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Journal of Clinical Pharmacology, 2005; 45:94-100
© 2005 the American College of Clinical Pharmacology

CLINICAL STUDIES

Impulsive-Aggressive Traits, Serotonin Function, and Alcohol-Enhanced Aggression

Carl Fulwiler, MD, PhD, Joy Eckstine, LICSW and Sapna Kalsy, BA

From the Department of Psychiatry, Tufts-New England Medical Center, Boston (Dr Fulwiler, J. Eckstine, S. Kalsy); Tufts University School of Medicine, Boston (Dr Fulwiler); and Lemuel Shattuck Hospital, Boston (Dr Fulwiler).

Address for reprints: Carl Fulwiler, MD, PhD, Department of Psychiatry, New England Medical Center, MS# 1007, 750 Washington Street, Boston, MA 02111.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 ACKNOWLEDGEMENTS
 REFERENCES
 
Although alcohol consumption is involved in most acts of violence, most people do not become violent when they drink. Individuals also respond differently to alcohol on laboratory measures of aggression. The objective of this study was to determine whether individual differences in the effects of alcohol on a laboratory measure of aggression are related to specific personality traits and/or serotonin function, as measured by prolactin response to pharmacochallenge. Psychometric scales for impulsiveness, aggression, and anger, as well as a probe for suspiciousness, were administered to 10 healthy male social drinkers. Trait serotonin function was determined by citalopram challenge. The effect of alcohol on the Point Subtraction Aggression Paradigm was determined by comparing aggression scores with and without 1 g/kg alcohol. Impulsivity scores were significantly correlated with the change in aggressive responding after alcohol. Aggression, anger, and suspiciousness scores were not. Prolactin response did not predict the effect of alcohol on aggressive responding. The results suggest that trait impulsiveness may mediate the effects of alcohol on aggression in normal males.

Key Words: Alcohol • aggression • impulsivity • personality • temperament • serotonin

Alcohol is estimated to be involved in more than 50% of all violent crimes1 and up to 86% of murders.2 Some epidemiological evidence is consistent with a causal role for alcohol,3-5 whereas other evidence suggests that common personality factors lead to both heavy drinking and aggressive behavior.6,7

Laboratory experiments in which alcohol is administered under controlled conditions provide an opportunity to study the relationship between alcohol ingestion and aggressive behavior. Using a variety of assays for aggressive behavior, normal subjects given alcohol score higher than sober subjects in groupwise comparisons.8,9 However, just as most people who drink do not become violent in the real world, individual responses in the laboratory differ. Whereas some individuals respond more aggressively, most either become less aggressive or show no change.10-12

It has been suggested that aggression-related personality traits may mediate individual responses to alcohol.13,14 Previous studies have examined trait hostility, anger, and aggression, but results have been mixed.15-19 Two traits related to aggression and violence, which have not been examined in laboratory studies on the effects of alcohol on aggressive responding, are impulsivity and suspiciousness.20-22

Impulsive-aggressive traits and impulsive violence are associated with abnormalities in central nervous system serotonin. An inverse relationship has been observed between indices of central serotonin function and aggression in humans23-29 and nonhuman primates.30-32 Trait variation in serotonin function may explain individual differences in the aggression-promoting effect of alcohol.19,33,34

In the present study, we measured individual variation on measures of personality traits and serotonin function in healthy males and examined the relationship between these characteristics and the effect of alcohol on aggressive behavior in the Point Subtraction Aggression Paradigm (PSAP).35,36 The PSAP has been validated in male parolees with histories of actual violence37,38 and is sensitive to individual differences in the effects of drugs and alcohol on aggressive responding.12,19,39-41


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 ACKNOWLEDGEMENTS
 REFERENCES
 
Subjects
Normal healthy male social drinkers were recruited by flyers and newspaper ads. Subjects were told that the purpose of the study was to examine the effects of alcohol on behavior and hormones. A telephone prescreen was used to exclude alcohol and substance abuse, as well as current psychiatric or medical illness. All procedures were carried out in the General Clinical Research Center at New England Medical Center. Medical screening consisted of examination by a physician, review of systems, and routine laboratory blood and urine tests. Psychiatric screening included a mental status examination and the Structured Clinical Interview for DSM-IV Axis I Disorders—Clinician Version.42 A urine drug test and alcohol breath test were also performed. Subjects were excluded if they had a current or past Axis I disorder, including alcohol or substance abuse or dependence. The study was approved by investigational review board of the New England Medical Center.

The mean age for the sample was 29.6 years (SD = 6.1), and the average educational level was 3 years of college or technical school (SD = 2.0).

Procedures
Psychometric assessments and serotonin challenge were performed on the same visit. Alcohol administration and aggression testing were conducted on a separate visit at least 2 days later.

Psychometrics. The self-report version of the modified Lifetime History of Aggression (LHA-R) Scale43 has a maximum possible score of 55. Subjects' scores showed a wide range (4-34; mean = 14.3, SD = 9.7), which overlapped with scores of psychiatric outpatients with a history of violence (mean = 31.8, SD = 9.6, unpublished data).

With the Buss-Perry Aggressiveness (BPA) Questionnaire,44 factor analysis identified 4 subscales that correlated with peer nominations of aggressiveness: Physical Aggression, Verbal Aggression, Anger, and Hostility. Scores for our subjects ranged from 33 to 67 (mean = 58, SD = 13.0).

The Barratt Impulsiveness Scale, version 11 (BIS-11)45,46 contains 3 subscales derived from factor analysis: Motor, Cognitive, and Nonplanning.46 Subjects' scores ranged from 15 to 61 (mean = 42.3, SD = 15.5), with the highest scores overlapping with scores obtained from psychiatric outpatients with a history of violence (mean = 61.9, SD = 10.9, unpublished data).

The State-Trait Anger Expression Inventory (STAXI)47,48 includes 2 subscales relevant to trait anger: Angry Temperament and Anger Expression. Raw scores were converted to percentiles according to the manual.48

Serotonin challenge. The prolactin response to challenge with the serotonin reuptake inhibitor citalopram was used to test central serotonergic function. Stimulation of serotonergic receptors in the hypothalamus causes release of prolactin from cells in the pituitary, and the prolactin response provides a measure of serotonergic responsiveness in the limbic-hypothalamic-pituitary axis.25,49 Citalopram is the most selective of the serotonin reuptake inhibitors.50-52 It has minimal effects on norepinephrine and dopamine neuronal reuptake, and it produces a robust prolactin response.53,54

Aggression assay. The PSAP, developed by Cherek35 and Cherek et al,36 uses loss of points (later exchanged for money) as the aversive stimulus. Subjects may respond by subtracting points from the fictitious opponent (aggressive response) or by continuing to accumulate points (money-earning response). The relative effects of alcohol on aggressive and money-earning responding provide a measure of specificity. The PSAP software (University of Texas-Houston) was supplied by Don R. Cherek, PhD.

Subjects were seated in a room with a computer monitor and a response panel with 3 buttons labeled A, B, C. The monitor and response panel were connected to a computer in a different room using an interface card (Med Associates, Inc, St. Albans, Vt). A set of instructions was read to the subjects stating that they would be competing with other subjects in different rooms to earn money by pressing buttons on the response panel. Only 1 button (A) would result in accumulating points (100 times to earn 1 point worth $0.10). The subject was told that other participants can take money from him or her (provocation), which appeared on his or her monitor as a subtraction of points. The subject had 3 options following a provocation: ignore it by continuing to press the money-earning button; press a second button (B) 10 times, which subtracts a point from the opponent (aggressive response); or press a third button (C) 10 times, which would protect against losing points for a period of time (escape response).

In reality, the computer served as the fictitious opponent and was programmed to initiate aggressive responding by subtracting points from the subject at random intervals. Aggressive responding was reinforced by having a provocation-free interval (125 seconds) follow an aggressive response, during which time no money is subtracted from the subject. Each assay consisted of four 20- to 25-minute sessions with 25-minute rest periods. Subjects could earn up to $25 per day and received an additional stipend for arriving on time and having a negative urine drug screen and breath alcohol screen. At the end of each day of testing, subjects were interviewed to confirm the deception by asking them (a) to estimate the number of opponents they had faced, (b) to describe the opponents, and (c) to evaluate who had subtracted the most money during the sessions.

Subjects were instructed to avoid alcohol or drugs for 2 weeks, follow a low-monoamine diet for 3 days, and fast overnight prior to the visit. Vital signs, a urine sample for drug screen, and breath alcohol concentration (Alcosensor III, Intoximeter, St. Louis, Mo) were obtained, and subjects were also interviewed by a dietician about compliance with the diet. An IV catheter was inserted, and a sample was taken for baseline plasma prolactin concentration. Thirty minutes later, 40 mg of citalopram was administered orally. Blood samples were collected and vital signs taken every hour for 4 hours. Samples were centrifuged and serum was frozen until analyzed. Prolactin level was determined by a magnetic separation, enzyme-linked immunoassay (Technicon Immuno 1® System, Bayer Corp, Tarrytown, NY). The assay has a sensitivity of 0.1 ng/mL. Intra-assay and interassay coefficients of variation were ≤2% and ≤3%, respectively. Serum prolactin concentrations at each time point after citalopram were subtracted from the baseline concentration and converted to a percentage of the baseline value. The value representing the greatest change from baseline was used to plot each subject's maximum response. The average maximum response after citalopram was +14.8%.

Alcohol Administration
Subjects completed 4 PSAP sessions per day on 2 different days. Prior to each assay, subjects provided a urine sample for drug screening, and breath alcohol was measured with the Alcosensor III (Intoximeters, Inc, St. Louis, Mo). The baseline testing session allowed subjects to become familiar with the apparatus and to achieve stable aggressive responding rates. On the second day, subjects consumed a beverage containing alcohol, 1 g/kg 95% ethanol, over 10 to 15 minutes. The alcohol dose was calculated to produce breath alcohol concentrations (BAC) of 0.08% to 0.120%. Actual concentrations ranged from 0.066% to 0.093%. Alcohol was mixed with 700 mL of ginger ale and 2 drops of peppermint oil to disguise the taste. Thirty minutes after administration of alcohol, breath alcohol measurements were recorded, and the subjects began the first session of the assay. Breath alcohol measurements were taken at the start of each session thereafter. Procedures conformed to the "Recommended Council Guidelines on Ethyl Alcohol Administration in Human Experimentation," published by the NIAAA. After the final session, subjects were debriefed to explain the deception and why it had been necessary. No subjects expressed negative feelings about the deception.

Data Analysis
The effects of alcohol were assessed on the average number of responses over 4 sessions as well as by subtracting the number of responses during the same session on the nonalcohol day. Group differences were compared using t tests. Spearman's correlation was used to examine the relationship between scores on personality trait instruments and the change in aggressive responding after administration of alcohol.

All reported P values are 2-tailed. Statistical analyses were performed with SPSS for Windows 7.5 (SPSS, Inc).


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 ACKNOWLEDGEMENTS
 REFERENCES
 
Personality Traits
Correlations between psychometric measurements and change in aggressive responding after alcohol are shown in Table I. Only the Barratt Impulsivity Scale showed a significant correlation. Total impulsiveness scores on the BIS-11 were strongly correlated with the effect of alcohol on aggressive responses but not money-earning responses (r = -0.21, P = .66). The correlation was strongest for the cognitive and nonplanning subscales (r = 0.69 and 0.71, respectively, P < .05). Aggression (LHA-R, BPA) and anger (STAXI) scores were positively correlated with the change in aggressive responding but did not reach significance. No significant correlations were found for any of the LHA-R and BPA subscales. Suspiciousness scores showed a weak inverse correlation with the effect of alcohol on aggression.


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  		Table I Spearman Rank Correlations Between Psychometric Measures and Change in Aggressive Responsiveness After Alcohol

 

There was no correlation between the change in aggressive responding and either age (r = 0.08, P = .83) or years of education (r = 0.04, P = .92). Two of the 10 subjects did not believe that they were competing against another individual. When these 2 subjects were removed from the analysis, our primary findings remained unchanged. The correlation between impulsivity and change in aggressive responding with alcohol was significant (r = 0.71, P = .048), and the correlations for the other psychometric scores were not.

Two subjects responded more aggressively after receiving alcohol, whereas the remaining subjects showed either no change or a decrease from baseline aggressive responding. The mean change in aggression scores in the 2 subjects exhibiting alcohol-heightened aggression (AHA) was significantly different from the change in aggression in the remaining subjects (+91% vs -61%, t = 2.82, P = .02). The AHA subjects scored significantly higher on cognitive impulsiveness (14.5 vs 7.5, t = -3.84, P = .005) and angry temperament (83.5 vs 23.9, t = -3.71, P = .006).

Serotonin Function
As shown in Figure 1 (upper panel), baseline aggressive responding was inversely correlated with prolactin response to citalopram (Spearman's r = -0.69, P = .03). In contrast, aggressive responding after receiving alcohol showed a nonsignificant trend toward a positive correlation with prolactin response (r = 0.25, P = .49; Figure 1, lower panel). We also compared prolactin responses in the 2 subjects who exhibited enhanced aggression after alcohol with those of the remaining subjects. The mean prolactin response for these 2 subjects was not significantly different from that of the 8 other subjects (16.9 vs 14.2, t = 0.11, P = .92).



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  		Figure 1. Correlations between maximum prolactin response and aggressive responding with and without alcohol. Serum prolactin concentrations at each time point after citalopram administration were subtracted from the baseline prolactin concentration and converted to a percentage of the baseline value. The value representing the greatest change from baseline was used to plot each subject's maximum prolactin response. Upper panel: Mean number of aggressive responses during 4 Point Subtraction Aggression Paradigm (PSAP) sessions without alcohol (baseline). Lower panel: The change in aggressive responding ({Delta}PSAP Aggression) after receiving 1.0 g/kg alcohol was calculated by subtracting the mean aggressive responses at baseline from the mean number of responses during 4 PSAP sessions with alcohol.

 


   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 ACKNOWLEDGEMENTS
 REFERENCES
 
Personality Traits
The effect of alcohol on aggressive responding was significantly correlated with impulsiveness, particularly cognitive and nonplanning impulsiveness. Subjects who became more aggressive after alcohol also scored higher on cognitive impulsiveness and trait anger. No significant associations were observed for trait aggression or suspiciousness.

To our knowledge, this is the first study to examine the relationship between impulsiveness and the direct effect of alcohol on aggression in the laboratory. Our finding is consistent with the strong correlation found between impulsiveness and violence in alcoholics.55-58

Trait aggression was not significantly related to the effect of alcohol on aggressive behavior. This result agrees with a study by Moeller et al,19 who found only a nonsignificant correlation between aggression scores and alcohol-enhanced aggression in the PSAP. Two earlier studies, which found a correlation between trait aggression and aggressive behavior with alcohol, used a different aggression assay and different psychometric measures of aggression.17,18

Angry Temperament scores were significantly higher in the 2 subjects who responded more aggressively with alcohol, but these results cannot be generalized and will need to be replicated with a larger sample.

The tendency to perceive the environment as threatening is associated with elevated rates of violence3,59 but was not associated with the effect of alcohol on PSAP aggression in the present study. We are not aware of other studies that have examined the relationship between suspiciousness and the effect of alcohol on laboratory aggression.

Serotonin
As expected, prolactin response to a serotonin challenge was inversely correlated with aggressive responding in the absence of alcohol. However, no correlation was observed with alcohol-induced changes in aggressive behavior. To our knowledge, there are no other published studies on the relationship between serotonin function and the effect of alcohol on laboratory aggression, despite the widely held belief that reduced serotonin function leads to violent behavior during intoxication.33,34,60,61 This negative result also awaits confirmation with a larger sample.

Limitations
Several limitations of this study should be noted. The small sample size raises the possibility of Type II error. In particular, the positive correlation observed between LHA-R aggression scores and alcohol-induced changes in aggression (r = 0.51) may have reached significance with a larger sample size. Our results with normal volunteers cannot be generalized to violent or aggressive individuals. With regard to serotonin function, because plasma levels of citalopram were not determined, we cannot rule out the possibility that some variation in plasma prolactin levels following citalopram administration may have been due to differences in pharmacokinetics. Also, our results with citalopram challenge cannot be compared directly to studies that used fenfluramine to stimulate prolactin release. Finally, despite important advantages of a laboratory paradigm for measuring the effects of alcohol directly in a controlled environment, the relevance of laboratory results to the real world requires further exploration.


   CONCLUSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
ACKNOWLEDGEMENTS
 REFERENCES
 
With these limitations in mind, our findings support a role for trait impulsivity in mediating the effects of alcohol on aggressive behavior in normal males. We did not find support for a relationship between trait aggressiveness or trait serotonin function and the effect of alcohol on laboratory aggression. Additional studies will be needed to confirm these findings and to determine if they extend to other populations and other types of aggressive behavior.


   ACKNOWLEDGEMENTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 ACKNOWLEDGEMENTS
REFERENCES
 
The authors are grateful to Dr Will Rand for advice on statistics and to the staff of the Clinical Research Center for administrative and technical assistance. Supported by the New England Medical Center Research Fund and National Center for Research Resources grant M01 RR000054 to the New England Medical Center.


   FOOTNOTES
 
DOI: 10.1177/0091270004270457

Submitted for publication April 9, 2004; Revised version accepted August 20, 2004.


   REFERENCES
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 ACKNOWLEDGEMENTS
 REFERENCES
 

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W. M. Dinn, D. A. Gansler, N. Moczynski, and C. Fulwiler
Brain Dysfunction and Community Violence in Patients With Major Mental Illness
Criminal Justice and Behavior, February 1, 2009; 36(2): 117 - 136.
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