CRIME CAUSATION: BIOLOGICAL THEORIES

Criminal behavior results from a complex interplay of social and biological factors. Social factors are a reflection of environmental sources of influence, such as socioeconomic status. The terms "biological" and "genetic" are often confused, in part due to the fact that they represent overlapping sources of influence. Biological factors are more inclusive, consisting of physiological, biochemical, neurological, and genetic factors. Genetic factors refer to biological factors that are inherited. Social factors, on the other hand, cannot be inherited. Until recently, the majority of criminological research focused solely on social contributors, either minimizing or negating the importance of genetic and biological influences on criminal behavior. In the past fifteen years, however, a large body of evidence has accumulated that suggests that the etiology of criminal behavior may be better understood when genetic and biological factors are also taken into account. Evidence for the role of genetic factors in the etiology of criminal behavior carries the assumption that biological factors mediate this relationship. Therefore, in this entry, we will first discuss the role of genetics in the etiology of criminal behavior, followed by evidence outlining the importance of biological factors.

Genetic epidemiological studies

Epidemiological evidence that genetic factors contribute to criminal behavior come from three sources: family, twin, and adoption studies. The limitation of family studies is the inability to separate the genetic and environmental sources of variation. Therefore, given the limited utility of family studies to separate issues of nature versus nurture, this section will focus on two other epidemiological research designs that are better equipped to test for genetic effects.

Twin studies. Twin studies support the contention that a heritable trait may increase risk for criminal behavior. Twin studies compare the rate of criminal behavior of twins who are genetically identical or monozygotic twins (MZ) with twins who are not, or dizygotic twins (DZ) in order to assess the role of genetic and environmental influences. To the extent that the similarity observed in MZ twins is greater than that in DZ twins, genetic influences may be implicated.

The twin design, however, does present some problems to this interpretation. The use of twin studies to test questions of heritablilty are limited in that it is a rare occurrence for the twins to be reared in separate environments. Moreover, Dalgaard and Kringlen suggest that the greater similarity of MZ twins may be attributed to their shared environmental experiences. In line with this hypothesis, Carey (1992) suggests that MZ twins may imitate one another more than DZ twins, and that this phenomenon could lead to an overestimation of heritability. Consequently, any review of twin studies must keep these limitations in mind.

Earlier twin studies reported considerable variations in the pairwise concordance rates (among monozygotic twins from 100 percent to 25 percent and in dizygotic twins from 81 percent to 0 percent). Several methodological flaws in earlier twin studies made it difficult to draw conclusions regarding genetic liability to criminal behavior. First, the operational definition of "criminal behavior" varied from mild incidental offenses to long-term incarceration. A potentially more serious methodological concern is that, with the exception of Dalgaard and Kringlen's study and the twin study that follows, all other twin samples suffered from biased samples.

Using an unselected sample of 3,586 twin pairs in Denmark, Christiansen reported 52 percent of the monozygotic twins were (proband-wise) concordant for criminal behavior whereas only 22 percent of the dizygotic twins were (probandwise) concordant for criminal behavior. A marked increase of probandwise concordance for criminal behavior among monozygotic twins suggests that the MZ twins inherit some biological characteristic(s) that increases their joint risk for criminal involvement.

Results from more recent twin studies are largely in agreement with results obtained from earlier twin studies. Variability in criteria for criminal behavior and sample composition does not appear to change the genetic effect, an outcome which suggests that criminal behavior and correlates of antisocial behavior (i.e., antisocial symptom counts, conduct disorder) may be genetically mediated. The twin design, as discussed earlier, is limited in that the assumption of equal environments is often violated. Studies comparing the concordance rates in MZ twins reared apart can avoid this problem, but it is difficult to obtain such subjects. Christiansen has noted that several of the earlier twin studies had cases in which a set of monozygotic twins were raised in separate environments; these preliminary data suggest that studying MZ twins reared apart may be an important behavioral genetics tool to investigate the etiology of criminal behavior. To the present authors' knowledge, only one modern twin study has employed this type of research design to test whether criminal behavior may be genetically mediated.

Twins reared apart. Grove and others investigated the concordance of antisocial problems, as measured by the Diagnostic Interview Schedule (DIS), among a sample of thirty-two sets of monozygotic twins reared apart (MZA) who were adopted by nonrelatives shortly after birth. Because this was a nonclinical sample, very few subjects met Diagnostic and Statistical Manual-III criteria for antisocial personality. To remedy this limitation, symptoms that contribute to the overall DSM-III diagnoses were counted to assess for subclinical manifestations of antisocial problems. Grove found substantial overlap between the genetic influences for both childhood conduct disorders (correlation of .41) and adult antisocial behaviors (correlation of .28). Although these findings are based on a small number of subjects, the Grove findings are congruent with the findings from other twin studies and extend the twin literature by evaluating MZ twins raised in separate environments.

Adoption studies. Another epidemiological design that may more cleanly parcel out most environmental effects is the adoption design. Adoption studies provide a natural experiment to test the existence and strength of inherited predispositions. Adoptees are separated at birth from their biological parents. Thus, similarities between the adoptee and biological parents can be regarded as estimates of genetic influences, while similarities between the adoptee and the adoptive parents may be thought of as estimates of environmental influences. Moreover, the adoption design allows for the assessment of interaction effects between environmental and genetic influences. Adoption studies have been carried out in three different countries: the United States, Sweden, and Denmark.

Iowa. The first adoption study to explore the genetic transmission of criminal behavior was carried out in Iowa by Crowe. The sample consisted of fifty-two adoptees (including twenty-seven males) born between 1925 and 1956 to a group of forty-one incarcerated female offenders. A group of control adoptees were matched for age, sex, race, and approximate age at the time of adoption. Seven of the fifty-two adoptees sustained a criminal conviction as adults whereas only one of the control adoptees had a conviction. Since these adoptees were separated from their incarcerated mothers at birth, this tends to implicate a heritable component to antisocial behavior.

A separate series of adoption studies carried out in Iowa by Cadoret and colleagues (1980, 1983, 1985, 1987, 1995) have supported Crowe's original findings. These independent replications lend support to the notion that criminal behavior may have important genetic influences.

Several characteristics of the Iowa adoption studies carried out by Cadoret and colleagues should be noted. First, the genetic factors of interest, namely the antisocial status of the biological parents, were ascertained from "poorly maintained adoption agency records" or incomplete prison and hospital records. Second, a high refusal rate of adoptee interviews introduces the possibility that adoptees who consented to be interviewed may be qualitatively different from those who declined. Third, in two of the Cadoret studies, antisocial status of the adoptees was determined from telephone interviews (1987, 1995). In short, what is needed is the use of criminal national registries that would provide a better opportunity to assess lifetime, cumulative records for all subjects (both biological and adoptive parents and adoptees). This condition is difficult if not impossible to meet in the United States. Such requirements, however, have been met by adoption studies from two Scandinavian countries, Denmark and Sweden.

Sweden. Bohman examined the criminality and alcoholism rates among 2,324 Swedish adoptees and their biological parents, as determined by a check with national criminal and alcohol registries. Preliminary findings led Bohman to conclude prematurely that biological fathers who were criminal only (without alcohol abuse) were not more likely to have criminal, adopted-away children than biological fathers with no criminal record (12.5 percent vs. 12 percent). He did not differentiate between criminality alone in the biological fathers and criminality accompanied by alcohol abuse in the biological fathers. Further statistical analysis reveals that when these two groups are separated, there are significantly more criminal-only sons (without alcohol abuse) of criminal-only biological fathers than there are criminal-only sons of other fathers (8.9 percent vs. 4.9 percent, p (significance level) < 0.05).

One of the chief findings to emerge from the Swedish Adoption Study is evidence for a distinct, highly heritable form of alcoholism and criminality that may be transmitted from father to son (Cloninger et al., 1981). Cross-fostering analyses revealed the emergence of two distinct subtypes of alcoholism that could be differentiated based upon genetic and environmental influences. The first subtype proposed by Cloninger, Type I alcoholism, appears to be affected by environmental factors, such as the socioeconomic status of the adoptive parents. Type I alcoholics were found to have a late onset of alcohol abuse (i.e., after age twenty-five) and did not engage in criminal behavior.

Type II alcoholism, in contrast, appears to have a strong genetic component. Type II alcoholics are typically males with alcohol and criminal registrations. The biological fathers of these Type II alcoholics had an early onset (i.e., before age twenty-five) of recurrent alcoholism and criminality (sample size, n = 36). Environmental factors, such as low socioeconomic status and alcoholism in the adoptive parents, were not found to influence the frequency of Type II alcoholism. Moreover, the male adoptees' risk of Type II alcoholism was not increased by an interaction between genetic and environmental factors. These findings were later replicated in independent adoption studies carried out in Sweden by Sigvardsson and others (1996) and in a reanalysis of the Danish Adoption Project (Tehrani and Mednick, forthcoming). Although the utility of the Type I, Type II paradigm in clinical samples has received mixed support, these data suggest the existence of a highly heritable form of criminality and alcoholism that is genetically transmitted from father to son.

Denmark. Mednick, Gabrielli, and Hutchins carried out a study of the genetic influence on criminal behavior using an extensive data set consisting of 14,427 Danish adoptees (ranging in age from twenty-nine to fifty-two years) and both sets of biological and adoptive parents. They found that adopted-away sons had an elevated risk of having a court conviction if their biological parent, rather than their adoptive parent, had one or more court convictions. If neither the biological nor adoptive parents were convicted, 13.5 percent of the sons were convicted. If the adoptive parents were convicted and the biological parents were not, this figure only increased to 14.7 percent. When examining sons whose biological parents were convicted and adoptive parents remained law-abiding, however, 20 percent of the adoptees had one or more criminal convictions. Moreover, as the number of biological parental convictions increased, the rate of adoptees with court convictions increased.

There were cases where a biological father, mother, or both contributed more than one child to this population. Some of these children, either full or half-siblings, were placed in different adoptive homes. There were 126 male-male half-sibling pairs placed in separate adoptive homes. Of the 126 male-male half-sibling pairs in the study 31 pairs had at least one member of the sibship convicted. Of these 31 pairs, 4 pairs were concordant for convictions (concordance rate = 12.9 percent for half-siblings). The study yielded 40 male-male full-sibling pairs who were adopted into separate homes. Fifteen pairs had at least one member of the sibship sustain a criminal conviction; of these 15 pairs, 3 pairs were concordant for convictions (concordance rate = 20 percent for full siblings). Although the numbers are small, these findings suggest that as the level of genetic relationship increases, the level of concordance increases.

These data, obtained from three different countries and in different laboratories, lend support to the notion that criminal behavior appears to have a strong genetic component. In addition, the combination of genetic and environmental factors, or gene-environment interactions, has also been the subject of investigation. Accordingly, several adoption studies have noted significant interactive effects when environmental variables are also taken into account.

Gene-environment interactions

The importance of gene-environment interactions are illustrated in several adoption studies. For example, the effects of socioeconomic status (SES) on inhibiting or promoting the expression of the genetic vulnerability to criminality have been examined in two large-scale adoption studies, the Danish and Swedish adoption studies. Cloninger and others (1982) and Van Dusen and others (1983) have reported that adoptive parent SES appears to interact with genetic vulnerability for criminality. Specifically, the risk of criminality among adoptees of criminal biological parents was significantly reduced if they were adopted into middle to high SES adoptive homes. Conversely, low adoptive parent socioeconomic status interacted with criminality in the biological parents to increase the adoptee's risk of criminality.

Other adverse environmental influences, such as adoptive parental registrations for alcohol and crime, and later age of placement, were found to interact with the genetic risk for criminal behavior. Crowe (1975) found that adoptees who had a criminal biological mother and spent longer time in an orphanage or foster placement had the highest rates of criminal conviction. In a separate series of adoption studies carried out by Cadoret and colleagues, evidence for the importance of gene-environment interactions in the development of antisocial problems in adoptees has been presented. Cadoret and others (1983) reported in a Missouri adoption sample (n = 108) that adoptees with an alcoholic or anti-social biological parent who were placed in an adoptive home at a later age had the highest rate of adolescent antisocial problems. In an Iowan adoption study (n = 246 male and female adoptees), Cadoret and Cain found that the presence of alcohol or antisocial symptoms in the biological parents interacted with adverse environmental conditions, such as the presence of alcohol and antisocial problems in the adoptive parents, time spent in foster care, and divorced status of the adoptive parents, to produce a marked increase in the incidence of adolescent antisocial behavior. Cadoret and others (1995) reported that a biological background of antisocial problems interacted with adverse environmental conditions, such as the presence of a psychiatric condition in the adoptive family, separation or divorce of the adoptive parents, adoptive parent alcohol or drug abuse, to increase the risk of childhood conduct disorder and adolescent aggressivity. Taken together, these studies demonstrate the utility of the gene-environmental model to our understanding of the etiological correlates of criminal behavior.

Sex differences in genetic liability to criminality

There is some evidence to suggest that genetic and environmental factors may differentially contribute to the risk of criminality for males and females. It has been hypothesized that females who engage in criminal activity may have a stronger genetic propensity for this type of behavior than males (Sellin). Evidence for this contention is provided by two independent adoption studies in which female property offenders had a much higher percentage of biological parents who were property offenders than did male adoptees (Sigvardsson et al.; Baker et al.). This finding is supportive of the contention that females are faced with more social pressures to remain law-abiding than males and therefore females who violate these social norms may have an added genetic push toward these behaviors.

Taken together, twin and adoption studies provide convincing evidence that criminal behavior, in both males and females, may have genetic influences. Establishing a heritable component to criminal behavior begs the question as to whether serious forms of criminal behavior, such as violent criminal offending in particular, may also be a heritable trait. Perhaps impulsive violent acts may reflect a genetic predisposition toward this type of behavior while property offending may be driven more by economic or social factors.

Is there a genetic liability to violence?

Twin and adoption studies have been employed to address this question, yielding mixed results. Relying on criminal arrest data, Cloninger and Gottesman reanalyzed the twin data collected by Christiansen and grouped subjects as either violent offenders or property offenders. Heritability for property offenses was found to be .78 while heritability for violent offenses was .50. Although the genetic effect for property offenses was greater than for violent offenses, the data suggest that violent offenses, as assessed by official crime statistics, may also have a heritable underlying component.

Two independent adoption studies, however, have failed to provide support for the hypothesis that violence is a heritable trait (Bohman et al.; Mednick et al.). The largest adoption study to date was carried out in Denmark by the present authors' research group (n = 14,427). Mednick, Gabrielli, and Hutchins had previously reported a significant relationship between the number of criminal convictions in the biological parent and the number of convictions in the adoptees. Subsequent statistical analyses revealed that this relationship held significantly for property offenses, but not significantly for violent offenses.

Perhaps a genetic predisposition toward violence may exist in the presence of some other unidentified mediator. A study in Oregon provided an important clue in that mental illness, particularly severe mental illness, may be genetically related to violence. In a classic study, Heston followed up a sample of forty-seven offspring born to schizophrenic mothers and compared them to a group of matched controls from the same orphanage. These offspring were separated from their mothers shortly after birth and placed in foster care or orphanages. Heston was primarily interested in determining if adopted-away offspring were at increased risk of becoming schizophrenic themselves. The findings supported the original hypothesis, as five of the forty-seven offspring became schizophrenic. An interesting finding is that an even greater number of the adopted-away offspring of schizophrenic biological mothers actually had been incarcerated for violent offenses. Eleven (23.4 percent) of the adoptees had been incarcerated for violent offenses. Since these offspring were not raised by their schizophrenic mothers, this suggested the possibility that mental illness and criminal violence may share a common genetic basis.

With the Heston study in mind, Moffit investigated the role of parental mental illness in the emergence of violent offending among the Danish adopted-away sons. When only the criminal behavior of the biological parents is considered, she found no increase in violent offending in the adoptees. A significant increase in the rate of violent offending is noted only among offspring whose biological parents were severely criminal (typically the biological father) and had been hospitalized one or more times for a psychiatric condition (typically the biological mother).

These findings suggest that a biological background positive for mental disorders appears to be associated with an increased risk of violent offending in the children. Other disorders in the biological parents may also increase the risk of violent offending in the adopted-away offspring. One such disorder that may elevate the risk of violent offending in children is the presence of alcoholism in the biological parents.

The genetic link between violence and alcoholism

Recent molecular genetics studies report that a gene related to the serotonin system may be associated with increased risk for the cooccurrence of violence and alcoholism. These efforts have been fueled by the robust finding that alcoholism and violence, in humans and nonhuman primates, may be related to serotonergic dysregulation (Virkkunen et al., 1989; Higley et al., 1992). In a reanalysis of data from the Swedish Adoption Study, Carey (1993) noted that paternal violence is linked to alcoholism in adopted-away males.

The present authors are currently investigating the possible genetic link between violence and alcoholism (Tehrani and Mednick, forthcoming). Within the context of the Danish Adoption Cohort, we found that alcoholic biological parents were twice as likely to have a violent adopted-away son than nonalcoholic parents. In contrast, the risk for property offenses in adopted-away sons of biological parents with alcohol problems was not significantly elevated. The significant genetic effect was specific to violent offenders. Moreover, violent offending, but not property offending, among the biological parents was associated with severe alcohol-related problems in the adopted-away males. These findings from our adoption cohort are in agreement with data from the Swedish adoption study, and support the overall interpretations from recent molecular genetic studies.

Genetic factors, as determined by a biological background positive for criminality or mental illness, may represent one pathway through which the risk for a certain negative outcome is conferred. Our research group has also explored the role of prenatal factors in the development of criminal behavior.

Prenatal factors

Another pathway that has been investigated as a potential determinant in the etiology of violence is prenatal factors. The prenatal period presents a nine-month window in which the developing fetus may be exposed to a variety of stressors and agents. There are reasons to suspect that these stressors or agents may operate differently depending on when they are introduced. Recently, an increasing amount of attention has been paid to pinpointing the gestational periods of highest risk for negative outcomes. One such teratogen that has been extensively investigated is the timing of maternal influenza exposure in relation to negative outcomes in the exposed fetuses.

Maternal prenatal influenza. In Helsinki, our research group reported that second-trimester maternal influenza significantly increased the risk of adult schizophrenia (Mednick et al., 1988) and major affective disorder (Machon and Mednick) in the exposed fetuses. The data have been replicated in numerous studies in various countries.

The "second-trimester schizophrenics" were interviewed and found to differ from non-influenza exposed schizophrenics in that their symptom picture was dominated by suspiciousness and delusions (Machon and Mednick). As both Volavka and Hodgins suggest, delusional paranoid individuals are characterized by elevated levels of violent behavior. Mednick, Machon, and Huttenen hypothesized that a common etiological link between schizophrenia and violence may be a disturbance in fetal neural development in the second trimester.

Accordingly, Mednick, Machon, and Huttenen (1996) hypothesized that maternal influenza during the second trimester was associated with an increased risk for violent offending, but not property offending among exposed fetuses. To test this hypothesis, the Finnish criminal register was searched for all of the Helsinki residents born in the nine months after the 1957 influenza epidemic. The results indicated that property crime was not significantly associated with period of exposure to the influenza virus. Individuals who had been exposed to the influenza virus during the second trimester of gestation, however, were significantly more likely to have a criminal conviction for violence than individuals who were exposed to the influenza virus during the first or third trimesters of gestation or not exposed to the virus at all.

The impact that the influenza virus has on fetal neural development, either negative or neutral, appears contingent upon the timing of the virus, relative to the stage of gestation. It may also be difficult if not impossible to identify a specific month or trimester associated with the highest risk of negative outcome in cases where the teratogen is present throughout development, or when the long-term effects of the teratogen may linger and have residual effects throughout the period of gestation. Introduction of some types of teratogens, such as illegal drugs, alcohol, and nicotine, may represent substances that, regardless of when they are introduced, could potentially be harmful to the exposed fetus. Much attention has recently been paid to the association between maternal smoking during pregnancy and negative behavioral outcomes among exposed fetuses. These negative outcomes include impulsivity and attention problems. Prenatal nicotine exposure has also been associated with criminal offending.

Maternal prenatal smoking. An investigation conducted in Finland by Rantakallio and colleagues, examined the criminal records of 5,966 members of a birth cohort and found that prenatal maternal smoking predicted to criminal offending at age twenty-two. These findings persisted after controlling for the effects of social variables such as socioeconomic status. With these recent studies in mind, Brennan, Grekin, and Mednick investigated the association between maternal smoking and criminal violence using a Danish birth cohort of 4,129 males. It was hypothesized that maternal smoking would be related to an increased risk of violent offending among males. One of the major strengths of the study was that maternal prenatal smoking was assessed through interviews during the pregnancy as opposed to retrospectively. Moreover, the study relied on the Danish criminal register to identify cases where the individuals were arrested for property or violent offenses.

The findings indicate a linear dose-response relationship between the number of cigarettes the mother smoked on a daily basis in her third trimester of pregnancy and the percent of offspring who became violent offenders. This relationship persists despite controlling for various potential confounds such as socioeconomic status, parental psychiatric hospitalization, and father's criminal history.

The recent finding that maternal smoking during pregnancy is linked to criminal violence in exposed offspring, along with Rantakallio's study, suggests the possibility that chemicals contained in cigarette smoke may alter fetal brain neurochemistry. Moreover, exposure to cigarette smoke prenatally may increase risk for asphyxia.

Biological factors

Biological influences, including psychophysiological and biochemical measures are thought to mediate the relationship between genetics and criminal behavior. Psychophysiological measures, including electroencephalogram (EEG) activity, heart rate (HR), event-related potentials (ERP), and skin conductance (SC), have been identified as potential biological markers that may help to distinguish criminals from noncriminals. This literature has been thoroughly reviewed by Raine.

Other, more direct measures of biological functioning, may provide additional information regarding the role of biological factors in the etiology of criminal behavior. One such factor that has been widely investigated since the last edition of this volume is the role of serotonergic dysregulation in criminal behavior.

Serotonin

Serotonin (5-HT; 5-hydroxytryptamine), a neurotransmitter produced by the raphe nuclei, is thought to be involved in the modulation of impulsivity. Consequently, serotonergic dysregulation may result in a decreased ability to inhibit certain externalizing behavioral patterns and may reflect a deficit in behavioral inhibition. It seems reasonable to hypothesize that violent criminal behavior, an outcome often marked by behavioral disinhibition, may be linked to some type of dysregulation of the serotonin system. A review of biochemical studies that have investigated the role of low serotonin concentrations in the emergence of criminal behavior follows. These studies have primarily examined levels of the cerebrospinal fluid (CSF) 5-HT metabolite, 5-hydroxyindolacetic acid, CSF 5-HIAA.

Recently, an impressive body of evidence, primarily obtained from biochemical studies, has accumulated regarding the role of the serotonin system in criminal behavior. Linnoila and colleagues have reported that within the context of a Finnish forensic population, violent offenders and impulsive fire-setters evidenced lower mean CSF 5-HIAA than normal controls (Virkkunen et al., 1989). This seems to suggest that serotonin dysfunction may play an etiologic role in more severe forms of antisocial behavior, such as violent offending. These studies have been extended to investigate whether serotonin levels can differentiate offender populations based upon type of the index offense and the presence or absence of alcohol abuse and violence in first-degree family members.

Virkkunen and others (1996) report that a combination of paternal violence and alcoholism, as measured by questionnaires to the first-degree relatives, was associated with low CSF 5-HIAA concentration levels in the male subjects, irrespective of subgroup classification (i.e., impulsive vs. nonimpulsive). The authors suggest that a familial trait may be associated with early-onset alcohol abuse, violent and impulsive offending, and low CSF 5-HIAA concentrations.

Subjects who had committed violent crimes during the 4.5-year follow-up period had lower CSF levels compared to nonrecidivists. Moreover, violent recidivists were more likely to have experienced paternal absence than nonrecidivists, suggesting the importance of both biological and environmental factors in the prediction of recidivistic violent offending. Due to the highly selective nature of the sample, results must be interpreted cautiously. A significant relationship between aggressiveness, parental absence, and low levels of serotonin was also noted in a study of nonhuman primates (Higley et al., 1993).

Virkkunen and others (1994) reported that impulsive violent offenses and impulsive fire-setters were found to evidence lower CSF 5-HIAA concentration levels; violent alcohol offenders whose index crime was not found to be impulsive had normal CSF 5-HIAA concentrations. The emphasis on the index offense as opposed to the qualitative nature of the cumulative criminal history, however, may be interpreted as a weakness of this study. On the basis of these findings, Virkkunen and colleagues propose that low serotonin may be a biological marker specific to impulsive violent offending accompanied by alcoholism. These conclusions, however, are drawn from a subject pool of forensic patients, representing a sample of heavily violent individuals. Within the context of a community sample, Hibbeln and others found that relative to the nonviolent control group, the violent group evidenced significantly lower concentration levels of CSF 5-HIAA.

One of the limitations of the biochemical studies is that CSF metabolites reflect presynaptic neurotransmitter activity; therefore, it is not known what is occurring at the postsynaptic level. Apart from the lack of specificity in information, efforts to investigate the role of serotonin in behavioral outcomes in humans have been challenging due to the fact that CSF levels of serotonin are collected via a lumbar puncture. More importantly, examination of the CSF does not provide information about the role of specific brain regions. Results from neuropsychological measures, for example, have consistently found neurological deficits to be present among antisocial persons than in nonantisocial persons. The limitation of neuropsychological indices, however, is that they present an indirect measure of brain functioning. Other, more recent techniques, have been applied to uncover the structural and functional properties of the brain in relation to criminal behavior. Brain imagining techniques, for example, have received an increasingly prominent role in the study of criminal behavior. These recent advances may in fact represent an important sector of the future of biological research in the field of criminal behavior.

Future directions: brain imaging and criminal behavior

The field of neuroscience, through the use of brain imaging techniques, has provided illuminating data on the etiology of severe mental disorders, including depression and schizophrenia. These recent technological innovations are computerized tomography (CT) and magnetic resonance imaging (MRI), which provide information on brain structure, and positron emission tomography (PET) and regional cerebral blood flow (RCBF), which provide information on brain functioning. The advances and disadvantages of each method are thoroughly discussed in Raine (1993). These methods have recently been applied to the study of criminal behavior, lending support to the theory that criminal behavior may be associated with brain dysfunction.

To date, over 20 studies using these techniques have been published (see Raine, 1996). Taken together, these studies suggest that frontal and temporal dysfunction may be associated with violent behavior. The link between frontal dysfunction and impulsive, violent criminality is consistent with the notion that frontal lobe damage may be associated with a variety of correlates of violent behavior, including impulsivity, behavioral disinhibition, and poor concentration (Raine, 1993). It should be noted that these brain abnormalities may be caused by genetic, biological, or environmental agents. Criminals may be more likely to be involved in physical fights than noncriminals, and sustain head injuries as a result. Frontal lobe damage may also be attributed to birth or delivery complications, for example. Another concern relates to the issue of timing. Are structural and functional deficits present prior to the onset of criminal behavior, or are these changes in the brain triggered after the individual has begun their criminal career? To our knowledge, no study has been conducted examining pre-morbid measures of brain structure and function among criminals. Despite these issues, it is likely that our understanding of the biological and genetic underpinnings of criminal behavior will be greatly advanced through continued developments in brain imaging research.

Conclusions

1. Twin and adoption studies lend support to the notion that criminal behavior has important genetic influences. The role of genetics in violent offending, however, is less clear. Our research, along with other epidemiological studies and molecular genetic investigations, have shown that violence may be genetically related to mental illness and to alcoholism.
2. Violent offending, but not property offending, may be associated with a disturbance in fetal development. We have demonstrated that prenatal disturbances, such as exposure to the influenza virus during the second trimester of gestation and maternal smoking during pregnancy, is linked to offspring violent offending. These data suggest the possibility that the introduction of some type of teratogen during gestation may alter normal fetal development.
3. Lower levels of serotonin have been found to distinguish criminals from noncriminals in both forensic and community samples. Serotonergic dysregulation appears to be specific to violent offenders who have committed impulsive crimes.
4. Technological advances, such as the use of brain imaging, will undoubtedly provide exciting new data on the biological underpinnings of criminal behavior. The data thus far suggest that frontal lobe deficits may be marked among violent offenders. Continued efforts to pinpoint specific brain regions associated with an increased risk in violent offending will advance our understanding of the etiology of violent criminal behavior.

Jasmine A. Tehrani

Sarnoff A. Mednick

See also Diminshed Capacity; Excuse: Insanity; Intelligence and Crime; Mentally Disordered Offenders; Prediction of Crime and Recidivism; Psychopathy; Scientific Evidence; Violence.

BIBLIOGRAPHY

Baker, Laura A.; Mack, Wendy; Moffitt, Temi E.; and Mednick, Sarnoff A. "Sex Differences in Property Crime in a Danish Adoption Cohort." Behavior Genetics 19 (1987): 355–370.

Bohman, Michael. "Some Genetic Aspects of Alcoholism and Criminality." Archives of General Psychiatry 35 (1978): 269–276.

Bohman, Michael; Cloninger, C. Robert; Sigvardsson, Soren; and von Knorring, Anne Lis. "Predisposition to Petty Criminality in Swedish Adoptees." Archives of General Psychiatry 39 (1982): 1233–1241.

Brennan, Patricia A.: Grekin, Emily R.; and Mednick, Sarnoff A. "Maternal Smoking during Pregnancy and Adult Male Criminal Outcomes." Archives of General Psychiatry 56 (1999): 215–219.

Cadoret, Remi J., and Cain, Colleen. "Sex Differences in Predictors of Antisocial Behavior in Adoptees." Archives of General Psychiatry 37 (1980): 1171–1775.

Cadoret, Remi J.; Cain, Colleen; and Crowe, R. R. "Evidence for Gene-Environment Interaction in the Development of Adolescent Anti-social Behavior." Behavior Genetics 13 (1983): 301–310.

Cadoret, Remi J.; O'Gorman, Thomas W.; Troughton, Ed; and Heywood, Ellen. "Alcoholism and Antisocial Personality: Interrelationships, Genetic and Environmental Factors." Archives of General Psychiatry 42 (1985): 161–167.

Cadoret, Remi J.; Troughton, Ed; and O'Gorman, Thomas. "Genetic and Environmental Factors in Alcohol Abuse and Antisocial Personality." Journal of Studies on Alcohol 48 (1987): 1–8.

Cadoret, Remi J.; Yates, William R.; Troughton, Ed; Woodworth, George; and Stewart, Mark A. "Genetic-Environmental Interaction in the Genesis of Aggressivity and Conduct Disorders." Archives of General Psychiatry 52 (1995): 916–924.

Carey, Gregory. "Twin Imitation for Antisocial Behavior: Implications for Genetic and Family Environment Research." Journal of Abnormal Psychology 101 (1992): 18–25.

——. "Multivariate Genetic Relationships among Drug Abuse, Alcohol Abuse and Anti-social Personality." Psychiatric Genetics 3 (1993): 141.

Carey, Gregory, and Goldman, David. "The Genetic of Antisocial Behavior." In The Handbook of Antisocial Behavior. Edited by Stoff, D. M., Breiling, J., and Maser J. D. New York: John Wiley, 1996.

Christiansen, Karl O. "A Preliminary Study of Criminality among Twins." In Biological Bases of Criminal Behavior. Edited by S. A. Mednick and K. O. Christiansen. New York: Gardener Press, 1997. Pages 89–108.

Cloninger, C. Robert, and Gottesman, Irving. "Genetic and Environmental Factors in Anti-social Behavior Disorders." In The Causes of Crime: New Biological Approaches. Edited by S. A. Mednick, T. E. Moffit, and S. A. Stack. New York: Cambridge University Press, 1987.

Cloninger, C. Robert; Bohman, Michael; and Sigvardsson, Soren. "Inheritance of Alcohol Abuse." Archives of General Psychiatry 38 (1981): 861–868.

Cloninger, C. Robert; Christiansen, Karl O.; Reich, Thomas; and Gottesman, Irving I. "Implications of Sex Differences in the Prevalences of Antisocial Personality, Alcoholism, and Criminality for Familial Transmission." Archives of General Psychiatry 35 (1978): 941–951.

Cloninger, C. Robert; Sigvardsson, Soren; Bohman, Michael; and von Knorring, Anne Lis. "Predisposition to Petty Criminality in Swedish Adoptees. II. Cross-fostering Analysis of Gene-Environment Interaction." Archives of General Psychiatry 39 (1982): 1242–1247.

Crowe, Raymond R. "An Adoption Study of Antisocial Behavior." Archives of General Psychiatry 31 (1974): 785–791.

Dalgaard, Ole S., and Kringlen, Einar A. "A Norwegian Twin Study of Criminality." British Journal of Criminology 16 (1976): 213–232.

Grove, William M.; Eckert, E. D.; Heston, L.; Bouchard, T. J.; Segal, Nyand; and Lykken, D. Y. "Heritability of Substance Abuse and Antisocial Behavior: A Study of Monozygotic Twins Reared Apart." Biological Psychiatry 27 (1990): 1293–1304.

Hallikainen, Tero; Saito, Takuta; Lachman, Herbert M.; and Volavka, Jan. "Association between Low Activity Serotonin Transporter Promoter Genotype with Habitual Impulsive Violent Behavior among Antisocial Early Alcoholics." Molecular Psychiatry 32 (1999): 432–438.

Heinz, Andres; Higley, J. Dee; Gorey, Julia G.; Saunders, Richard C.; Jones, Douglas; Hommer, Daniel; Zajicek, Kristin; Soumi, Stephen; Lesch, Klaus-Peter; Weinberger, Daniel; and Linnoila, Markku. "In Vivo Association between Alcohol Intoxication, Aggression and Serotonin Transporter Availability in Nonohuman Primates." American Journal of Psychiatry 155 (1998): 1023–1028.

Heston, Lee L. "Psychiatric Disorders in Foster-Home Reared Children of Schizophrenics." British Journal of Psychiatry 112 (1996): 819–825.

Hibbeln, J. R.; Linnoila, M.; Umhau, J. C.; Rawlings, R.; George, D. T.; and Salem, N. "Essential Fatty Acids Predict Metabolites of Serotonin and Dopamine in Cerebrospinal Fluid among Healthy Control Subjects, and Early and Late-Onset Alcoholics." Biological Psychiatry 44 (1998): 235–242.

Higley, J. Dee; Thompson, W.; Champoux, M.: Goldman, D.; Haert, M. F.; Kraemer, G. W.; Scanlan, J. M.; Suomu, S. J.; and Linnoila, M. "Paternal and Maternal Genetic and Environmental Contributions to Cerebrospinal Fluid Monoamine Metabolites in Rhesus Monkeys." Archives of General Psychiatry 50 (1993): 615–662.

Lappalainen, Jaakko; Long, Jeffrey C.; Eggert, Monica; Ozaki, Norio; Robin, Robert W.; Brown, Gerald L.; Naukkarinen, Hannu; Virkkunen, Matti; Linnoila, Markku; and Goldman, David. "Linkage of Antisocial Alcoholism to the Serotonin 5-HT1B Receptor Gene in 2 Populations." Archives of General Psychiatry 55 (1998): 989–994.

Lyons, Michael J. "A Twin Study of Self-Reported Criminal Behavior." In Genetics of Criminal and Antisocial Behavior. Edited by C. Foundation. Chichester, U.K.: Wiley, 1996. Pages 61–69.

Machon, Ricardo A., and Mednick, Sarnoff A. "Adult Schizophrenia and Early Neurodevelopmental Disturbances." In Confrontations Psychiatriques: Epidemiologie et Psychiatrie, no. 35. Specia Rhone-Poulenc Rorer, 1994. Pages 189–215.

Machon, Ricardo A.; Mednick, Sarnoff A.; and Huttenen, Matti O. "Adult Major Affective Disorder following Prenatal Exposure to an Influenza Epidemic." Archives of General Psychiatry 54 (1997): 322–328.

Mednick, Sarnoff A.; Gabrielli, William F.; and Hutchings, Barry. "Genetic Influences in Criminal Convictions: Evidence From an Adoption Cohort." Science 224 (1984): 891–894.

Mednick, Sarnoff A.; Machon, Ricardo A.; Huttunen, Matti O.; and Barr, Christopher E. "Influenza and Schizophrenia: Helsinki vs. Edinburgh." Archives of General Psychiatry 47 (1990): 875–876.

Mednick, Sarnoff A.; Machon, Ricardo A.; Huttunen, Matti O.; and Bonnet, D. "Adult Schizophrenia following Prenatal Exposure to an Influenza Epidemic." Archives of General Psychiatry 45 (1988): 189–192.

Mednick, Sarnoff A.; Machon, Ricardo A.; and Huttenen, Matti. "Second Trimester Influenza Virus Predicts to Violent but not Property Offending." In Tehrani, Jasmine A.; Brennan, Patricia A.; Hodgins, Sheleigh; and Mednick, Sarnoff A. "Mental Illness and Criminal Violence." Social Psychiatry and Psychiatric Epidemiology 33 (1998): 81–85.

Moffit, Temi E. "Parental Mental Disorder and Offspring Criminal Behavior: An Adoption Study." Psychiatry: Interpersonal and Biological Processes 50 (1987): 346–360.

Raine, Adrian. The Psychopathology of Crime: Criminal Behavior as a Clinical Disorder. San Diego, Calif.: Academic Press, 1993.

——. "Antisocial Behavior and Psychophysiology: A Biosocial Perspective and a Prefrontal Dysfunctional Hypothesis." Edited by D. M. Stoff, J. Breiling, and J. D. Maser. New York: Wiley, 1996.

Rantakallio, P.; Laara, E.; Isohanni, M.; and Moilanen, I. "Maternal Smoking during Pregnancy and Delinquency of the Offspring: An Association Without Causation?" International Journal of Epidemiology 1992. 21, 1106–1113.

Sigvardsson, Soren; Bohman, Michael; and Cloninger, C. Robert. "Replication of the Stockholm Adoption Study of Alcoholism." Archives of General Psychiatry 53 (1996): 681–687.

Sigvardsson, Soren; Cloninger, C. Robert; Bohman, Michael; and von Knorring, Anne Lis. "Predisposition to Petty Criminality in Swedish Adoptees. III. Sex Differences and Validation of the Male Typology." Archives of General Psychiatry 39 (1982): 1248–1253.

Slutske, Wendy S.; Heath, Andrew C.; Dinwiddie, S. H.; and Madden, Pamela. "Modeling Genetic and Environmental Influences in the Etiology of Conduct Disorder: A Study of 2,682 Adult Twin Pairs." Journal of Abnormal Psychology 106 (1996): 266–279.

Tehrani, Jasmine A.; and Mednick, Sarnoff A. "Genetic Cross-relationships between Criminal Behavior and Severe Alcohol-related Problems." (Manuscript submitted.)

Van Dusen, Karen T.; Mednick, Sarnoff A.; Gabrielli, William F.; and Hutchings, Barry. "Social Class and Crime in an Adoption Cohort." The Journal of Criminal Law and Criminology 74 (1983): 249–261.

Virkkunen, Matti; De Jong, Judith; Bartko, F.; Goodwin, Fredrick; and Linnoila, Markku. "Relationship of Psychobiological Variables to Recidivism in Violent Offenders and Impulsive Fire Setters." Archives of General Psychiatry (1989): 600–604.

Virkkunen, Matti; Eggert, Monika; Rawlings, Robert; and Linnoila, Markku. "A Prospective Follow-up Study of Alcoholic Violent Offenders and Fire Setters." Archives of General Psychiatry 53 (1996): 523–529.

Virkkunen, Matti; Rawlings, Robert; Tokola, Riita; Poland, Russell; Guidotti, Alessandro; Nemeroff, Charles; Bissette, Garth; Kalogeras, Konstantine; Karonen, Sirkka-Liisa; and Linnoila, Markku. "CSF Biochemistries, Glucose Metabolism, and Diurnal Activity Rhythms in Alcoholic, Violent Offenders, Fire Setters and Healthy Volunteers." Archives of General Psychiatry 51 (1994): 20–27.

Volavka, Jan. Neurobiology of Violence. Washington D.C.: American Psychiatric Press, 1995.

Wolfgang, Marvin; Figlio, R. M.; and Sellin, T. Delinquency in a Birth Cohort. Chicago: University of Chicago Press, 1972.