1. Introduction
In psychology research, the impulsivity trait has been studied in different personality models and personality theories that relate it to different behavioral dispositions such as precipitation, lack of anticipation or sensation seeking [
1,
2,
3]. Various different models have set out to describe the components of impulsivity. Barrat [
4] proposed a three-factor impulsivity model, and Dickman [
5] suggested differentiating between functional and dysfunctional impulsivity. Human personality structural models also present different views about the impulsivity construct. For instance, Eysenck located impulsivity on the Psychoticism super trait [
6,
7] but later Gray, extending Eysenck's theory, located it in the high Neuroticism and high Extraversion quadrant, describing impulsivity as a component of sensitivity to reward, according to the Reinforcement Sensitivity Theory (RST) [
8,
9]. In the Five Factor Model, impulsivity is mainly considered the inverse pole of the Conscientiousness trait, but Neuroticism presents a facet named Impulsiveness in the NEO-PI-R [
10]. This is a good example of the different nature of the various components of impulsivity. Considering the varying approaches to the concept of impulsivity, it could be concluded that this construct is not unidimensional, and involves various sub-traits with moderate relationships among them [
11,
12].
Impulsivity is an important psychological correlate of risk behaviors [
13,
14,
15]. It is well established that impulsivity and aggression are linked. In this line, a meta-analysis showed significant correlations between facets of the UPPS-P Impulsive Behavior Scale and several different forms of aggression [
16], and Cognitive and motor impulsivity were predictors of self-reported total aggression [
17]. Given the relevance of this construct to predict and explain several relevant outcomes, it is not surprising that some specific (mono-trait) measures have been developed. Self-report measures addressed to exclusively measure impulsivity are the UPPS-P Behavior Scale (this instrument also includes a scale of Sensation Seeking) [
11], or the Barratt Impulsivity Scale, BIS-11 [
18]. From instruments developed after the structural human personality models, a scale addressed to measure impulsivity is the Reward Sensitivity scale (SR), from the Sensitivity to Punishment and Sensitivity to Reward Questionnaire (SPSRQ) [
19,
20]. The SR is related to Eysenck's Psychoticism and Impulsivity, and Zuckerman's Sensation Seeking scales [
19,
20,
21,
22]. Gray’s BAS is a neurobehavioral system that depends on dopamine-supplied structures and mediates individual differences in sensitivity and reactivity to appetitive stimuli associated with the BAS and impulsivity [
23]. It should be noted that dopamine activity increases impulsivity [
24]. In Zuckerman’s personality model, Impulsivity was a facet of the broader Impulsive Sensation Seeking trait (ImpSS) [
3].
Impulsive personality traits are heritable (40–60%) [
25,
26] and are related to the frontal-subcortical circuitry. In this way, subscales of both UPPS-P and BIS-11 showed strong genetic correlations with phenotypic behaviors characterized by high impulsivity, such as drug addictions and attention deficit hyperactivity disorder (ADHD) [
27]. At the molecular genetics level of analysis, it has been shown, for instance, that Motor and Non-Planning impulsivity scales in BIS-11 were associated with two single nucleotide polymorphisms (SNPs) within the 5-HT2a receptor gene [
28]. The androgen receptor (AR) gene has been linked to disinhibited impulsive personality in male prison inmates measured through a combination of the following personality scales: Sensation Seeking, Aggression-Hostility, Psychoticism, Sensitivity to Reward, Novelty Seeking and Impulsivity. Inmates carrying CAG short and GGN long (trinucleotide repeat polymorphisms) haplotype group (short–long haplotype) obtained significantly higher scores on the impulsive-disinhibited index [
21]. The interaction between free testosterone and CAG, and between sex hormone binding globulin testosterone transporter (SHBG) and CAG explained some of the differences in impulsivity. This occurred mostly in the group of short CAG repetitions and motor impulsivity [
29]. Human aggression/impulsivity-related traits have a complex background that is greatly influenced by genetic and non-genetic factors [
30].
The dehydroepiandosterone sulfate (DHEA-S) is an anabolic steroid secreted by the adrenal cortex and is a precursor of testosterone and estrogens [
31]. DHEA-S is produced in the zona reticularis of the adrenal cortex by the action of adrenocorticotrophic hormone (ACTH). DHEA-S levels peak in young adulthood, and then decline progressively by 2-4% per year [
32]. The DHEA-S has been associated with different personality questionnaires related to impulsivity. Do Vale et al. [
33] studied the relationship between the DHEA-S and the combination of the psychopathic deviance and hypomania scales of the Minnesota Multiphasic Personality Inventory (MMPI) [
34]. These two scales are considered to be indicators of impulsivity [
35]. Presence of Borderline Personality Disorder (BPD), a disorder with predominant impulsivity, is also associated with high concentrations of DHEA-S in relation to subjects without personality disorders [
36]. In a study with Attention-deficit/hyperactivity disorder (ADHD) patients and controls, salivary DHEA levels were related to distractibility and impulsivity scores on the Continuous Performance Test (CPT). The authors concluded that DHEA-S might be a biomarker for ADHD [
37]. In another study, morning DHEA-S levels were significantly higher in borderline subjects than controls [
38]. In this sense, DHEA-S has been pointed to as a biomarker of acute stress [
39], and it was significantly and positively associated with anger [
40].
Testosterone production is primarily dependent on luteinizing hormone (LH) acting on the conversion of cholesterol to pregnenolone within the mitochondria of Leydig cells [
41]. Testosterone levels also decline with age, while LH levels rise slightly or remain unchanged. The decline in testosterone with age is associated with a drop in energy level, muscular strength, physical, sexual and cognitive functions and mood [
42]. In men, the percentages of testosterone decrease 1% per year from the age of forty [
43], 4% of testosterone is converted to dihydrotestosterone via a reductase enzyme and 0.2% to estradiol via the aromatase enzyme [
44]. In women with polycystic ovarian syndrome, significant relationships were found between total testosterone (TT) levels and Motor impulsivity and Non-planning impulsivity [
40].
Significant relationships between impulsivity and Sensation Seeking and testosterone have been reported in general and criminal samples [
45,
46]. Thus, it has been replicated that subjects with high scores on impulsive-related traits such as Experience Seeking, Disinhibition or Boredom Susceptibility tended to present higher testosterone scores [
21,
29,
47,
48,
49,
50]. These studies support the theoretical association between Impulsive Sensation Seeking and gonadal hormones raised by Zuckerman’s psychobiological personality model [
51]. Recently, exogenous testosterone supplementation has been found to be associated with trait impulsivity [
52,
53,
54].
In spite of the evidence relating both testosterone and DHEA-S with impulsivity and related personality characteristics, few studies have examined the relationship between impulsivity and testosterone and DHEA-S all together. Besides, since testosterone and DHEA-S androgens are related, it is necessary to simultaneously explore the role of both androgens in the differences observed in impulsivity. Thus, the main objective of this study is to examine the relationships between DHEA-S and testosterone and impulsivity simultaneously in a sample of healthy middle-aged men. Based on the studies reviewed, a moderate relationship is expected among both androgens (DHEA-S and testosterone) and impulsivity scales.
4. Discussion
The main goal of this study was to examine the relationship between two androgenic steroids, DHEA-S and testosterone, and the impulsivity trait measured with different instruments. Preliminary results show a significant correlation between the two androgens, as expected, and a significant negative correlation with age [
32,
43]. Hormone means and ranges fit the values expected in a normal population. High Skewness was as expected, so values were logarithmically transformed as is customary in a hormone study. Logarithmic transformations tend to normalize the distribution of hormones taking into account the distances between the different values [
68]. With regard to psychometric measures of impulsivity, it is also observed that the BIS-11 and the UPPS-P scales do not represent a one-dimensional construct [
11,
12]. In this line, for example, non-significant correlations were obtained between impulsivity scales such as Negative Urgency, Motor impulsivity and Non-Planning Lack of Perseverance and Negative Urgency.
Age is negatively related to impulsive personality traits, with Sensation Seeking and Sensitivity to Reward being the variables with the highest partial correlations, controlling for the rest of the variables. In this line, there are also significant associations between DHEA-S and Motor impulsivity, Sensitivity to Reward, Lack of premeditation, Sensation Seeking and Positive Urgency. Testosterone correlated with Sensitivity to Reward, Sensation Seeking and Positive Urgency. However, the sum of all the BIS-11, UPPS-P and SR scales correlates significantly with DHEA-S and testosterone, demonstrating an association, albeit a weak one, between the broad construct of impulsivity with the two hormones. Several of the impulsivity scales are associated with the variance of DHEA-S (up to 28% of the variance) and, to a lesser extent (9%), with the variance of the testosterone. Therefore, a moderate relationship between the measures of impulsivity with the two androgens is confirmed. It should be remarked that DHEA-S presents a much stronger relationship with impulsivity scales than testosterone.
Additionally, in this study, the nonlinear relationships between the two hormones and the impulsivity scales are also examined using a nonparametric LOESS graphical regression. LOESS curve (local polynomial regression) is a method of fitting a smooth curve between two variables [
69]. This method combines the simplicity of least squares linear regression with the flexibility of nonlinear regression. In reference to the relationships between the impulsivity variables and DHEA-S, the graph clearly shows that as the DHEA-S values increase, the impulsivity scales increase, except for Lack of premeditation. On the other hand, in the testosterone graph, only Lack of Perseverance, Attention impulsivity and Positive Urgency show a tendency.
As commented in the introductory section, the relationship in humans between aggressiveness and impulsivity with steroid hormones is moderate. However, biological theories of personality suggest that impulsivity interacts with traits such as Sensation Seeking or similar ones such as Cloninger’s Novelty Seeking [
70,
71,
72,
73]. Dopamine also plays a role in impulsive behavior and reward seeking, while serotonin plays an inhibiting role. Testosterone and dopamine are related; dopamine can influence testosterone, and testosterone can influence dopamine, and both of them play an important role in male sexuality. Crucial to health is male sexual function. One study found that endogenous administration of dopamine agonists to the medial preoptic area of rats increased sexual activity [
74]. Another study found that castrated male rats did not show sexual interest and did not release dopamine in the medial preoptic area. After testosterone injections, castrated rats had sexual intercourse and increased dopamine release in the medial preoptic area [
75].
Following Zuckerman's theory, it has been proposed that testosterone could have an antagonistic role in monoamine oxidase (MAO) allowing a higher concentration of activating catecholamine in receptors due to lack of degradation [
76]. DHEA-S is also an inhibitor of MAO activity [
77]. The BAS (impulsivity) is associated with the dopaminergic system, while the BIS (anxiety) is associated with the septo-hippocampal system and the amygdala. These structures have a high density of steroid receptors, so differences in personality can be expected [
78]. The BAS system is a neurobehavioral system that depends on dopamine-supplied structures and mediates individual differences in sensitivity and reactivity to appetitive stimuli associated with the BAS and impulsivity [
22]. Dopamine activity increases impulsivity [
23]. Exogenous DHEA-S produces a significant increase in the levels of acetylcholine, norepinephrine, and dopamine in the brain [
79].
Therefore, research on aggressivity/impulsivity and androgens may in the future provide new findings and explanations about their biological connection, including genetics, thanks to a potentially greater understanding of the functioning of the prefrontal lobe and the dopaminergic pathways of the brain. Studies with rats suggest that the GABA A receptor may be associated with testosterone-mediated impulsivity [
80]. In the current study, Sensitivity to Reward, and to a lesser extent Sensation Seeking, both of which have considerable biological basis in the literature, have been the variables most closely related to hormones.
This study has several limitations. It is a cross-sectional design, so no causal conclusions can be drawn. The sample size is moderate, and it is possible that these findings could be less significant in a larger sample, and as the sample was restricted to men, it precludes additional confounding factors such as biochemistry differences on androgens between males and females. In addition, other variables affecting androgen concentrations such as smoking, diet, alcohol consumption, physical activity, weight, height or muscle mass have not been controlled, which could affect data and results. Finally, since the subjects volunteered for this study, it is possible that the results cannot be generalized to the general population.
In conclusion, the present results support a moderate relationship between impulsivity and the androgenic steroids DHEA-S and testosterone, in line with the findings reported by investigators in male samples. These results are greatly affected by age, both in impulsivity levels and in androgen levels. Research on DHEA-S and impulsivity has been much scarcer than on testosterone. Our results report a greater relationship between DHEA-S than testosterone with impulsivity. This consistent association of DHEA-S with impulsive or disinhibited personality has been demonstrated by other researchers, who found that DHEA-S was directly related to the deviant behavior triad and type A personality [
32] or borderline personality disorder subjects [
37]. Taking into account the limitations outlined above, future studies should continue to study the role of DHEA-S in personality in general, and aggressive and impulsive behavior in particular. Variables such as dopamine, norepinephrine, cortisol/testosterone ratio and cortisol/DHEA-s and GABA A receptor and androgen receptor (AR) genes should also be included.
Figure 1.
Empirical network with the age, testosterone, DHEA-S, UPPS-P and SR domains (partial correlations). Nodes represent domains. The edges represent the relationship among domains. The thicker the edge, the greater is the relationship between domains. Green and red lines represent positive and negative relationships, respectively. AI: Attention, MI: Motor (MI), NPI: Non-Planning, SR: Sensitivity to Reward, NU: Negative urgency, PR: Lack of Premeditation, PS: Lack of Perseverance, SS: Sensation Seeking (SS) and PU: Positive Urgency.
Figure 1.
Empirical network with the age, testosterone, DHEA-S, UPPS-P and SR domains (partial correlations). Nodes represent domains. The edges represent the relationship among domains. The thicker the edge, the greater is the relationship between domains. Green and red lines represent positive and negative relationships, respectively. AI: Attention, MI: Motor (MI), NPI: Non-Planning, SR: Sensitivity to Reward, NU: Negative urgency, PR: Lack of Premeditation, PS: Lack of Perseverance, SS: Sensation Seeking (SS) and PU: Positive Urgency.
Figure 2.
LOESS plots for DHEA-S (T-score) and impulsivity scales: 1-Age, 2- Lack of premeditation, 3-Attention, 4-Non-planing, 5-Positive Urgency, 6-Motor, 7-Negative urgency, 8-Sensation Seeking, 9- Lack of perseverance and 10-Sensitivity to Reward (Z-score).
Figure 2.
LOESS plots for DHEA-S (T-score) and impulsivity scales: 1-Age, 2- Lack of premeditation, 3-Attention, 4-Non-planing, 5-Positive Urgency, 6-Motor, 7-Negative urgency, 8-Sensation Seeking, 9- Lack of perseverance and 10-Sensitivity to Reward (Z-score).
Figure 3.
LOESS plots for Testosterone (T-score) and impulsivity scales: 1-Age, 2-Lack of Premeditation, 3-Lack of Perseverance, 4-Non-planing, 5-Negative urgency, 6-Positive urgency, 7-Atention, 8-Motor and 9-Sensation Seeking and 10-Sensitivity to Reward (Z- score).
Figure 3.
LOESS plots for Testosterone (T-score) and impulsivity scales: 1-Age, 2-Lack of Premeditation, 3-Lack of Perseverance, 4-Non-planing, 5-Negative urgency, 6-Positive urgency, 7-Atention, 8-Motor and 9-Sensation Seeking and 10-Sensitivity to Reward (Z- score).
Table 1.
Descriptive, ANOVA age groups comparison, frequency distribution values and internal consistency of scales.
Table 1.
Descriptive, ANOVA age groups comparison, frequency distribution values and internal consistency of scales.
|
(1) n = 40 |
(2) n = 39 |
(3) n =41 |
|
|
|
|
|
< 38 years |
38 to 50 years |
< 50 years |
p < |
|
|
|
|
M |
SD |
M |
SD |
M |
SD |
Scheffe |
K |
S |
α |
Age |
29.93 |
4.28 |
44.41 |
3.89 |
58.64 |
5.84 |
--- |
-.99 |
.11 |
--- |
DHEA-S* (ng/mL) |
.86 |
.20 |
.76 |
.24 |
.61 |
.18 |
1>2 (.001); 2 >3 (.007) |
-.34 |
.04 |
--- |
Testosterona* (pg/mL) |
2.09 |
.17 |
2.01 |
.21 |
1.97 |
.16 |
1 > 3 (.014) |
1.8 |
.44 |
-- |
Attention (BIS-11) |
14.39 |
5.26 |
13.11 |
4.48 |
13.83 |
4.50 |
|
-.08 |
.56 |
.62 |
Motor (BIS-11) |
13.80 |
6.78 |
12.08 |
5.26 |
11.63 |
5.51 |
|
.73 |
.83 |
.73 |
Non-planning (BIS-11) |
15.63 |
7.01 |
15.24 |
5.97 |
14.76 |
7.48 |
|
.79 |
.94 |
.72 |
Negative Urgency |
7.80 |
1.91 |
7.47 |
2.33 |
8.12 |
3.12 |
|
.11 |
.49 |
.80 |
Lack of Premeditation |
8.10 |
2.08 |
7.74 |
2.10 |
7.44 |
2.21 |
|
-.34 |
.08 |
.81 |
Lack of Perseverance |
8.61 |
1.46 |
8.76 |
1.97 |
8.78 |
1.98 |
|
-.41 |
.07 |
.69 |
Sensation Seeking |
9.93 |
3.03 |
8.71 |
2.69 |
7.73 |
2.37 |
1 >3 (.002) |
-.60 |
.07 |
.85 |
Positive Urgency |
7.46 |
2.42 |
6.97 |
2.68 |
7.07 |
2.59 |
|
.27 |
.77 |
.83 |
Sensitivity to Reward |
21.90 |
4.12 |
21.37 |
3.82 |
19.02 |
4.61 |
1>3 (.010); 2>3 (.05) |
-.68 |
-.05 |
.76 |
Table 3.
Linear multiple regression analysis for gender including age, BIS-11, SR, and UPPS-P as independent variables, and DHEA-S and testosterone as dependent variables (standardized.
Table 3.
Linear multiple regression analysis for gender including age, BIS-11, SR, and UPPS-P as independent variables, and DHEA-S and testosterone as dependent variables (standardized.
DHEA-S |
Testosterone |
Adjusted R2 =.28 |
β |
t |
p < |
Adjusted R2 = .09 |
β |
t |
p < |
(Constant) |
|
4.92 |
.001 |
(Constant) |
|
14.14 |
.001 |
Age |
-.39 |
-4.39 |
.001 |
Age |
-.22 |
-2.25 |
.027 |
Attention (BIS-11) |
-.04 |
-.40 |
.690 |
Attention (BIS-11) |
.16 |
1.45 |
.151 |
Motor (BIS-11) |
.15 |
1.34 |
.183 |
Motor (BIS-11) |
-.11 |
-.93 |
.352 |
Non-planning (BIS-11) |
-.05 |
-.51 |
.609 |
Non-planning (BIS-11) |
.00 |
-.02 |
.982 |
Sensitivity to Reward |
.21 |
2.11 |
.037 |
Sensitivity to Reward |
.15 |
1.30 |
.196 |
Negative Urgency |
-.34 |
-3.05 |
.003 |
Negative Urgency |
-.20 |
-1.59 |
.115 |
Lack of premeditation |
.05 |
.46 |
.649 |
Lack of premeditation |
-.13 |
-1.04 |
.300 |
Lack of perseverance |
.09 |
.91 |
.365 |
Lack of perseverance |
.07 |
.66 |
.510 |
Sensation Seeking |
-.13 |
-1.35 |
.180 |
Sensation Seeking |
-.01 |
-.09 |
.927 |
Positive Urgency |
.32 |
2.71 |
.008 |
Positive Urgency |
.36 |
2.73 |
.007 |