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The tridimensional personality questionnaire and the intensity dependence of auditory evoked dipole source activity
The Tridimensional Personality Questionnaire and the Intensity Dependence of Auditory Evoked Dipole Source Activity Georg Juckel, Lutz G. Schmidt, Hans Rommelspacher, and Ulrich Hegerl
The relationship between the tridimensional personality questionnaire's (TPQ) dimensions "novelty seeking," "harm avoidance, "and "reward dependence" and the intensity dependence of the auditory evoked N1/P2-component was investigated in healthy subjects. Using dipole source analysis, evoked activity of the primary auditory cortex (tangential dipole) could be analyzed at least in part separately from that of secondary auditory areas (radial dipole). It was found that the intensity dependence of the tangential dipole was positively correlated to the TPQ dimension "novelty seeking," but not to "harm avoidance" and "reward dependence." This is in line with findings concerning similar personality traits like "sensation seeking," "impulsivity," or "extraversion." It is therefore concluded that a strong intensity dependence may characterize subjects with an action-oriented and extroverted personality style. The results are discussed within the concept that a low central serotonergic neurotransmission is underlying both an impulsive personality type and a strong intensity dependence of the tangential dipole.
Key Words: Personality, sensation seeking, auditory evoked potentials, serotonin, alcohol
Introduction Cortical processing of different stimulus intensities, reflected by the intensity dependence of sensory evoked potentials, seems to be related to certain kinds of personality traits. There is now converging evidence that subjects showing a strong increase of their evoked potential amplitudes with increasing stimulus intensity (components later than 50 msec after the stimulus: N1 and P2 component) are characterized by higher orientation to the environment and by a more action-oriented behavior than subjects showing From the Laboratory of Clinical Psychophysiology (GJ, UH); and Clinical Research Group "Neurobiological Mechanisms of Drug Addiction," (GJ, LGS, HR, UH); Department of Psychiatry, Freie Universit~it Berlin, Berlin, Germany. Address reprint requests to Priv.-Doz. Dr. U. Hegerl, Psychiatrische Klinik, Ludwig--Maximilians--Universit~it Mtinchen, Nui3baumstr. 7 80336 Miiochert, Germany. Received October 8, 1993; revised March 30, 1994.
© 1995 Society of Biological Psychiatry
weak increase or decrease of their amplitude values with increasing intensity. A strong intensity dependence of auditory and visual evoked potentials (AEP, VEP) has been found in subject with high values of the "sensation seeking" scale developed by Zuckerman (1979), especially in the subdimension "disinhibition" (Hegerl et al 1989; Zuckerman et a11988; Stenberg et a11988; Lukas 1987; for reviews see Carrillo-de-la-Pena 1992; Zuckerman 1990). A relationship in the same direction was also described for "cognitive and motor impulsivity" (VEP; Barratt et al 1987) and Eysenk's (1967) dimension "extroversion" (AEP, VEP; Stenberg et al 1988; Friedman and Meares 1979; Soskis and Shagass 1974). The literature is quite consistent on this issue, although some negative and even one contradictory findings have been reported (Lolas et al 1989; Bruneau et al 1984; Haler et al 1984). These deviating findings were 0006-3223/95/$09.50 SSDI 0006-3223(94)00118-M
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interpreted in terms of attention effects (Stenberg et al 1990) or methodological differences (Carrillo-de-la-Pena 1992). The relationship between a strong intensity dependence and personality traits implicating high activity and environmental orientation is supported by several other findings, Hegerl et al (1992) demonstrated a positive correlation between the intensity dependence of AEP and the factors "excitability," "stress," and "frankness" of the Freiburg personality questionnaire (Fahrenberg et al 1984). These factors were highly correlated to the "sensation seeking" scale, especially to the subdimension "disinhibition" (Hegerl et al 1992). Davidson et al (1980) described a relationship between "low need of power," which corresponds to "high sensation seeking," and a strong intensity dependence of word evoked potentials. A strong intensity dependence of VEP was found in psychopaths (Raine 1989) and criminals (Raine and Venables 1990), which was interpreted by these authors as pronounced "stimulation or sensation seeking" in these groups. Finally, cats exhibiting "sensation seeking" behavior (exploring, active, and aggressive behavior that is sensitive to novel stimuli) have also a stronger intensity dependence of their VEP than cats without such behavior (Saxton et al 1987; Lukas and Siegel 1977; Hall et al 1970). The Tridimensional Personality Questionnaire (TPQ) developed by Cloninger (1987) was not yet investigated in relation to the intensity dependence of sensory evoked potentials. This personality questionnaire consists of three dimensions: "novelty seeking," "harm avoidance," and "reward dependence." These dimensions possibly reflect different biochemical and anatomical brain systems for the activation ("novelty seeking"), inhibition ("harm avoidance"), and maintenance ("reward dependence") of behavior. We investigated the relationship between the TPQ and the intensity dependence of AEP (NI/P2 component) in healthy volunteers, using dipole source analysis (Brain Electrical Source Analysis [BESA]; Scherg and Picton 1991; Scherg 1990). BESA represents a crucial methodological progress because subcomponents of the auditory evoked N1/P2 component overlapping on the scalp can be separated. The scalp-recorded NI/P2 component can be explained by one tangential dipole representing activity of the primary auditory cortex and one radial dipole representing activity of secondary auditory fields in each hemisphere (Scherg and von Cramon 1990). With this method a better test-retest reliability and a closer relationship to the sensation-seeking scale were found for the intensity dependence than when relying on scalp potentials only (Hegerl and Juckel 1993; Hegerl et al 1994a). Furthermore the physiological interpretation of AEP data is facilitated because the intensity dependence of evoked responses from primary and secondary auditory areas can be investigated independently.
Methods
Subjects Sixteen healthy men [age: 41.6 (30-59 years] without somatic or psychic diseases were investigated. Any history of drug addiction or diminution of hearing was denied by all participants. At the recording day, no signs of ethanol, illegal drugs, or psychotropic medication were found in urine. Close to the AEP recording, all items of the TPQ were filled out by the subjects. At the next day, additional AEP recordings were performed in 13 of these 16 subjects 1 hr after the load of 1 g/kg body weight of ethanol per os (ethanol concentration in blood: 0.83 +_ 0.24 mg of ethanol/100 ml of blood). Ethanol-related or technical problems prevented successful recordings in the other three subjects. All subjects were paid for participation.
AEP Procedure Thirty-two-channel AEP recordings were performed in a sound-attenuated and electrically shielded room adjacent to the recording apparatus. Cz was used as reference. Binaural 1000-Hz tones (30 msec duration; 10 ms rise and fall time; ISI randomized between 1800 and 2200 msec) of five intensity levels (60, 70, 80, 90, 100 dB SPL) were presented in pseudo-randomized form by headphones. Data were collected with a sampling rate of 500 Hz (analog lowpass filter of 150 Hz) from 200 msec prestimulus to 500 msec poststimulus. Eighty-one sweeps were recorded for each intensity. For artifact suppression, all trials were automatically excluded from averaging when the voltage exceeded +_ 50 p~V in any one of the 32 channels at any point during the averaging period (mean artifact rate: 3.2% of the presented stimuli). The first five responses were rejected in order to avoid short-term habituation effects. The sweeps were then averaged separately for the five intensity levels in each subject. The signal-to-noise ratio of the poststimulus data was 13.0 +_ 9.7:1. Dipole source analysis was performed with BESA (Scherg and Picton 1991; Scherg 1990). Because the N l/P2 component seems to be mainly generated by the primary and secondary auditory cortex (Scherg and yon Cramon 1990), we assumed two dipoles per hemisphere to be simultaneously active in the time range of the N l/P2 component. BESA decomposes the measured scalp potentials, in our case the 32-channel N1/P2 waves, into two dipole source activities per hemisphere (tangential and radial dipole). The optimal location and orientation of these dipoles are found by an iterative process (simplex algorithm) optimizing the residual variance (variance of the measured scalp data unexplained by the model), whereas the dipole source potentials are determined by the direct linear approach as described by Scherg and Picton (1991). An approximation of a three-shell head model is used.
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4
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Figure I. Dipole source analysis (BESA) performed on grand mean AEP of the 16 subjects. With two dipoles in each hemisphere more than 98% of the variance of the scalp potentials in the time range of the N 1/P2 component can be explained. Most of the variance is explained by the tangential dipoles (1 and 2), which are located in the area of the Heschl gyms (primary auditory cortex). The dipole source potentials of the radial dipoles (3 and 4) are smaller and their N 1/P2 waves occur later than those of the tangential dipoles. The radial dipoles are located in lateral and deeper parts of the superior temporal gyrus (secondary auditory fields).
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2 pUe~f
The averaged curves of each subject were entered into BESA, where data reduction (from 350 to 90 data points), correction by the prestimulus baseline, digital filtering (1 to 20 Hz), and transformation to average reference data (to give equal weight to each location) took place. In order to determine only neuronal dipole activity, all five channels around the eyes reflecting mainly ocular activity were not considered in the following analysis. In order to get a "basic dipole model," a dipole fit was performed on the grand mean curves of all subjects for the period of the NI/P2 component (63.5-207 msec). Interhemispherical (mirror) symmetry constraints were used for location and orientation fitting in order to reduce the number of independent parameters to be determined. Fitting was done by strictly adhering to the following steps: • The iterative fit procedure was started with bilateral regional sources (two tangential and one radial dipole at the same fixed location, see Scherg and Picton 1991) and locations were fitted for these two regional sources.
• The frontally oriented tangential dipole of each hemisphere was switched off and first orientation and then location of the remaining two dipoles per hemisphere were fitted. Performing dipole source analysis in this way, more than 98% of variance of the scalp-recorded channels in the time range of the N1/P2 component can be explained by one tangential dipole located on the superior temporal plane (mainly primary auditory cortex) and by one radial dipole located in lateral and deeper structures of the superior temporal gyrus (secondary auditory areas) per hemisphere (Fig-
ure 1). The tangential dipoles are more stable than the radial dipoles and explain most of the variance of the scalp data. The "individual dipole model" was found by starting with the "basic dipole model" and individually adjusting the orientation and location of the tangential dipoles in the individual mean data of all intensity levels. The residual variance of the "individual dipole models" had a mean of 6.3%. The N1/P2 component of the individual dipole source potentials of each intensity level was measured as dipole moment (IxVoef),which corresponds to the mean amplitude in the time range of this component (for details see Scherg 1990). The intensity dependence was measured independently for the tangential and radial dipoles calculating the median slope of all possible straight lines connecting the N1/P2 amplitude values to the five intensity levels. The mean amplitudes of both hemispheres were used because no differences between the hemispheres could be observed in several own studies using this method in the described steps.
Statistics Statistics were performed with the SAS package (version 6.0). For the relationship between the intensity dependence and the TPQ dimensions, Spearman correlation coefficients were calculated. Partialling out of covariables were performed by regression analysis. T-tests were used in order to compare group means. The significance level wasp < 0.05.
Results The TPQ values of the 16 subjects for the dimensions "novelty seeking," "harm avoidance," and "reward depen-
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Table 1. Comparison of TPQ Scores Found in 16 Healthy German Subjects with those of an American Normative Populationa (1019 Subjects) Study subjects
American normatives
14.4 - 5.8 4.8 _+2.4
13.0 -+ 5.0 4.1 -+ 1.9
2.7 _+ 1.6
2.3 -4- 1.8
3.8 -+ 2.3
3.1 _+ 1.7
3.2 _+2.3 9.9 _+4.0
3.4 .+ 1.9 12.0 _+5.9
3.1 .+ 1.4
2.5-+ 2.0
3.4 _+ 1.6
4.3 _+ 1.8
1.4 .+ 1.2
2.6 _+2.0
2.1 + 1.6
2.5 -+2.3
16.6 + 3.4 3.2 + 1.3
18.9 .+ 4.0 4.0 .+ 1.0
3.8 .+ 2.5
5.5 .+ 1.9
7.3 .+ 1.7
6.7 - 2.3
2.3 + 1.3
2.6 .+ 1.3
TPQ scores Novelty seeking
Exploratoryexcitability versus stoic rigidity Impulsivenessversus reflection Extravagance versusreserve Disorderlinessversus regimentation Harm avoidance
Anticipatoryworryversus uninhibitedoptimism Fear of uncertainty versus confidence Shynesswithstrangers versus gregariousness Fatigabilityand asthenia versus vigor Reward dependence
Sentimentalityversus insensitiveness Persistenceversus irresoluteness Attachmentversus detachment Dependenceversus independence
Table 2 shows that the dimension "novelty seeking" was significantly correlated to the intensity dependence of the auditory evoked tangential dipole activity (r = 0.53; p < 0.05). Such a relationship was not found for the radial dipole ( r = 0.37; ns). As Figure 2 reveals, the difference of high and low novelty seekers concerning the intensity dependence of the tangential dipole occurred mainly in the higher intensity range. None of the coefficients for the subdimensions of "novelty seeking" reached the significance level. The scores of the dimensions "harm avoidance" or "reward dependence" were found to be not related to the intensity dependence of the tangential and radial dipole (see Table 2). Only, the subdimension "persistence versus irresoluteness" of "reward dependence," which is identical with the fourth dimension of the new TPQ version, showed a statistical trend for a positive correlation to the intensity dependence of the tangential dipole (r = 0.46, p < 0.10). Neither the TPQ scores nor the intensity dependence of the tangential dipole were significantly correlated to age. Only the intensity dependence of the radial dipole was significantly influenced by age. After partialling out this influence, the correlation coefficients between the intensity dependence of the radial dipole and the TPQ scores were again nonsignificant. The 13 subjects with an acceptable recording under ethanol were classified by the median of the "novelty seeking" dimension (13 points) as "high novelty seekers" (n = 7) and 1.7
°The American population consisted of 1019 subjects taken from Cloninger et al 199l.
h
low novelty seekers
1.6 ~ beforeethanol intake O-----@ after ethanol intake
1.5 Table 2. Spearman Correlation Coefficients between TPQ Scores and Intensity Dependence of the Auditory Evoked Tangential and Radial Dipole
Noveltyseeking Harm avoidance Reward dependence
Intensity dependenceof the tangentialdipole
Intensity dependence of the radial dipole
0.53° -0.10 0.23
0.37 0. I0 0.24
ap < 0.05.
o
1.4
> ~.~ 1.3 "~ 1.2 ~. 1.1 ~ 1.0 0.9 Z 0.8 0.7 0.6
dence" are quite comparable with the values of an American normative population (1019 subjects, Cloninger et al 1991) (Table 1). Compared to the American normative population, our 16 subjects had lower scores in the "harm avoidance" and "reward dependence" dimensions (2.1 and 2.3 points which correspond to about half of the SD), caused by the difference in two subdimensions, respectively ("fear of uncertainty" and "shyness with strangers"; "sentimentality" and "persistence").
0.5
L/ I
I
I
I
I
I
I
I
I
I
60
70
80
90
100
60
70
80
90
100
stimulus intensity (dB) Figure 2. Intensity dependence of the tangential dipole before and after acute administration of ethanol (lg/kg body weight) in the "high" (n = 7) and "low novelty seeking" groups (n = 6). After ethanol, less amplitude increase with increasing stimulus intensity was observed in the "high novelty seekers", whereas the amplitude increase in the "low novelty seekers" was nearly unchanged.
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"low novelty seekers" (n = 6). In general, ethanol depressed the intensity dependence, but the "high novelty seekers" showed a 10-times stronger decrease of the intensity dependence under ethanol compared to the ethanol free recording than the "low novelty seekers" (see Figure 2). This was statistically significant for the intensity dependence of the tangential (-0.10 ___0.07 pNon/10dB versus-0.01 -4- 0.06,p = 0.02) and not for that of the radial dipole (-0.04 _ 0.08 I~Vedl0dB versus +0.02 + 0.02, ns). The ethanol blood concentration was comparable in both groups (0.89 +__0.24 versus 0.77 +__0.24 mg of ethanol/100 ml of blood, ns).
Discussion The main result of this study is the stable relationship between high "novelty seeking" and a strong intensity dependence of the auditory evoked N1/P2 component. This finding is in line with studies reporting a positive correlation between the intensity dependence of sensory evoked potentials and Zuckerman's "sensation seeking" scale. This scale is highly related to the "novelty seeking" dimension of the TPQ (Earleywine et a11992; C. R. Cloninger 1992, personal communication). "Novelty seeking" was found to be correlated to the intensity dependence of only one subcomponent of the N l/P2 complex, that is, the tangential dipole, but not to that of the other subcomponent: the radial dipole. Interestingly, "sensation seeking" was also only correlated to the intensity dependence of the tangential dipole (Hegerl and Juckel 1993; Hegerl et al 1994a) and a corresponding finding was observed concerning antisocial tendencies in alcohol dependent patients (Hegerl et al 1994b). Some overlap of "novelty seeking" may also exist with other action-oriented personality traits like "impulsivity" or "extraversion," which are also related to a strong intensity dependence of sensory evoked potentials. It can be assumed that the personality traits "novelty seeking," "sensation seeking," "impulsivity," and "extroversion" reflect a behaviorally relevant individual personality style of acting and orienting to environmental stimuli. Nevertheless, it seems to be difficult to assess exactly the common core of these four personality traits, which are related to the intensity dependence. "Sensation seeking" seems to be a composite of high "novelty seeking" and low "harm avoidance" (Cloninger 1988a), and therefore Cloninger (1988b) predicted that subjects with high "novelty seeking" andlow "harm avoidance" scores should exhibit a strong intensity dependence. We found, however, no correlation between the intensity dependence and "harm avoidance." This could imply that a impulsive personality style characterized more by behavioral activation ("exploratory excitability," "impulsiveness," "extravagance," "disorderliness") than by noninhibition ("uninhibited optimism,"
"confidence," "gregariousness," "vigor") is related to the intensity dependence. Furthermore, different ethanol effects on the intensity dependence of the tangential dipole were observed between high and low "novelty seekers." "High novelty seekers" showed a stronger decrease of the intensity dependence under ethanol than "low novelty seekers," suggesting that "high novelty seekers" are more sensitive to ethanol than "low novelty seekers." Concerning a common neurochemical pattern underlying personality traits like "novelty" or "sensation seeking," "impulsivity," or "extroversion," it is of interest that such personality traits have been related to low or suboptimal activation of the central nervous system (CNS). In subjects with such a low activation, sensation seeking, impulsive or extraverted behavior has the autoregulative function to enhance the CNS activation level into the optimal range by increasing the stimulation from outside (Ellis 1987; Zuckerman 1983; Eysenk 1967; Cloninger 1987). The low activation state of CNS in this personality type could result from low activity of one of the most widespread and oldest neuromodulatory system in the brain, that is, the serotonergic system (see Spoont 1992). In subjects with high "sensation seeking" or high "impulsivity," low concentrations of 5-HIAA in cerebrospinal fluid were found (Schalling and Asberg 1985; Schalling et al 1984; Brown and Linnoila 1990; Linnoila et al 1983). The postulated association between dopaminergic activity and "novelty seeking" (Cloninger 1987) is supported by one (Menza et al 1990), but not by other studies (Limson et al 1991; Wailer et al 1993; Pfohl et al 1990). In this context it is of considerable interest that there are several findings supporting a relationship between a strong intensity dependence of the auditory evoked N1/P2-component and low central serotonergic neurotransmission (Hegerl and Juckel 1993, Juckel et al 1993). Due to the different serotonergic innervation of the primary and secondary auditory cortex (Lewis et al 1986), a close relationship between the intensity dependence, especially of the tangential dipole and low serotonergic activity can be expected. It is therefore speculated that the relationship between a strong intensity dependence of the tangential dipole and an action-oriented and impulsive personality style could be mediated by the serotonergic system.
This study was supported by Deutsche Forschungsgemeinschaft(He 916/7). We wouldliketo thankMs. S. Kuhn,Mr. P. Dufeu,Ms. B. Schildhauer, and Mr. J. Gallinatverymuchfor theirgreathelpand assistance.
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The relationship between the tridimensional personality questionnaire's (TPQ) dimensions "novelty seeking," "harm avoidance, "and "reward dependence" and the intensity dependence of the auditory evoked N1/P2-component was investigated in healthy subjects. Using dipole source analysis, evoked activity of the primary auditory cortex (tangential dipole) could be analyzed at least in part separately from that of secondary auditory areas (radial dipole). It was found that the intensity dependence of the tangential dipole was positively correlated to the TPQ dimension "novelty seeking," but not to "harm avoidance" and "reward dependence." This is in line with findings concerning similar personality traits like "sensation seeking," "impulsivity," or "extraversion." It is therefore concluded that a strong intensity dependence may characterize subjects with an action-oriented and extroverted personality style. The results are discussed within the concept that a low central serotonergic neurotransmission is underlying both an impulsive personality type and a strong intensity dependence of the tangential dipole.
Key Words: Personality, sensation seeking, auditory evoked potentials, serotonin, alcohol
Introduction Cortical processing of different stimulus intensities, reflected by the intensity dependence of sensory evoked potentials, seems to be related to certain kinds of personality traits. There is now converging evidence that subjects showing a strong increase of their evoked potential amplitudes with increasing stimulus intensity (components later than 50 msec after the stimulus: N1 and P2 component) are characterized by higher orientation to the environment and by a more action-oriented behavior than subjects showing From the Laboratory of Clinical Psychophysiology (GJ, UH); and Clinical Research Group "Neurobiological Mechanisms of Drug Addiction," (GJ, LGS, HR, UH); Department of Psychiatry, Freie Universit~it Berlin, Berlin, Germany. Address reprint requests to Priv.-Doz. Dr. U. Hegerl, Psychiatrische Klinik, Ludwig--Maximilians--Universit~it Mtinchen, Nui3baumstr. 7 80336 Miiochert, Germany. Received October 8, 1993; revised March 30, 1994.
© 1995 Society of Biological Psychiatry
weak increase or decrease of their amplitude values with increasing intensity. A strong intensity dependence of auditory and visual evoked potentials (AEP, VEP) has been found in subject with high values of the "sensation seeking" scale developed by Zuckerman (1979), especially in the subdimension "disinhibition" (Hegerl et al 1989; Zuckerman et a11988; Stenberg et a11988; Lukas 1987; for reviews see Carrillo-de-la-Pena 1992; Zuckerman 1990). A relationship in the same direction was also described for "cognitive and motor impulsivity" (VEP; Barratt et al 1987) and Eysenk's (1967) dimension "extroversion" (AEP, VEP; Stenberg et al 1988; Friedman and Meares 1979; Soskis and Shagass 1974). The literature is quite consistent on this issue, although some negative and even one contradictory findings have been reported (Lolas et al 1989; Bruneau et al 1984; Haler et al 1984). These deviating findings were 0006-3223/95/$09.50 SSDI 0006-3223(94)00118-M
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interpreted in terms of attention effects (Stenberg et al 1990) or methodological differences (Carrillo-de-la-Pena 1992). The relationship between a strong intensity dependence and personality traits implicating high activity and environmental orientation is supported by several other findings, Hegerl et al (1992) demonstrated a positive correlation between the intensity dependence of AEP and the factors "excitability," "stress," and "frankness" of the Freiburg personality questionnaire (Fahrenberg et al 1984). These factors were highly correlated to the "sensation seeking" scale, especially to the subdimension "disinhibition" (Hegerl et al 1992). Davidson et al (1980) described a relationship between "low need of power," which corresponds to "high sensation seeking," and a strong intensity dependence of word evoked potentials. A strong intensity dependence of VEP was found in psychopaths (Raine 1989) and criminals (Raine and Venables 1990), which was interpreted by these authors as pronounced "stimulation or sensation seeking" in these groups. Finally, cats exhibiting "sensation seeking" behavior (exploring, active, and aggressive behavior that is sensitive to novel stimuli) have also a stronger intensity dependence of their VEP than cats without such behavior (Saxton et al 1987; Lukas and Siegel 1977; Hall et al 1970). The Tridimensional Personality Questionnaire (TPQ) developed by Cloninger (1987) was not yet investigated in relation to the intensity dependence of sensory evoked potentials. This personality questionnaire consists of three dimensions: "novelty seeking," "harm avoidance," and "reward dependence." These dimensions possibly reflect different biochemical and anatomical brain systems for the activation ("novelty seeking"), inhibition ("harm avoidance"), and maintenance ("reward dependence") of behavior. We investigated the relationship between the TPQ and the intensity dependence of AEP (NI/P2 component) in healthy volunteers, using dipole source analysis (Brain Electrical Source Analysis [BESA]; Scherg and Picton 1991; Scherg 1990). BESA represents a crucial methodological progress because subcomponents of the auditory evoked N1/P2 component overlapping on the scalp can be separated. The scalp-recorded NI/P2 component can be explained by one tangential dipole representing activity of the primary auditory cortex and one radial dipole representing activity of secondary auditory fields in each hemisphere (Scherg and von Cramon 1990). With this method a better test-retest reliability and a closer relationship to the sensation-seeking scale were found for the intensity dependence than when relying on scalp potentials only (Hegerl and Juckel 1993; Hegerl et al 1994a). Furthermore the physiological interpretation of AEP data is facilitated because the intensity dependence of evoked responses from primary and secondary auditory areas can be investigated independently.
Methods
Subjects Sixteen healthy men [age: 41.6 (30-59 years] without somatic or psychic diseases were investigated. Any history of drug addiction or diminution of hearing was denied by all participants. At the recording day, no signs of ethanol, illegal drugs, or psychotropic medication were found in urine. Close to the AEP recording, all items of the TPQ were filled out by the subjects. At the next day, additional AEP recordings were performed in 13 of these 16 subjects 1 hr after the load of 1 g/kg body weight of ethanol per os (ethanol concentration in blood: 0.83 +_ 0.24 mg of ethanol/100 ml of blood). Ethanol-related or technical problems prevented successful recordings in the other three subjects. All subjects were paid for participation.
AEP Procedure Thirty-two-channel AEP recordings were performed in a sound-attenuated and electrically shielded room adjacent to the recording apparatus. Cz was used as reference. Binaural 1000-Hz tones (30 msec duration; 10 ms rise and fall time; ISI randomized between 1800 and 2200 msec) of five intensity levels (60, 70, 80, 90, 100 dB SPL) were presented in pseudo-randomized form by headphones. Data were collected with a sampling rate of 500 Hz (analog lowpass filter of 150 Hz) from 200 msec prestimulus to 500 msec poststimulus. Eighty-one sweeps were recorded for each intensity. For artifact suppression, all trials were automatically excluded from averaging when the voltage exceeded +_ 50 p~V in any one of the 32 channels at any point during the averaging period (mean artifact rate: 3.2% of the presented stimuli). The first five responses were rejected in order to avoid short-term habituation effects. The sweeps were then averaged separately for the five intensity levels in each subject. The signal-to-noise ratio of the poststimulus data was 13.0 +_ 9.7:1. Dipole source analysis was performed with BESA (Scherg and Picton 1991; Scherg 1990). Because the N l/P2 component seems to be mainly generated by the primary and secondary auditory cortex (Scherg and yon Cramon 1990), we assumed two dipoles per hemisphere to be simultaneously active in the time range of the N l/P2 component. BESA decomposes the measured scalp potentials, in our case the 32-channel N1/P2 waves, into two dipole source activities per hemisphere (tangential and radial dipole). The optimal location and orientation of these dipoles are found by an iterative process (simplex algorithm) optimizing the residual variance (variance of the measured scalp data unexplained by the model), whereas the dipole source potentials are determined by the direct linear approach as described by Scherg and Picton (1991). An approximation of a three-shell head model is used.
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4
-,-v v
~2BB
v
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v
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Figure I. Dipole source analysis (BESA) performed on grand mean AEP of the 16 subjects. With two dipoles in each hemisphere more than 98% of the variance of the scalp potentials in the time range of the N 1/P2 component can be explained. Most of the variance is explained by the tangential dipoles (1 and 2), which are located in the area of the Heschl gyms (primary auditory cortex). The dipole source potentials of the radial dipoles (3 and 4) are smaller and their N 1/P2 waves occur later than those of the tangential dipoles. The radial dipoles are located in lateral and deeper parts of the superior temporal gyrus (secondary auditory fields).
-
2 pUe~f
The averaged curves of each subject were entered into BESA, where data reduction (from 350 to 90 data points), correction by the prestimulus baseline, digital filtering (1 to 20 Hz), and transformation to average reference data (to give equal weight to each location) took place. In order to determine only neuronal dipole activity, all five channels around the eyes reflecting mainly ocular activity were not considered in the following analysis. In order to get a "basic dipole model," a dipole fit was performed on the grand mean curves of all subjects for the period of the NI/P2 component (63.5-207 msec). Interhemispherical (mirror) symmetry constraints were used for location and orientation fitting in order to reduce the number of independent parameters to be determined. Fitting was done by strictly adhering to the following steps: • The iterative fit procedure was started with bilateral regional sources (two tangential and one radial dipole at the same fixed location, see Scherg and Picton 1991) and locations were fitted for these two regional sources.
• The frontally oriented tangential dipole of each hemisphere was switched off and first orientation and then location of the remaining two dipoles per hemisphere were fitted. Performing dipole source analysis in this way, more than 98% of variance of the scalp-recorded channels in the time range of the N1/P2 component can be explained by one tangential dipole located on the superior temporal plane (mainly primary auditory cortex) and by one radial dipole located in lateral and deeper structures of the superior temporal gyrus (secondary auditory areas) per hemisphere (Fig-
ure 1). The tangential dipoles are more stable than the radial dipoles and explain most of the variance of the scalp data. The "individual dipole model" was found by starting with the "basic dipole model" and individually adjusting the orientation and location of the tangential dipoles in the individual mean data of all intensity levels. The residual variance of the "individual dipole models" had a mean of 6.3%. The N1/P2 component of the individual dipole source potentials of each intensity level was measured as dipole moment (IxVoef),which corresponds to the mean amplitude in the time range of this component (for details see Scherg 1990). The intensity dependence was measured independently for the tangential and radial dipoles calculating the median slope of all possible straight lines connecting the N1/P2 amplitude values to the five intensity levels. The mean amplitudes of both hemispheres were used because no differences between the hemispheres could be observed in several own studies using this method in the described steps.
Statistics Statistics were performed with the SAS package (version 6.0). For the relationship between the intensity dependence and the TPQ dimensions, Spearman correlation coefficients were calculated. Partialling out of covariables were performed by regression analysis. T-tests were used in order to compare group means. The significance level wasp < 0.05.
Results The TPQ values of the 16 subjects for the dimensions "novelty seeking," "harm avoidance," and "reward depen-
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Table 1. Comparison of TPQ Scores Found in 16 Healthy German Subjects with those of an American Normative Populationa (1019 Subjects) Study subjects
American normatives
14.4 - 5.8 4.8 _+2.4
13.0 -+ 5.0 4.1 -+ 1.9
2.7 _+ 1.6
2.3 -4- 1.8
3.8 -+ 2.3
3.1 _+ 1.7
3.2 _+2.3 9.9 _+4.0
3.4 .+ 1.9 12.0 _+5.9
3.1 .+ 1.4
2.5-+ 2.0
3.4 _+ 1.6
4.3 _+ 1.8
1.4 .+ 1.2
2.6 _+2.0
2.1 + 1.6
2.5 -+2.3
16.6 + 3.4 3.2 + 1.3
18.9 .+ 4.0 4.0 .+ 1.0
3.8 .+ 2.5
5.5 .+ 1.9
7.3 .+ 1.7
6.7 - 2.3
2.3 + 1.3
2.6 .+ 1.3
TPQ scores Novelty seeking
Exploratoryexcitability versus stoic rigidity Impulsivenessversus reflection Extravagance versusreserve Disorderlinessversus regimentation Harm avoidance
Anticipatoryworryversus uninhibitedoptimism Fear of uncertainty versus confidence Shynesswithstrangers versus gregariousness Fatigabilityand asthenia versus vigor Reward dependence
Sentimentalityversus insensitiveness Persistenceversus irresoluteness Attachmentversus detachment Dependenceversus independence
Table 2 shows that the dimension "novelty seeking" was significantly correlated to the intensity dependence of the auditory evoked tangential dipole activity (r = 0.53; p < 0.05). Such a relationship was not found for the radial dipole ( r = 0.37; ns). As Figure 2 reveals, the difference of high and low novelty seekers concerning the intensity dependence of the tangential dipole occurred mainly in the higher intensity range. None of the coefficients for the subdimensions of "novelty seeking" reached the significance level. The scores of the dimensions "harm avoidance" or "reward dependence" were found to be not related to the intensity dependence of the tangential and radial dipole (see Table 2). Only, the subdimension "persistence versus irresoluteness" of "reward dependence," which is identical with the fourth dimension of the new TPQ version, showed a statistical trend for a positive correlation to the intensity dependence of the tangential dipole (r = 0.46, p < 0.10). Neither the TPQ scores nor the intensity dependence of the tangential dipole were significantly correlated to age. Only the intensity dependence of the radial dipole was significantly influenced by age. After partialling out this influence, the correlation coefficients between the intensity dependence of the radial dipole and the TPQ scores were again nonsignificant. The 13 subjects with an acceptable recording under ethanol were classified by the median of the "novelty seeking" dimension (13 points) as "high novelty seekers" (n = 7) and 1.7
°The American population consisted of 1019 subjects taken from Cloninger et al 199l.
h
low novelty seekers
1.6 ~ beforeethanol intake O-----@ after ethanol intake
1.5 Table 2. Spearman Correlation Coefficients between TPQ Scores and Intensity Dependence of the Auditory Evoked Tangential and Radial Dipole
Noveltyseeking Harm avoidance Reward dependence
Intensity dependenceof the tangentialdipole
Intensity dependence of the radial dipole
0.53° -0.10 0.23
0.37 0. I0 0.24
ap < 0.05.
o
1.4
> ~.~ 1.3 "~ 1.2 ~. 1.1 ~ 1.0 0.9 Z 0.8 0.7 0.6
dence" are quite comparable with the values of an American normative population (1019 subjects, Cloninger et al 1991) (Table 1). Compared to the American normative population, our 16 subjects had lower scores in the "harm avoidance" and "reward dependence" dimensions (2.1 and 2.3 points which correspond to about half of the SD), caused by the difference in two subdimensions, respectively ("fear of uncertainty" and "shyness with strangers"; "sentimentality" and "persistence").
0.5
L/ I
I
I
I
I
I
I
I
I
I
60
70
80
90
100
60
70
80
90
100
stimulus intensity (dB) Figure 2. Intensity dependence of the tangential dipole before and after acute administration of ethanol (lg/kg body weight) in the "high" (n = 7) and "low novelty seeking" groups (n = 6). After ethanol, less amplitude increase with increasing stimulus intensity was observed in the "high novelty seekers", whereas the amplitude increase in the "low novelty seekers" was nearly unchanged.
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"low novelty seekers" (n = 6). In general, ethanol depressed the intensity dependence, but the "high novelty seekers" showed a 10-times stronger decrease of the intensity dependence under ethanol compared to the ethanol free recording than the "low novelty seekers" (see Figure 2). This was statistically significant for the intensity dependence of the tangential (-0.10 ___0.07 pNon/10dB versus-0.01 -4- 0.06,p = 0.02) and not for that of the radial dipole (-0.04 _ 0.08 I~Vedl0dB versus +0.02 + 0.02, ns). The ethanol blood concentration was comparable in both groups (0.89 +__0.24 versus 0.77 +__0.24 mg of ethanol/100 ml of blood, ns).
Discussion The main result of this study is the stable relationship between high "novelty seeking" and a strong intensity dependence of the auditory evoked N1/P2 component. This finding is in line with studies reporting a positive correlation between the intensity dependence of sensory evoked potentials and Zuckerman's "sensation seeking" scale. This scale is highly related to the "novelty seeking" dimension of the TPQ (Earleywine et a11992; C. R. Cloninger 1992, personal communication). "Novelty seeking" was found to be correlated to the intensity dependence of only one subcomponent of the N l/P2 complex, that is, the tangential dipole, but not to that of the other subcomponent: the radial dipole. Interestingly, "sensation seeking" was also only correlated to the intensity dependence of the tangential dipole (Hegerl and Juckel 1993; Hegerl et al 1994a) and a corresponding finding was observed concerning antisocial tendencies in alcohol dependent patients (Hegerl et al 1994b). Some overlap of "novelty seeking" may also exist with other action-oriented personality traits like "impulsivity" or "extraversion," which are also related to a strong intensity dependence of sensory evoked potentials. It can be assumed that the personality traits "novelty seeking," "sensation seeking," "impulsivity," and "extroversion" reflect a behaviorally relevant individual personality style of acting and orienting to environmental stimuli. Nevertheless, it seems to be difficult to assess exactly the common core of these four personality traits, which are related to the intensity dependence. "Sensation seeking" seems to be a composite of high "novelty seeking" and low "harm avoidance" (Cloninger 1988a), and therefore Cloninger (1988b) predicted that subjects with high "novelty seeking" andlow "harm avoidance" scores should exhibit a strong intensity dependence. We found, however, no correlation between the intensity dependence and "harm avoidance." This could imply that a impulsive personality style characterized more by behavioral activation ("exploratory excitability," "impulsiveness," "extravagance," "disorderliness") than by noninhibition ("uninhibited optimism,"
"confidence," "gregariousness," "vigor") is related to the intensity dependence. Furthermore, different ethanol effects on the intensity dependence of the tangential dipole were observed between high and low "novelty seekers." "High novelty seekers" showed a stronger decrease of the intensity dependence under ethanol than "low novelty seekers," suggesting that "high novelty seekers" are more sensitive to ethanol than "low novelty seekers." Concerning a common neurochemical pattern underlying personality traits like "novelty" or "sensation seeking," "impulsivity," or "extroversion," it is of interest that such personality traits have been related to low or suboptimal activation of the central nervous system (CNS). In subjects with such a low activation, sensation seeking, impulsive or extraverted behavior has the autoregulative function to enhance the CNS activation level into the optimal range by increasing the stimulation from outside (Ellis 1987; Zuckerman 1983; Eysenk 1967; Cloninger 1987). The low activation state of CNS in this personality type could result from low activity of one of the most widespread and oldest neuromodulatory system in the brain, that is, the serotonergic system (see Spoont 1992). In subjects with high "sensation seeking" or high "impulsivity," low concentrations of 5-HIAA in cerebrospinal fluid were found (Schalling and Asberg 1985; Schalling et al 1984; Brown and Linnoila 1990; Linnoila et al 1983). The postulated association between dopaminergic activity and "novelty seeking" (Cloninger 1987) is supported by one (Menza et al 1990), but not by other studies (Limson et al 1991; Wailer et al 1993; Pfohl et al 1990). In this context it is of considerable interest that there are several findings supporting a relationship between a strong intensity dependence of the auditory evoked N1/P2-component and low central serotonergic neurotransmission (Hegerl and Juckel 1993, Juckel et al 1993). Due to the different serotonergic innervation of the primary and secondary auditory cortex (Lewis et al 1986), a close relationship between the intensity dependence, especially of the tangential dipole and low serotonergic activity can be expected. It is therefore speculated that the relationship between a strong intensity dependence of the tangential dipole and an action-oriented and impulsive personality style could be mediated by the serotonergic system.
This study was supported by Deutsche Forschungsgemeinschaft(He 916/7). We wouldliketo thankMs. S. Kuhn,Mr. P. Dufeu,Ms. B. Schildhauer, and Mr. J. Gallinatverymuchfor theirgreathelpand assistance.
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