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Association Between the Dopamine D4 Receptor (DRD4) Molecular Psychiatry (1999) 4, 378–384 1999 Stockton Press All rights reserved 1359–4184/99 $15.00 and the 4,4 vs 4,7 genotype, respectively, were chosen ORIGINAL RESEARCH ARTICLE as independent variables in the one-way analyses of variance. We could observe the reported association between Association between the DRD4 exon III allele length and Novelty Seeking dopamine D4 receptor (Tables 1 and 2). The presence of the 7 repeat was asso- ciated with significantly elevated Novelty Seeking total = = (DRD4) exon III scores (F1,134 11.54, P 0.001). The effect had a size of 0.6 standard deviation units and accounted for 8% polymorphism and of the variance. Among Novelty Seeking subscales, the presence of the 7 repeat was associated with elevated = measures of Novelty scores on NS1 (Exploratory Excitability; F1,134 4.97, = = = P 0.027), NS2 (Impulsiveness; F1,134 4.60, P 0.034), = = Seeking in a German and NS3 (Extravagance; F1,134 19.06, P 0.00003). Similar, and even stronger, associations could be population observed when comparing subjects with the 4,4 vs 4,7 A Strobel1, A Wehr1, A Michel2 and B Brocke1 genotype (Table 2). However, only the associations between the 7 repeat and NS total and NS3, and 1Institute of Clinical, Diagnostic and Personality between the 4,7 genotype and NS, NS1, and NS3 Psychology, Technical University Dresden, remained significant after correction for multiple test- Mommsenstrasse 13, 01062 Dresden; 2Institute of ing (␣ = 0.0016; see Methods and Materials). Zoology, Technical University Dresden, Mommsenstrasse As effects of demographic variables can confound 13, 01062 Dresden, Germany the results of association studies, we carried out analy- ses of variance with age and sex as covariates (Tables 1 and 2). The use of ethnicity as covariate was not Keywords: association; dopamine D4 receptor; genetics; appropriate in our almost entirely German sample. The Novelty Seeking; personality; polymorphism; TPQ analyses revealed that there was only a significant age Since the observation of an association between the effect on NS2 scores. Although this association dopamine D4 receptor (DRD4) exon III polymorphism remained significant at the 0.05 level when comparing 1 = and the temperament trait of Novelty Seeking, repli- subjects with the 4,4 vs 4,7 genotype (NS2: F1,82 5.35, 2–5 = = = = cation studies have yielded both positive and nega- P 0.023; age: F1,82 6.35, r 0.24, P 0.014), it dimin- tive6–12 results. This raised the question whether the ished when comparing subjects with absence vs pres- initial findings must be regarded as false positives.13 = = ence of the 7 repeat (NS2: F1,132 2.26, P 0.135; age: However, demographic or methodological differences = = = F1,132 8.47, r 0.24, P 0.004). between studies may have obscured the small effect of In order to examine a differential effect of the DRD4 the DRD4 polymorphism on Novelty Seeking.14 Examin- exon III polymorphism on different subtypes of novelty ation of clinical or older cohorts may have led to an underestimation of possible associations due to a seeking related behavior, we employed four person- restricted variation of Novelty Seeking in these cohorts. ality questionnaires which are widely used in the The use of different questionnaires provides another assessment of normal as well as pathological person- source of variation. In order to replicate the initial find- ality, and which contain scales for measurement of ings as precisely as possible, a cohort of 136 healthy, considerably heritable personality traits which are young volunteers was genotyped, and Novelty Seeking thought to share variance with Novelty Seeking (see was ascertained using the TPQ.15,16 In addition, further Methods and Materials): the Sensation Seeking Scales aspects of novelty seeking behavior have been ascer- form V (SSS V),17,18 the scales Impulsiveness and Ven- tained through additional trait measures. We could turesomeness of the Eysenck Impulsivity Question- observe the reported association between long DRD4 naire (I7),19,20 the Revised Eysenck Personality Ques- alleles and significantly elevated scores (age- and sex- tionnaire (EPQ-R),21,22 and the NEO Five Factor residualized) on the TPQ-Novelty Seeking total scale as Inventory (NEO-FFI),23,24 a 60-item short form of the well as on two of the subscales, Exploratory Excitability 23 and Extravagance. The results provide further confir- Revised NEO-Personality Inventory (NEO-PI-R). We mation for the role of the DRD4 exon III polymorphism assumed that the following scales may be substantially in modulation of Novelty Seeking. In addition, the pat- related to novelty seeking behavior and therefore may tern of associations between the polymorphism and show associations with DRD4 exon III allele length: other scales suggests that this polymorphism has its NEO-Extraversion and Conscientiousness, SSS-total effect on exploratory, extravagant, and extraverted, and subscales, I7 Impulsiveness and Venturesomeness, rather than on impulsive and monotony-avoidant sub- and EPQ-Extraversion and Psychoticism. The results types of Novelty Seeking. based on these scales were corrected for multiple test- DRD4 exon III allele frequencies in our cohort were ing (␣ = 0.0016, see Methods and Materials). comparable to those observed in other populations. The results of the analyses of variance (Table 3) indi- The two most common alleles were the 4 and the 7 cated that the presence of the DRD4 exon III 7 repeat repeat, the two most common genotypes were 4,4 and allele showed a tendency towards associations with 4,7. Thus, absence vs presence of the 7 repeat allele, elevated scores on Extraversion from the NEO-FFI, Association between DRD4 polymorphism and Novelty Seeking A Strobel et al 379 Table 1 Presence of DRD4 exon III 7 repeat and TPQ scale score differences Raw mean scores ± SD One-way ANOVA ANOVA with covariates 7 repeat absent 7 repeat present P effect ␩2 effects P r (n = 92) (n = 44) size NS: Novelty Seeking 17.16 ± 5.58 20.59 ± 5.35 0.001a 0.60 0.08 NS 0.003 Age 0.068 0.19 Sex 0.670 0.02 NS1: Exploratory Excitability 4.95 ± 1.71 5.66 ± 1.83 0.027a 0.40 0.04 NS1 0.037 Age 0.506 0.11 Sex 0.514 −0.06 NS2: Impulsiveness 3.50 ± 2.16 4.34 ± 2.10 0.034a 0.39 0.03 NS2 0.135 Age 0.004 0.24 Sex 0.082 0.10 NS3: Extravagance 3.98 ± 1.75 5.30 ± 1.39 0.00003a 0.75 0.12 NS3 0.0001 Age 0.085 0.19 Sex 0.439 0.06 NS4: Disorderliness 4.74 ± 2.06 5.30 ± 2.14 0.148 HA: Harm Avoidance 14.62 ± 6.91 12.30 ± 6.17 0.060 HA1: Anticipatory Worry 4.57 ± 2.46 3.48 ± 2.11 0.013b −0.75 0.05 HA1 0.011 Age 0.801 −0.04 Sex 0.308 −0.07 HA2: Fear of Uncertainty 3.91 ± 2.14 3.68 ± 1.89 0.541 HA3: Shyness with Strangers 2.93 ± 1.78 2.36 ± 1.88 0.088 HA4: Fatigability 3.21 ± 2.42 2.77 ± 2.07 0.307 RD134: Reward Dependence 19.26 ± 3.83 18.20 ± 4.26 0.149 RD1: Sentimentality 3.95 ± 1.22 3.95 ± 1.14 0.968 RD3: Attachment 7.72 ± 1.92 7.73 ± 2.17 0.979 RD4: Dependence 2.83 ± 1.36 2.64 ± 1.22 0.434 RD2: Persistence 4.77 ± 2.01 3.89 ± 2.26 0.022b −0.41 0.04 RD2 0.007 Age 0.086 0.07 Sex 0.057 0.11 P, significance of F values; effect size, standard deviation units; ␩2, explained variance; r, correlations of covariates with depen- dent variables. Effect sizes, ␩2 and ANOVA with covariates were calculated only for significant associations in the one-way ANOVA. For effects significant at the 0.05 level: aBonferroni-adjusted level of significance ␣ = 0.0016; bBonferroni-adjusted level of sig- nificance ␣ = 0.0017. = Impulsiveness from the I7, Psychoticism, and Extraver- effect of sex on Impulsiveness (Imp: F1,82 3.76, = = = = sion from the EPQ-R. The same constellation could be P 0.056; sex: F1,82 2.37, P 0.127, r 0.16), and an = seen when comparing subjects with the 4,4 vs 4,7 geno- effect of age on EPQ-Psychoticism (EPQ-P: F1,82 5.96, = = = = type, but none of the effects reached the adjusted level P 0.017; age: F1,82 8.61, P 0.004, r 0.34). On the of significance. Furthermore, we observed trends other hand, the associations between the DRD4 exon towards associations between the 4,7 genotype and III genotype and Sensation Seeking total, Thrill and elevated scores on the Sensation Seeking total scale, Adventure Seeking, and Venturesomeness, respect- Thrill and Adventure Seeking, and I7 Venture- ively, raised due to effects of sex on these scales (SSS: = = = = someness. Analyses of variance with the DRD4 exon III F1,82 6.10, P 0.016; sex: F1,82 9.15, P 0.003, =− = = = genotype as independent variable and age and sex as r 0.31; TAS: F1,82 9.09, P 0.003; sex: F1,82 6.21, = =− = = covariates provided a more differentiated view on this P 0.015, r 0.24; Vent: F1,82 7.40, P 0.008; sex: = = = putative association (Table 3). The effects of the 4,7 F1,82 4.06, P 0.047, r 0.18). genotype on elevated NEO- and EPQ-Extraversion Among the remaining TPQ scales, for which we did scores were independent from effects of age and sex not expect associations, lower scores on Harm Avoid- = (NEO-E: age- and sex-residualized F1,82 4.88, ance subscale Anticipatory Worry (HA1) and Persist- = = P 0.030; EPQ-E: age- and sex-residualized F1,82 4.89, ence (RD2) were associated with the presence of the 7 = = = = P 0.03).
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