, our group conducted
sensation-seeking
and emotional
research, the authors concluded sensations
and to compensate
that high sensation
i.e. blunted-affect
the relationships
and anhedonia.
seeking can be considered
From this
as intended to provide
for anhedonia due to a basal arousal deficit (Carton et al 1992a). It was
also shown that frontal P3 amplitudes retardation
deficiency,
several studies investigating
and blunted-affect,
were abnormally
and a correlation
low in depressed
patients with psychomotor
was observed between frontal amplitude and negative
symptoms (Pierson et al 1991; Partiot et al 1993). The present study was designed to investigate
indices of frontal dysfunction
in subjects presenting
a
sensation seeking trait. The task selected was designed to analyze cortical indices of arousal related to certain cognitive processes by manipulating 1) the probability
of occurrence
two experimental
of the stimulus,
variables:
which
mainly
required
automatic
orienting
processes, 2) the classification
of the stimulus as being a target or a non-target for a motor response, that mainly
required selective attentional (and therefore controlled) processes. The task consisted
in differentiating
two types of stimulus presented
in different
proportions,
with
either frequent or rare stimuli being the target for the motor response (oddball task). Working on the assumption that sensation seeking is an adaptive behavior intended to compensate basal anhedonia
or blunted-affect,
made. A population
of interest
a clinical emotional
and affective
for such a study appeared
evaluation
of the subjects
to be people practicing
high-risk
generally described as very high sensation seekers. Several studies have reported relationships sensation
seeking and the practice of sport (Hymbaugh
higher relationship
observed
and Garrett
1974; Zuckerman
in men (Straub 1982). The present study examined
sexes practicing skydiving as a sport.
for was
sports, between
1979), with a
parachutists
of both
Frontal reactivity and sensation seeking
449
Inclusion Criteria Skydivers were recruited from a French center for sportive parachuting;
they had been jumping and
skydiving regularly for at least two years. Controls were recruited by advertising in public buildings and were matched for age, sex and social-cultural
background.
All subjects were volunteers
and were paid
(4OUS$) for taking part in the study. To be included they had to give a written consent. Each group consisted of twenty-two
subjects (16M, 6F).
Exclusion Criteria Interviews
were
conducted
psychiatric or neurological Psvchooatholonical
by a psychiatrist
to ensure
subjects: Montgomery
and Asberg Depressive
by Lemperiere
Echelle de Ralentissement Abrams-Taylor
17 item version (HRSD, Hamilton 1984) Tyrer Anxiety
et al 1989) and Widlbcher
Depressif,
Widlocher
Scale (Tyrer et al 1984; French
Depressive
Retardation
1983). Emotional disturbances
et al 1996). The EHD scale, consisting
structure based on five factors: anhedonia, hyper-emotionality, sadness, hyper-attentiveness.
Subjects also completed
Seeking
Sensation
(TAS),
factorial
emotional hyper-or hypo-expressiveness,
provides a more accurate overall
deficit. Two other clinical constructs
the following
questionnaires:
and Chapman
Seeking Scale (SSS-form
Experience
Jouvent et al 1988; Carton
(hyper-emotionality
and
assess lack of control.
et al 1976, Chapman
(Zuckerman
were assessed with the
of 20 items, has a coherent
and the conjugate use of these two clinical constructs
of blunted-affect/emotional
Zuckerman’s
Scale (ERD -
Two factors focus on emotional deficits: anhedonia and emotional hypo-
emotional hyper-expressiveness)
Chapman
and Asberg 1979),
Scale for Blunted AITect (AT, Abrams and Taylor 1978; French version by Ammar et al
et al 1992b; Bungener
assessment
a psychiatrist
1967), Covi Brief Anxiety
1983) and the Depressive Mood Scale (EHD - Echelle d’Humeur Depressive,
expressiveness
from
scales were used to rate the
Rating Scale (MADRS, Montgomery
et al 1981; Covi and Lipman
validated
as well as emotional disturbances,
interview with each subject. The following
Hamilton Rating Scale for Depression,
version
suffering
Evaluations
a semi-structured
Scale (Lipman
were
conditions or any visual problems that could interfere with the task.
To evaluate depressive and anxious symptomatology conducted
that no subjects
Seeking
et al 1964; French
Tridimensional-Personality-Questionnaire
(ES),
version
Chapman’s Physical Anhedonia
1978; French
version
validated
V, including four dimensions:
Disinhibition validated
(Dis)
by Carton
(TPQ, Cloninger
Scale (PAS,
by Loas
1993),
Thrill and Adventure
and Boredom
Susceptibility
et aI 1992b),
and the Cloninger
1987; French version validated
(BS)
by Lepine
A. Pierson et aI.
450
1994) indexing three independent
dimensions,
the dimension
of interest in this study being Novelty
Seeking (NS) ERP Procedure After clinical assessment, recording.
the subject was placed in a dimly-lit,
The subject was seated comfortably,
sound-attenuated
150 cm from the computer
chamber for ERP
screen where visual stimuli
were presented for the oddball task. The subject was asked to stare at a fixation point (0.5 cm x 0.5 cm white square) and to press a response
button as fast as possible after the target stimulus (3cm x 3cm
yellow square), but to ignore the non-target stimulus (red square). Two task conditions
were used with varying probability
non-target or 80% target/20% non-target).
of the target occurrence (20% target/llO%
Under each experimental
condition, the subject was presented
with stimuli until 30 responses had been obtained for the rare stimulus. The Inter-Stimulus-Interval varied at random between counterbalanced
1 set and 1.5 sec. The order of presentation
across subjects in each group. Test sessions
conducted before commencing
the ERP recording.
(ISI)
of the two task conditions
was
lasted 30 minutes. Training trials were
Subjects were asked to relax and to blink as little as
possible during the test. EEG was recorded international
from 9 electrodes
(Fpz, Fz, Cz, Pz, Oz, T3, T4, C3, C4) according
lo-20 system (Jasper 1958) with respect to a linked-earlobe
were embedded in a cap (Electrocap,
eye in order to reject trials contaminated and maintained
The EEG electrodes
Dallas, USA). The earth electrode was attached to the right cheek.
Two electrodes for bipolar recording of vertical ocular movements
was controlled
reference.
to the
by electro-oculogram
as being less than 2 kilo-ohms.
were placed above and under the left
(EOG 2 f 50 uV). Electrode
impedance
Signals were low-pass filtered at 25 Hz
and high-pass filtered at 0.16 Hz by analogue filters in the amplifiers.
Data were digitized on-line at a
sampling rate of 250 Hz using the InstEP system (Ottawa, Canada). The sampling period was 1024 msec (200 msec pre-stimulus
to 824 msec post-stimulus).
Assessment After elimination
of trials with excessive
eye movements,
according to task condition (target or non-target)
ERP were averaged
and response (correct, omission,
of the small number of errors observed in the task, only ERP corresponding analyzed;
corresponding
Reaction
Times (RT) were obtained
for each subject
false alarm). Because
to correct responses were
from the average procedure.
The ERP
recordings were then low-pass filtered (off-line procedure of the InstEP system) using a digital filter set at 12 Hz (-3 dB/octave). system using time-windows
Computer-assisted determined
scoring of ERP components
from grand-average
was realized
(overall subjects)
with InstEP
ERP. Peak amplitudes
were measured for the N2 and P3 components. N2 was measured at Fz between 200 msec and 350 msec
Frontal reactivity and sensation
seeking
451
P3 was measured at Fz and at Pz between 280 msec and 500 msec. Peak amplitudes with respect to the 200 msec pre-stimulus measuring peak-to-peak
amplitudes
baseline.
The frontal N2-P3
of these components
complex
were calculated was assessed
as well as their separate values
by
The P3b was
measured at the parietal site (Pz) The FzTz P3 amplitude ratio and RT were also analyzed. All scorings were performed
automatically
examined independently
by computer.
In case of aberrant measures,
individual recordings
were
by two judges to reach consensus
Statistical Analvsis Comparisons
between
demographic
and clinical parameters
for each group were tested using the
Mann and Whitney U-test. Analysis of Variance (ANOVA) was used to compare RT and amplitudes of the ERP components correction
when
Satterthwaite’s
in the two groups. Significance
appropriate.
approximation
of Bravais-Pearson)
Student
t-test
levels were adjusted using the Greenhouse-Geisser
was then used
for 2 x 2 planned
comparisons
with
for the degrees of freedom when variances were unequal. Correlations
were calculated
between the different
measures
affect, sensation seeking, novelty seeking). The level of significance
of interest (anhedonia,
(r
blunted-
was set at p < 05
Results One control subject was excluded therefore
consisted
of 22 skydivers
according to demographic
because of noisy EEG recordings and the control group of 21 subjects.
parameters (age, sex, social-professional
significant statistical differences
group
Pairing of the two groups
background)
was satisfactory
and no
were found. The mean age was 24.8 for both groups (Table 1)
Table Demographic
Age Cultural level* * the cultural level
The high risk-taking
Parameters
1
in the Two
Groups
of Subjects
Skydivers Controls Mann-Whitney 16 Men 15 Men 6 Women 6 Women (n=22) (n=21) m SD SD m U P 220.5 0.80 24.77 3.85 24.76 3.31 190.0 0.31 5.63 1.18 6.00 1.10 was scored from 1 = illiterate to 6 = long higher education
Clinical Results
The medical history, specifically A history of minor depressive
psychiatric disorders and addictions, were similar in the two groups.
episodes was mentioned
by 4 skydivers and 3 controls. Drugs had been
used, but rarely (less than three times) and only by a minority of subjects
in each group (hashish: 8
A. Pierson et al.
452
skydivers and 7 controls; heroin: 1 skydiver); 7 skydivers and 4 controls were smokers. No subjects suffered from any psychiatric disorder at the time of the experiment. This was confirmed by the low scores observed on the depression and anxiety scales in both groups. No difference between the two groups was observed for these scores. The data used for clinical and psychological assessments and the results of the statistical comparisons of the two groups are presented in Table 2. For Sensation Seeking, skydivers showed significantly more Thrill and Adventure Seeking and more Boredom Susceptibility than controls. There was a tendency for Experience Seeking to be greater in skydivers than in controls (p = ,064). Novelty Seeking as measured on the TPQ also tended to be greater in skydivers, but again the difference did not reach significance (p =.077; Table 2).
Scores
for Clinical
Table 2 and Personality Evaluations Groups of Subjects Skydivers n=22 m SD
3.95 MADRS (Montgomery and Asberg 1979) 3.05 HRSD (Hamilton 1967) 1.00 Covi (Covi and Lipman 1984) 4.63 Tyrer (Tyrer et al 1984) 0.59 Widlijcher ERD (WidlCicher 1983) 1.91 Abrams-Taylor (Abrams and Taylor 1978) 1.41 EHD F1:anhedonia (Jouvent et al 1988) 3.68 EHD F2:hyperemotivity -0.86 EHD F3:emotional expressiveness 0.77 EHD F4:sadness 0.86 EHD F5:anxious hyperattentivity 3.50 EHD:blunted-affect (Fl + F3 hypo) 4.91 EHD:lack of control (F2 + F3 hyper) Chapman PAS (Chapman and Chapman 14.95 1978) 9.23 Zuckerman:Thrill and Adventure (Zuckerman et al 1964) 6.64 Zuckerman:Experience Seeking 4.91 Zuckerman:Disinhibition 5.18 Zuckerman:Boredom Susceptibility TPQ Novelty Seeking (Cloninger 1987) 19.77 + * p1.05 ** p1.01
3.84
in the Two
Controls n=2 1 m SD 2.18 2.44
MannWhitney U p+ 174.5 .I62
2.68
1.73
I .64
171.5
.I41
1.02
0.86
I .08
214.5
,670
5.04
2.32
2.03
180.0
,210
0.73
0.68
1.67
187.0
.I97
2.39
0.41
1.18
128.0
.004
** *
1.99
0.50
1.37
159.5
,041
2.98
3.45
2.36
223.5
.854
0.99
0.59
2.58
221.0
,793
1.34
0.45
0.86
221.5
.770
0.99
0.77
0.87
221.0
,793
3.78
1.14
2.92
132.5
.008
3.90
4.68
3.29
223.5
.854
5.41
13.77
6.87
208.0
.575
0.61
7.36
2.42
137.5
.018
2.08
5.36
2.24
155.5
.064
2.05
4.59
2.87
200.0
.455
1.71
3.82
2.15
143.0
,030
3.90
17.36
6.18
158.5
,077
**
Another important observation concerns emotional blunting in skydivers. Compared to the controls, the skydivers had significantly higher level of both hetero- and self-rated emotional deficits. Higher
*
*
Frontal reactivity
and sensation seeking
453
scores were observed on both the Abram+Taylor blunted-affect scale and the Depressive Mood Scale (EHD - anhedonia and hypo-expressiveness). A positive correlation was also found for these self-rated (AT) and hetero-evaluated (EHD) deficits: Abrams-Taylor/EHD anhedonia [r(22) = .63, p = ,001 in skydivers, r(21) = 57, p < .Ol in controls], and Abrams-Taylor/EHD emotional hypo-expressiveness [r(22) = .75, p < .OOOlin skydivers, r(21) = .62, p < .Ol in controls]. No correlation was found between these indices of emotional deficits and sensation or novelty seeking within each group. However, another dimension of the EHD (lack of control) showed the two groups of subjects to be different, both for the personality trait (experience seeking in skydivers, novelty seeking in controls) and the direction of the correlation. A negative correlation was found in skydivers between experience seeking and both hyper-emotionality [r(21) = -.53, p < .Ol] and lack of control [r(21) = -.55, p < .Ol], whereas a positive correlation was found in controls between novelty seeking and both hyper- emotionality [r(22) = .61, p < ,011 and lack of control [r(22) = .51, p < ,021.
ERP and Behavioral Results ANOVA conducted for each parameter used two inter-group factors (Group: skydivers vs controls and Sex: males vs females) and two intra-group factors with two levels each (Target: targets vs nontargets and Proportion: 20/80% vs 80/20%). No main effect of sex was found; the results are therefore presented for males and females together.
No group effect was observed on RT (348 f 52 ms in skydivers vs 342 f 63 ms in controls)
Grand-average ERP traces are shown in Fig 1. ERP amplitudes are given in Table 3 ERP amplitudes revealed two main group effects. The first was that the frontal N2P3 peak-to-peak amplitude was greater for skydivers compared to controls in all experimental conditions (no interactions) (F(1,41) = 5.85, p < .02). This result seems to be mainly attributable to frontal P3 amplitudes, which were significantly greater in skydivers than in controls (p = -05) rather than to frontal N2 amplitudes which did not show any significant inter-group difference.
A further difference between the two groups was observed for the frontal/parietal P3 ratio (Fig 2) which was, on average, significantly higher in skydivers than in controls (F(1,41) = 3.96, p < .05). Again this result seems to be due to differences in frontal P3 amplitudes (Fz), since the parietal P3 component (Pz) did not show any significant difference in amplitude between the two groups. A Group x Target interaction did, however, indicate that the difference between the two groups was significant for non-targets only (t(84) = 2.47, p < .02). In skydivers, the frontal/par&al
P3 ratio was in fact
significantly greater for non-targets (0.76) than for targets (0.43) (t(76) = 3.77, p < ,001).
454
A. Pierson et al.
-00
x
2.31 4.71 5.06 5.59
-0.46 6.75 7.21 16.63
3.55 0.22 4.24 4.67 3.80 4.45 4.30 10.34
2.18 3.64 3.39 3.80
0.58 3.66 3.08 8.14
2.71 2.67 2.60 3.67
-2.83 11.71 14.54 16.13
3.37 5.70 5.49 5.95
-2.08 10.58 12.66 16.87
4.22 4.78 5.71 5.76
= Amplitude
* Amp.
Lat. = Latency
Conditions
1.30 0.30 1.48 2.37 1.55 1.44 2.73 1.25 2.02 3.11 4.49 2.10 0.75 0.59 0.40 0.41 345.8 44.6 364.4 75.3
0.67 3.10 3.03 5.60
Frequent Non-Targets Skydivers Controls m SD m SD
Experimental
Infrequent Non-Targets Skydivers Controls m SD m SD
Table 3 of Subjects for the Different
Frequent Targets Skydivers Controls m SD m SD
Groups
0.45 0.31 0.39 0.18 0.41 0.33 0.47 0.37 0.76 0.31 0.65 0.30 363.4 30.2 362.7 34.9 332.7 29.0 322.5 42.4 377.5 49.4 352.6 40.6
P3b
P3a/P3b
Amp
-1.12 7.14 8.26 16.93
Lat*
N2bP3a
P3b
Amp
N2b P3a
Amp
Amp* Amp
in the Two
Infrequent Targets Skydivers Controls m SD m SD
ERP Amplitudes
i
B I !z
!z
i 2 R 4g
7
456
A. Pierson et al.
FzfPz 1
.oo skydivers controls
0.80
@J
0.60
targets
nontargets
Fig 2 The ordinate gives the ratio of P3 amplitudes measured at Fz and Pz sites respectively (Fflz). This ratio was significantly larger in skydivers compared to controls only for non-targets. This was essentially due to a larger frontal (Fz) P3 in skydivers.
The other effects of the experimental probability
of occurrence
conditions were similar in both groups. The classic effect of the
of the stimulus on P3 amplitudes
infrequent compared to frequent stimulations, this typical effect was also observed amplitudes and N2P3 peak-to-peak
irrespective
was found, with a greater parietal P3 for
of target/non-target
for indices related to automatic
amplitude. A target/non-target
was also apparent in both groups of subjects, but depended amplitudes for targets greater than for non-targets,
classification.
processes,
Moreover,
frontal N2 and P3
effect on these same ERP parameters on the probability
of stimulation,
with
but only when stimuli were frequent (80%).
An Emotional Deficit in Skvdivers The main finding
of the present
(anhedonia and blunted-affect) any depressive
episode.
constitutes a trait.
study was that skydivers
presented
a larger emotional
deficit
than controls. These negative symptoms were observed independently
This point supports the argument
that the presence
of an emotional
of
deficit
Frontal reactivity
As was expected, sensation
and sensation
seeking
457
seeking (Thrill and Adventure Seeking, Boredom Susceptibility) was
greater in skydivers than in controls. The existence of negative symptoms in these subjects indicates that sensation seeking may be an adaptive reaction to emotional deficits. It could be assumed that with repetition, the sensation seeking value of jumps may be diminished. Indeed, it has been established that anxiety or fear are reported by both experienced and inexperienced subjects (according to a different time pattern), which would suggest that a jump always has a certain character of novelty (Schedlowski and Tewes 1992; Bockheler 1995). A number of psychological studies have pointed out how unique this threatening situation is (Galor and Tenenbaum 1986). Frontal P3 Amnlitude as an Index of Larger Orienting Reactions in Skvdivers Comnared to Controls From the cognitive point of view, the two groups of subjects did not show any significant difference in the effects of the two intra group variables on ERP (targets vs non-targets and frequent vs rare stimuli). This indicates, in particular, that controlled processes which are necessary to classify stimuli as being targets or non-targets were similar in skydivers and in controls. In contrast, there was an effect on ERP of the inter-group variable (skydivers vs controls): the frontal P3 component was larger in skydivers than in controls whatever could be the stimulus but this difference between the two groups was only significant for non-targets. As the non-target stimuli required more automatic processing, results are in favor of an increase of automatic processes in skydivers, compared to controls. Moreover, as frontal P3 amplitude (P3a) is known to index, with the preceding negative component (N2b), orienting response (Renault 1983, Niiatanen and Gaillard 1983, Wijers et al 1989) it could be suggested that skydivers have developed an ability to react automatically to all stimuli, including non-relevant stimuli. Why an Orienting Resnonse to Non-Relevant Stimuli in Skydivers? Sokolov’s theory of orienting (1963) postulates that orienting reflexes occur when recognizing novelty but also when recognizing any discriminable change in the stimulus
The basic finding of an
anteriorly distributed positivity (P3a), with a relatively shorter latency than the classical pa&al
P3
(P3b) in response to rare non-targets has been observed in a number of studies (Graham and Hackley, 1991). Sokolov (1960) proposed that the development of a neuronal model for repetitive stimuli should block inputs in the reticular formation. This accounts for habituation provoked by repetition and explains that the most frequent stimuli in an oddball task do not provoke as large orienting responses than rare stimuli. Before complete habituation, residual indices of orienting might however be observed for frequent stimuli and it is plausible that larger indices of orienting (here, NZb-P3a amplitude) in skydivers by comparison to controls may be related to a more important residual orienting response not only to rare but also to frequent non-targets (because, in comparison with controls, OR should be larger and/or because of a less rapid habituation).
458
A. Pierson et al.
What is the Orienting in an Oddball Task? It is common to consider after Lindsley (1970) that the orienting reflex results from a sudden increase in reticular or thalamic non-specific
activation.
response should have two components:
However Naatanen (1986) proposed that the orienting
an arousal component,
specific activation but also an attentional
component
resulting from a transient increase in non-
consisting
in a reflex-like
attention switch to the
eliciting stimulus. For his part, Sanders (1983) in his cognitive-energetical
model of arousal, stress and
performance
resources
perceptive proposed
related linear stages of information stages be dependent
be dependent
major neuroanatomical Williamson
to energetical
on arousal (phasic activation)
on tonic activation.
(1975) neurophysiological
processing
involved
in contrast to motor stages which he
This model is based upon the Pribram and McGuiness
scheme describing structures
and proposed that
three different systems in the control of attention and the in these processes.
In the same perspective,
Tucker and
(1984) consider the phasic arousal system as regulating the phasic response of the brain to
environmental
events and as being the primary mechanism
should be dependent on norepinephrine
The position
of Pribram
emotional processes are considered environmental characteristic
pathways.
(the tonic activation system being important to motivational
as the events.
processes
by which
the
brain
evaluates
In the same view, Tucker and Williamson
of the phasic arousal system and of its norepinephrine
form of depression
reflex. This mechanism
and MC Guiness (1975) is that the phasic arousal system is integral to
is coherent with catecholaminergic
the
processes).
subjective
Emotions
significance
of
(1984) suggest that the emotional substrate is depression-elation.
That
models of affective disorders that several authors relate to the only
with emotional deficit, in contrast with agitated and impulsive depression
be more dependent on serotoninergic An Impairment
of the orienting
that could
pathways (Jouvent et al 1991, Hansenne et al 1995, 1998).
in Frontal Structures of the Brain?
Although ERPs recorded at the frontal sites do not indicate that they originate from frontal sources, the question of such frontal generators
can be raised since some neuropsychological
syndrome
caused by, or involving,
deficiencies
depressive
state and lack of interest in the outside world (George et al 1994).
Several authors (George et al. 1994) consider govern the primitive unmodulated
behaviors
of the dorsomedial
that frontal regions
frontal
data describe a
cortex with a pseudo-
may in some way regulate or
(drives or natural tendencies)
which are ingrained in sub-
cortical structures and the limbic system. Other studies, principally those by Knight (1984), have observed a reduction in the amplitude of the P3 wave in reaction to novel stimuli in frontally lesioned patients and interpreted this as the expression
Frontal reactivity and sensation seeking
of a deficit in prefrontal
control of the external/sensory-intemablimbic
459
system. Knight
also
demonstrated that in normal subjects the frontal P3 was greater in amplitude, and that the frontahparietal P3 ratio was greater than 1, for novel stimuli. In the present study, while the fiontal/parietal P3 ratio is not greater than 1, the higher ratio for non-targets in skydivers compared to controls (0.76 vs 0.36) seems to suggest that skydivers show an abnormally strong orienting reaction towards non-targets. This could be due to an involvement of frontal structures in processing not only of novel or rare relevant stimuli but also of irrelevant stimuli in these individuals. The Development of Orienting as a Mean of Adaptation The increase of the P3a component amplitude in skydivers in comparison with controls is in opposition to what we found in depressed patients with blunted-atTect (Pierson et al 1991, Partiot et al 1993). The authors have shown that blunted-affect in depression was primarily related to abnormally low P3a amplitudes that they have interpreted as an impairment of orienting automatic processes, This deficit extended to cover controlled processes, but only for high effort-demanding tasks (Pierson et al, 1996). On the basis of Pribram and MC Guiness’s and Tucker and Williamson’s approaches, the larger OR observed in skydivers than in controls for non-target stimuli seem to indicate that skydivers give an emotional significance not only to relevant but also to irrelevant stimuli. The abnormal reactivity to nontargets of skydivers could be interpreted as an adaptive reinforcement procedure which consists in using the context as arousing stimuli. It may be suggested that skydiving is an adaptive form of behavior that contributes to the development of orienting reactions. Indeed, when individuals display a primary emotional deficit, two different attitudes are possible: either they let the emotional deficit take hold and (with time or because of specific events) reach a stage of clinical depression, or they react by developing certain adaptive forms of behavior aimed at compensating for the deficit. High-risk taking activity is one of these possible forms of adaptive behavior. This interpretation of skydiving as an active adaptation procedure is reinforced by the existence of correlations showing that while skydivers register the highest scores for experience seeking, they record the lowest scores for hyper-emotionality and lack of control. Their experience seeking is not an impulsive behavior resulting from lack of control. This last result is coherent with an improvement in the orienting attentional component. Conclusion: The Frontal P3 Amplitude as an Index of Adaptive Capacities Examining two populations with emotional deficits, we observed opposite results concerning some indices of orienting (P3a amplitude). The former population (depressed patients), examined in a previous work (Pierson et al 1991, Partiot et al 1993), showed a deficit in these indices whereas the
460
A. Pierson et al.
other population development emotional
(skydivers),
examined
of these indices than control deficits,
in the present
study,
showed,
subjects. This opposition
the frontal P3 amplitude
measured
on the contrary,
a larger
suggests that, in individuals
in reaction
with
time tasks does not reflect the
emotional deficit per se. We suggest that it rather reflects the capacity to use some behaviors
which
improve
could
automatic
counterbalance
attentional
the emotional
processes
in order
deficit. Depressions
to
obtain
with emotional
arousing
stimulation
that
deficit might be due to the lack of
such a capacity.
Acknowledgement The authors thank B. Renault and R Ragot for their valuable comments in revision qf manuscript
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& BioL
Psychic&.
1999, Vol. 23, pp. 447463 1999 Ekvier Science Inc.
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0278~5844/99/$-sm
ELSEVIER
PlI
FROIUTAL REACTMTY
so2?8-5846(99pnmQa-
fmnt matter
1
AND SENSATION SEEKING AN ERP STUDY IN SKYDIVERS
ANNICK PIERSON, JACQUES LE HOUEZEC, ARNAUD FOSSAERT, STEPHANIE DUBAL and ROLAND JOUVENT CNRS UMR 7593, H6pital de la Salp&i&e, Paris, France
(Final form, March 1999)
Abstract Pierson Annick, Jacques Le Houezec, Amaud Fossaert, StP;phanie Dubal and Roland Jouvent: Frontal Reactivity and Sensation Seeking: An ERP Study in Skydivers. Prog. Neuro-Psychopharmacol. & Biol. Psychiat. 1999,2& pp. 447463.81999 ElsevierScienazInc. 1.
2. 3.
4.
In the line of Zuckerman’s studies on sensation seeking and optimal level of arousal, the authors hypothesized that high sensation seeking might be used to compensate for anhedonia due to basal arousal deficit. A population of interest was found with parachutists practicing skydiving, generally described aa very high sensation seekers. After clinical assessment of emotional and affective components, amplitudes of the frontal P3 of the ERP were used as indices of arousal. Skydivers presented more negative symptoms (anhedonia and blunted-affect) than controls. This was observed in isolation from any depressive episode, which would suggest the presence of emotional deficit as a trait. As expected, skydivers presented more sensation seeking than controls. These two results taken together could indicate that sensation seeking is an adaptive reaction to anhedonia. ERP results showed that l?ontal P3 amplitudes were larger in skydivers than in controls, whereas in a previous study we showed the opposite in depressed patients with a similar emotional deficit. This could indicate that the frontal P3 amplitude does not reflect the emotional deficit per se. We suggest that it rather reflects the capacity to use some behaviors which improve automatic attentional processes in order to obtain arousing stimulation that could counterbalance the emotional deficit. Depressions with emotional deficit might be due to the lack of such a capacity.
Kev_words: emotional deficit, ERP, frontal reactivity, negative symptoms, orienting reflex, personality, sensation seeking. Abbreviations: Abram+Taylor blunted-affect scale (AT), Cchelle d’humeur depressive - depressive mood scale (EHD), 6chelle de ralentissement dkpressif - depressive retardation scale (ERD), event related potentials (E&P), Hamilton rating scale for depression (I-IRSD), Montgomery and Asberg depressive rating scale (MADRS), orienting reflex (OR), reaction time (RT), t&personality questionnaire (TPQ).
A. Pierson et
448
al.
Introduction Sensation
seeking was described
novel and complex sensations the sake of experience”. physiological perspective,
by Zuckerman
and experiences
Zuckerman
basis for the sensation
(1979) as a “trait defined by the need for varied,
and the willingness
et al (1972) asserted
to take physical and social risks for
that the optimal
seeking trait. Such an approach
is in keeping with a biological
being based upon Berlyne’s (1950) and Hebb’s (1955) concept
arousal and upon Eysenck
and Eysenck’s
later theory
hypothesis was that certain personality traits (extraversion chronic under-arousal
which makes these individuals
level of arousal is the
incorporating
of an optimal level of
this same notion.
Eysenck’s
for the case in question) may be explained by
seek sources of stimulation
so as to increase their
arousal to an hedonic point (Eysenck and Eysenck 1978). Following between
along the same lines, our group conducted
sensation-seeking
and emotional
research, the authors concluded sensations
and to compensate
that high sensation
i.e. blunted-affect
the relationships
and anhedonia.
seeking can be considered
From this
as intended to provide
for anhedonia due to a basal arousal deficit (Carton et al 1992a). It was
also shown that frontal P3 amplitudes retardation
deficiency,
several studies investigating
and blunted-affect,
were abnormally
and a correlation
low in depressed
patients with psychomotor
was observed between frontal amplitude and negative
symptoms (Pierson et al 1991; Partiot et al 1993). The present study was designed to investigate
indices of frontal dysfunction
in subjects presenting
a
sensation seeking trait. The task selected was designed to analyze cortical indices of arousal related to certain cognitive processes by manipulating 1) the probability
of occurrence
two experimental
of the stimulus,
variables:
which
mainly
required
automatic
orienting
processes, 2) the classification
of the stimulus as being a target or a non-target for a motor response, that mainly
required selective attentional (and therefore controlled) processes. The task consisted
in differentiating
two types of stimulus presented
in different
proportions,
with
either frequent or rare stimuli being the target for the motor response (oddball task). Working on the assumption that sensation seeking is an adaptive behavior intended to compensate basal anhedonia
or blunted-affect,
made. A population
of interest
a clinical emotional
and affective
for such a study appeared
evaluation
of the subjects
to be people practicing
high-risk
generally described as very high sensation seekers. Several studies have reported relationships sensation
seeking and the practice of sport (Hymbaugh
higher relationship
observed
and Garrett
1974; Zuckerman
in men (Straub 1982). The present study examined
sexes practicing skydiving as a sport.
for was
sports, between
1979), with a
parachutists
of both
Frontal reactivity and sensation seeking
449
Inclusion Criteria Skydivers were recruited from a French center for sportive parachuting;
they had been jumping and
skydiving regularly for at least two years. Controls were recruited by advertising in public buildings and were matched for age, sex and social-cultural
background.
All subjects were volunteers
and were paid
(4OUS$) for taking part in the study. To be included they had to give a written consent. Each group consisted of twenty-two
subjects (16M, 6F).
Exclusion Criteria Interviews
were
conducted
psychiatric or neurological Psvchooatholonical
by a psychiatrist
to ensure
subjects: Montgomery
and Asberg Depressive
by Lemperiere
Echelle de Ralentissement Abrams-Taylor
17 item version (HRSD, Hamilton 1984) Tyrer Anxiety
et al 1989) and Widlbcher
Depressif,
Widlocher
Scale (Tyrer et al 1984; French
Depressive
Retardation
1983). Emotional disturbances
et al 1996). The EHD scale, consisting
structure based on five factors: anhedonia, hyper-emotionality, sadness, hyper-attentiveness.
Subjects also completed
Seeking
Sensation
(TAS),
factorial
emotional hyper-or hypo-expressiveness,
provides a more accurate overall
deficit. Two other clinical constructs
the following
questionnaires:
and Chapman
Seeking Scale (SSS-form
Experience
Jouvent et al 1988; Carton
(hyper-emotionality
and
assess lack of control.
et al 1976, Chapman
(Zuckerman
were assessed with the
of 20 items, has a coherent
and the conjugate use of these two clinical constructs
of blunted-affect/emotional
Zuckerman’s
Scale (ERD -
Two factors focus on emotional deficits: anhedonia and emotional hypo-
emotional hyper-expressiveness)
Chapman
and Asberg 1979),
Scale for Blunted AITect (AT, Abrams and Taylor 1978; French version by Ammar et al
et al 1992b; Bungener
assessment
a psychiatrist
1967), Covi Brief Anxiety
1983) and the Depressive Mood Scale (EHD - Echelle d’Humeur Depressive,
expressiveness
from
scales were used to rate the
Rating Scale (MADRS, Montgomery
et al 1981; Covi and Lipman
validated
as well as emotional disturbances,
interview with each subject. The following
Hamilton Rating Scale for Depression,
version
suffering
Evaluations
a semi-structured
Scale (Lipman
were
conditions or any visual problems that could interfere with the task.
To evaluate depressive and anxious symptomatology conducted
that no subjects
Seeking
et al 1964; French
Tridimensional-Personality-Questionnaire
(ES),
version
Chapman’s Physical Anhedonia
1978; French
version
validated
V, including four dimensions:
Disinhibition validated
(Dis)
by Carton
(TPQ, Cloninger
Scale (PAS,
by Loas
1993),
Thrill and Adventure
and Boredom
Susceptibility
et aI 1992b),
and the Cloninger
1987; French version validated
(BS)
by Lepine
A. Pierson et aI.
450
1994) indexing three independent
dimensions,
the dimension
of interest in this study being Novelty
Seeking (NS) ERP Procedure After clinical assessment, recording.
the subject was placed in a dimly-lit,
The subject was seated comfortably,
sound-attenuated
150 cm from the computer
chamber for ERP
screen where visual stimuli
were presented for the oddball task. The subject was asked to stare at a fixation point (0.5 cm x 0.5 cm white square) and to press a response
button as fast as possible after the target stimulus (3cm x 3cm
yellow square), but to ignore the non-target stimulus (red square). Two task conditions
were used with varying probability
non-target or 80% target/20% non-target).
of the target occurrence (20% target/llO%
Under each experimental
condition, the subject was presented
with stimuli until 30 responses had been obtained for the rare stimulus. The Inter-Stimulus-Interval varied at random between counterbalanced
1 set and 1.5 sec. The order of presentation
across subjects in each group. Test sessions
conducted before commencing
the ERP recording.
(ISI)
of the two task conditions
was
lasted 30 minutes. Training trials were
Subjects were asked to relax and to blink as little as
possible during the test. EEG was recorded international
from 9 electrodes
(Fpz, Fz, Cz, Pz, Oz, T3, T4, C3, C4) according
lo-20 system (Jasper 1958) with respect to a linked-earlobe
were embedded in a cap (Electrocap,
eye in order to reject trials contaminated and maintained
The EEG electrodes
Dallas, USA). The earth electrode was attached to the right cheek.
Two electrodes for bipolar recording of vertical ocular movements
was controlled
reference.
to the
by electro-oculogram
as being less than 2 kilo-ohms.
were placed above and under the left
(EOG 2 f 50 uV). Electrode
impedance
Signals were low-pass filtered at 25 Hz
and high-pass filtered at 0.16 Hz by analogue filters in the amplifiers.
Data were digitized on-line at a
sampling rate of 250 Hz using the InstEP system (Ottawa, Canada). The sampling period was 1024 msec (200 msec pre-stimulus
to 824 msec post-stimulus).
Assessment After elimination
of trials with excessive
eye movements,
according to task condition (target or non-target)
ERP were averaged
and response (correct, omission,
of the small number of errors observed in the task, only ERP corresponding analyzed;
corresponding
Reaction
Times (RT) were obtained
for each subject
false alarm). Because
to correct responses were
from the average procedure.
The ERP
recordings were then low-pass filtered (off-line procedure of the InstEP system) using a digital filter set at 12 Hz (-3 dB/octave). system using time-windows
Computer-assisted determined
scoring of ERP components
from grand-average
was realized
(overall subjects)
with InstEP
ERP. Peak amplitudes
were measured for the N2 and P3 components. N2 was measured at Fz between 200 msec and 350 msec
Frontal reactivity and sensation
seeking
451
P3 was measured at Fz and at Pz between 280 msec and 500 msec. Peak amplitudes with respect to the 200 msec pre-stimulus measuring peak-to-peak
amplitudes
baseline.
The frontal N2-P3
of these components
complex
were calculated was assessed
as well as their separate values
by
The P3b was
measured at the parietal site (Pz) The FzTz P3 amplitude ratio and RT were also analyzed. All scorings were performed
automatically
examined independently
by computer.
In case of aberrant measures,
individual recordings
were
by two judges to reach consensus
Statistical Analvsis Comparisons
between
demographic
and clinical parameters
for each group were tested using the
Mann and Whitney U-test. Analysis of Variance (ANOVA) was used to compare RT and amplitudes of the ERP components correction
when
Satterthwaite’s
in the two groups. Significance
appropriate.
approximation
of Bravais-Pearson)
Student
t-test
levels were adjusted using the Greenhouse-Geisser
was then used
for 2 x 2 planned
comparisons
with
for the degrees of freedom when variances were unequal. Correlations
were calculated
between the different
measures
affect, sensation seeking, novelty seeking). The level of significance
of interest (anhedonia,
(r
blunted-
was set at p < 05
Results One control subject was excluded therefore
consisted
of 22 skydivers
according to demographic
because of noisy EEG recordings and the control group of 21 subjects.
parameters (age, sex, social-professional
significant statistical differences
group
Pairing of the two groups
background)
was satisfactory
and no
were found. The mean age was 24.8 for both groups (Table 1)
Table Demographic
Age Cultural level* * the cultural level
The high risk-taking
Parameters
1
in the Two
Groups
of Subjects
Skydivers Controls Mann-Whitney 16 Men 15 Men 6 Women 6 Women (n=22) (n=21) m SD SD m U P 220.5 0.80 24.77 3.85 24.76 3.31 190.0 0.31 5.63 1.18 6.00 1.10 was scored from 1 = illiterate to 6 = long higher education
Clinical Results
The medical history, specifically A history of minor depressive
psychiatric disorders and addictions, were similar in the two groups.
episodes was mentioned
by 4 skydivers and 3 controls. Drugs had been
used, but rarely (less than three times) and only by a minority of subjects
in each group (hashish: 8
A. Pierson et al.
452
skydivers and 7 controls; heroin: 1 skydiver); 7 skydivers and 4 controls were smokers. No subjects suffered from any psychiatric disorder at the time of the experiment. This was confirmed by the low scores observed on the depression and anxiety scales in both groups. No difference between the two groups was observed for these scores. The data used for clinical and psychological assessments and the results of the statistical comparisons of the two groups are presented in Table 2. For Sensation Seeking, skydivers showed significantly more Thrill and Adventure Seeking and more Boredom Susceptibility than controls. There was a tendency for Experience Seeking to be greater in skydivers than in controls (p = ,064). Novelty Seeking as measured on the TPQ also tended to be greater in skydivers, but again the difference did not reach significance (p =.077; Table 2).
Scores
for Clinical
Table 2 and Personality Evaluations Groups of Subjects Skydivers n=22 m SD
3.95 MADRS (Montgomery and Asberg 1979) 3.05 HRSD (Hamilton 1967) 1.00 Covi (Covi and Lipman 1984) 4.63 Tyrer (Tyrer et al 1984) 0.59 Widlijcher ERD (WidlCicher 1983) 1.91 Abrams-Taylor (Abrams and Taylor 1978) 1.41 EHD F1:anhedonia (Jouvent et al 1988) 3.68 EHD F2:hyperemotivity -0.86 EHD F3:emotional expressiveness 0.77 EHD F4:sadness 0.86 EHD F5:anxious hyperattentivity 3.50 EHD:blunted-affect (Fl + F3 hypo) 4.91 EHD:lack of control (F2 + F3 hyper) Chapman PAS (Chapman and Chapman 14.95 1978) 9.23 Zuckerman:Thrill and Adventure (Zuckerman et al 1964) 6.64 Zuckerman:Experience Seeking 4.91 Zuckerman:Disinhibition 5.18 Zuckerman:Boredom Susceptibility TPQ Novelty Seeking (Cloninger 1987) 19.77 + * p1.05 ** p1.01
3.84
in the Two
Controls n=2 1 m SD 2.18 2.44
MannWhitney U p+ 174.5 .I62
2.68
1.73
I .64
171.5
.I41
1.02
0.86
I .08
214.5
,670
5.04
2.32
2.03
180.0
,210
0.73
0.68
1.67
187.0
.I97
2.39
0.41
1.18
128.0
.004
** *
1.99
0.50
1.37
159.5
,041
2.98
3.45
2.36
223.5
.854
0.99
0.59
2.58
221.0
,793
1.34
0.45
0.86
221.5
.770
0.99
0.77
0.87
221.0
,793
3.78
1.14
2.92
132.5
.008
3.90
4.68
3.29
223.5
.854
5.41
13.77
6.87
208.0
.575
0.61
7.36
2.42
137.5
.018
2.08
5.36
2.24
155.5
.064
2.05
4.59
2.87
200.0
.455
1.71
3.82
2.15
143.0
,030
3.90
17.36
6.18
158.5
,077
**
Another important observation concerns emotional blunting in skydivers. Compared to the controls, the skydivers had significantly higher level of both hetero- and self-rated emotional deficits. Higher
*
*
Frontal reactivity
and sensation seeking
453
scores were observed on both the Abram+Taylor blunted-affect scale and the Depressive Mood Scale (EHD - anhedonia and hypo-expressiveness). A positive correlation was also found for these self-rated (AT) and hetero-evaluated (EHD) deficits: Abrams-Taylor/EHD anhedonia [r(22) = .63, p = ,001 in skydivers, r(21) = 57, p < .Ol in controls], and Abrams-Taylor/EHD emotional hypo-expressiveness [r(22) = .75, p < .OOOlin skydivers, r(21) = .62, p < .Ol in controls]. No correlation was found between these indices of emotional deficits and sensation or novelty seeking within each group. However, another dimension of the EHD (lack of control) showed the two groups of subjects to be different, both for the personality trait (experience seeking in skydivers, novelty seeking in controls) and the direction of the correlation. A negative correlation was found in skydivers between experience seeking and both hyper-emotionality [r(21) = -.53, p < .Ol] and lack of control [r(21) = -.55, p < .Ol], whereas a positive correlation was found in controls between novelty seeking and both hyper- emotionality [r(22) = .61, p < ,011 and lack of control [r(22) = .51, p < ,021.
ERP and Behavioral Results ANOVA conducted for each parameter used two inter-group factors (Group: skydivers vs controls and Sex: males vs females) and two intra-group factors with two levels each (Target: targets vs nontargets and Proportion: 20/80% vs 80/20%). No main effect of sex was found; the results are therefore presented for males and females together.
No group effect was observed on RT (348 f 52 ms in skydivers vs 342 f 63 ms in controls)
Grand-average ERP traces are shown in Fig 1. ERP amplitudes are given in Table 3 ERP amplitudes revealed two main group effects. The first was that the frontal N2P3 peak-to-peak amplitude was greater for skydivers compared to controls in all experimental conditions (no interactions) (F(1,41) = 5.85, p < .02). This result seems to be mainly attributable to frontal P3 amplitudes, which were significantly greater in skydivers than in controls (p = -05) rather than to frontal N2 amplitudes which did not show any significant inter-group difference.
A further difference between the two groups was observed for the frontal/parietal P3 ratio (Fig 2) which was, on average, significantly higher in skydivers than in controls (F(1,41) = 3.96, p < .05). Again this result seems to be due to differences in frontal P3 amplitudes (Fz), since the parietal P3 component (Pz) did not show any significant difference in amplitude between the two groups. A Group x Target interaction did, however, indicate that the difference between the two groups was significant for non-targets only (t(84) = 2.47, p < .02). In skydivers, the frontal/par&al
P3 ratio was in fact
significantly greater for non-targets (0.76) than for targets (0.43) (t(76) = 3.77, p < ,001).
454
A. Pierson et al.
-00
x
2.31 4.71 5.06 5.59
-0.46 6.75 7.21 16.63
3.55 0.22 4.24 4.67 3.80 4.45 4.30 10.34
2.18 3.64 3.39 3.80
0.58 3.66 3.08 8.14
2.71 2.67 2.60 3.67
-2.83 11.71 14.54 16.13
3.37 5.70 5.49 5.95
-2.08 10.58 12.66 16.87
4.22 4.78 5.71 5.76
= Amplitude
* Amp.
Lat. = Latency
Conditions
1.30 0.30 1.48 2.37 1.55 1.44 2.73 1.25 2.02 3.11 4.49 2.10 0.75 0.59 0.40 0.41 345.8 44.6 364.4 75.3
0.67 3.10 3.03 5.60
Frequent Non-Targets Skydivers Controls m SD m SD
Experimental
Infrequent Non-Targets Skydivers Controls m SD m SD
Table 3 of Subjects for the Different
Frequent Targets Skydivers Controls m SD m SD
Groups
0.45 0.31 0.39 0.18 0.41 0.33 0.47 0.37 0.76 0.31 0.65 0.30 363.4 30.2 362.7 34.9 332.7 29.0 322.5 42.4 377.5 49.4 352.6 40.6
P3b
P3a/P3b
Amp
-1.12 7.14 8.26 16.93
Lat*
N2bP3a
P3b
Amp
N2b P3a
Amp
Amp* Amp
in the Two
Infrequent Targets Skydivers Controls m SD m SD
ERP Amplitudes
i
B I !z
!z
i 2 R 4g
7
456
A. Pierson et al.
FzfPz 1
.oo skydivers controls
0.80
@J
0.60
targets
nontargets
Fig 2 The ordinate gives the ratio of P3 amplitudes measured at Fz and Pz sites respectively (Fflz). This ratio was significantly larger in skydivers compared to controls only for non-targets. This was essentially due to a larger frontal (Fz) P3 in skydivers.
The other effects of the experimental probability
of occurrence
conditions were similar in both groups. The classic effect of the
of the stimulus on P3 amplitudes
infrequent compared to frequent stimulations, this typical effect was also observed amplitudes and N2P3 peak-to-peak
irrespective
was found, with a greater parietal P3 for
of target/non-target
for indices related to automatic
amplitude. A target/non-target
was also apparent in both groups of subjects, but depended amplitudes for targets greater than for non-targets,
classification.
processes,
Moreover,
frontal N2 and P3
effect on these same ERP parameters on the probability
of stimulation,
with
but only when stimuli were frequent (80%).
An Emotional Deficit in Skvdivers The main finding
of the present
(anhedonia and blunted-affect) any depressive
episode.
constitutes a trait.
study was that skydivers
presented
a larger emotional
deficit
than controls. These negative symptoms were observed independently
This point supports the argument
that the presence
of an emotional
of
deficit
Frontal reactivity
As was expected, sensation
and sensation
seeking
457
seeking (Thrill and Adventure Seeking, Boredom Susceptibility) was
greater in skydivers than in controls. The existence of negative symptoms in these subjects indicates that sensation seeking may be an adaptive reaction to emotional deficits. It could be assumed that with repetition, the sensation seeking value of jumps may be diminished. Indeed, it has been established that anxiety or fear are reported by both experienced and inexperienced subjects (according to a different time pattern), which would suggest that a jump always has a certain character of novelty (Schedlowski and Tewes 1992; Bockheler 1995). A number of psychological studies have pointed out how unique this threatening situation is (Galor and Tenenbaum 1986). Frontal P3 Amnlitude as an Index of Larger Orienting Reactions in Skvdivers Comnared to Controls From the cognitive point of view, the two groups of subjects did not show any significant difference in the effects of the two intra group variables on ERP (targets vs non-targets and frequent vs rare stimuli). This indicates, in particular, that controlled processes which are necessary to classify stimuli as being targets or non-targets were similar in skydivers and in controls. In contrast, there was an effect on ERP of the inter-group variable (skydivers vs controls): the frontal P3 component was larger in skydivers than in controls whatever could be the stimulus but this difference between the two groups was only significant for non-targets. As the non-target stimuli required more automatic processing, results are in favor of an increase of automatic processes in skydivers, compared to controls. Moreover, as frontal P3 amplitude (P3a) is known to index, with the preceding negative component (N2b), orienting response (Renault 1983, Niiatanen and Gaillard 1983, Wijers et al 1989) it could be suggested that skydivers have developed an ability to react automatically to all stimuli, including non-relevant stimuli. Why an Orienting Resnonse to Non-Relevant Stimuli in Skydivers? Sokolov’s theory of orienting (1963) postulates that orienting reflexes occur when recognizing novelty but also when recognizing any discriminable change in the stimulus
The basic finding of an
anteriorly distributed positivity (P3a), with a relatively shorter latency than the classical pa&al
P3
(P3b) in response to rare non-targets has been observed in a number of studies (Graham and Hackley, 1991). Sokolov (1960) proposed that the development of a neuronal model for repetitive stimuli should block inputs in the reticular formation. This accounts for habituation provoked by repetition and explains that the most frequent stimuli in an oddball task do not provoke as large orienting responses than rare stimuli. Before complete habituation, residual indices of orienting might however be observed for frequent stimuli and it is plausible that larger indices of orienting (here, NZb-P3a amplitude) in skydivers by comparison to controls may be related to a more important residual orienting response not only to rare but also to frequent non-targets (because, in comparison with controls, OR should be larger and/or because of a less rapid habituation).
458
A. Pierson et al.
What is the Orienting in an Oddball Task? It is common to consider after Lindsley (1970) that the orienting reflex results from a sudden increase in reticular or thalamic non-specific
activation.
response should have two components:
However Naatanen (1986) proposed that the orienting
an arousal component,
specific activation but also an attentional
component
resulting from a transient increase in non-
consisting
in a reflex-like
attention switch to the
eliciting stimulus. For his part, Sanders (1983) in his cognitive-energetical
model of arousal, stress and
performance
resources
perceptive proposed
related linear stages of information stages be dependent
be dependent
major neuroanatomical Williamson
to energetical
on arousal (phasic activation)
on tonic activation.
(1975) neurophysiological
processing
involved
in contrast to motor stages which he
This model is based upon the Pribram and McGuiness
scheme describing structures
and proposed that
three different systems in the control of attention and the in these processes.
In the same perspective,
Tucker and
(1984) consider the phasic arousal system as regulating the phasic response of the brain to
environmental
events and as being the primary mechanism
should be dependent on norepinephrine
The position
of Pribram
emotional processes are considered environmental characteristic
pathways.
(the tonic activation system being important to motivational
as the events.
processes
by which
the
brain
evaluates
In the same view, Tucker and Williamson
of the phasic arousal system and of its norepinephrine
form of depression
reflex. This mechanism
and MC Guiness (1975) is that the phasic arousal system is integral to
is coherent with catecholaminergic
the
processes).
subjective
Emotions
significance
of
(1984) suggest that the emotional substrate is depression-elation.
That
models of affective disorders that several authors relate to the only
with emotional deficit, in contrast with agitated and impulsive depression
be more dependent on serotoninergic An Impairment
of the orienting
that could
pathways (Jouvent et al 1991, Hansenne et al 1995, 1998).
in Frontal Structures of the Brain?
Although ERPs recorded at the frontal sites do not indicate that they originate from frontal sources, the question of such frontal generators
can be raised since some neuropsychological
syndrome
caused by, or involving,
deficiencies
depressive
state and lack of interest in the outside world (George et al 1994).
Several authors (George et al. 1994) consider govern the primitive unmodulated
behaviors
of the dorsomedial
that frontal regions
frontal
data describe a
cortex with a pseudo-
may in some way regulate or
(drives or natural tendencies)
which are ingrained in sub-
cortical structures and the limbic system. Other studies, principally those by Knight (1984), have observed a reduction in the amplitude of the P3 wave in reaction to novel stimuli in frontally lesioned patients and interpreted this as the expression
Frontal reactivity and sensation seeking
of a deficit in prefrontal
control of the external/sensory-intemablimbic
459
system. Knight
also
demonstrated that in normal subjects the frontal P3 was greater in amplitude, and that the frontahparietal P3 ratio was greater than 1, for novel stimuli. In the present study, while the fiontal/parietal P3 ratio is not greater than 1, the higher ratio for non-targets in skydivers compared to controls (0.76 vs 0.36) seems to suggest that skydivers show an abnormally strong orienting reaction towards non-targets. This could be due to an involvement of frontal structures in processing not only of novel or rare relevant stimuli but also of irrelevant stimuli in these individuals. The Development of Orienting as a Mean of Adaptation The increase of the P3a component amplitude in skydivers in comparison with controls is in opposition to what we found in depressed patients with blunted-atTect (Pierson et al 1991, Partiot et al 1993). The authors have shown that blunted-affect in depression was primarily related to abnormally low P3a amplitudes that they have interpreted as an impairment of orienting automatic processes, This deficit extended to cover controlled processes, but only for high effort-demanding tasks (Pierson et al, 1996). On the basis of Pribram and MC Guiness’s and Tucker and Williamson’s approaches, the larger OR observed in skydivers than in controls for non-target stimuli seem to indicate that skydivers give an emotional significance not only to relevant but also to irrelevant stimuli. The abnormal reactivity to nontargets of skydivers could be interpreted as an adaptive reinforcement procedure which consists in using the context as arousing stimuli. It may be suggested that skydiving is an adaptive form of behavior that contributes to the development of orienting reactions. Indeed, when individuals display a primary emotional deficit, two different attitudes are possible: either they let the emotional deficit take hold and (with time or because of specific events) reach a stage of clinical depression, or they react by developing certain adaptive forms of behavior aimed at compensating for the deficit. High-risk taking activity is one of these possible forms of adaptive behavior. This interpretation of skydiving as an active adaptation procedure is reinforced by the existence of correlations showing that while skydivers register the highest scores for experience seeking, they record the lowest scores for hyper-emotionality and lack of control. Their experience seeking is not an impulsive behavior resulting from lack of control. This last result is coherent with an improvement in the orienting attentional component. Conclusion: The Frontal P3 Amplitude as an Index of Adaptive Capacities Examining two populations with emotional deficits, we observed opposite results concerning some indices of orienting (P3a amplitude). The former population (depressed patients), examined in a previous work (Pierson et al 1991, Partiot et al 1993), showed a deficit in these indices whereas the
460
A. Pierson et al.
other population development emotional
(skydivers),
examined
of these indices than control deficits,
in the present
study,
showed,
subjects. This opposition
the frontal P3 amplitude
measured
on the contrary,
a larger
suggests that, in individuals
in reaction
with
time tasks does not reflect the
emotional deficit per se. We suggest that it rather reflects the capacity to use some behaviors
which
improve
could
automatic
counterbalance
attentional
the emotional
processes
in order
deficit. Depressions
to
obtain
with emotional
arousing
stimulation
that
deficit might be due to the lack of
such a capacity.
Acknowledgement The authors thank B. Renault and R Ragot for their valuable comments in revision qf manuscript
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