by Adrian Raine
We see here, very clearly, that Gage had been transformed from a well-controlled, well-respected railway worker into a pseudo-psychopath—an individual with psychopathic traits. Like many patients with frontal-lobe damage, he was impulsive, irresponsible, and was reputed to have been sexually promiscuous and a drunkard.15 He was fired by his employer because he was unreliable. He took on a series of jobs and moved around, switching from one job to another. Eventually he went on tour with the tamping rod and appeared in Barnum’s American Museum in New York and other public shows (see Figure 5.3). Among his many jobs he worked at an inn in Hanover, New Hampshire, in 1851, looking after horses. A spirited, risk-taking adventurer, he even spent several years in Chile as a stagecoach driver before traveling to California, where he worked on a series of farms until his premature death on May 21, 1860, after a series of epileptic seizures. Despite a most remarkable recovery from what should have been a mortal wound, that tamping rod he carried with him for the remainder of his life eventually got the better of him.
The case was such a remarkable one that medical doctors at the time scoffed at the idea that anyone could survive such an injury, and viewed it as a hoax. It could not possibly be true. While it was indeed a true case, could it nevertheless be unique? Can accidental damage to the prefrontal cortex really transform an otherwise normal, law-abiding individual into a capricious, psychopathic–like, antisocial individual?
Figure 5.3 Phineas Gage at Barnum’s American Museum holding the tamping rod that destroyed his prefrontal cortex
The answer can be found back in Antonio Damasio’s and others’ laboratories. A large body of evidence has now convincingly shown that adults suffering head injuries that damage the prefrontal cortex—especially the lower, ventral region—do indeed show disinhibited, impulsive, antisocial behavior that does not conform to the norms of society.16
But you could counter that adults have brains that are relatively fixed. What about children, whose developing brains show much greater plasticity? Does damage to the prefrontal cortex in youngsters also lead to antisocial behavior? Overwhelmingly, studies of the behavioral changes that follow head injuries in children find that conduct disorder and externalizing behavior problems are common.17, 18 While some other children develop internalizing behavior problems like anxiety and depression,19 there is little doubt overall that head injuries in children predispose them to impulsive, dysregulated behavior.20
But what if the damage to the prefrontal cortex occurs really early during infancy? Surely there is enormous plasticity of the brain at this developmental stage, allowing it to recover lost functions and to resume normality. Clinical cases of such selective prefrontal damage are rare, but they confirm that prefrontal lesions very early in life can directly lead to antisocial and aggressive behavior. A study from Damasio’s laboratory reported on two cases—one female, one male—who suffered selective lesions to the prefrontal cortex in the first sixteen months of life.21 Both showed early antisocial behavior that progressed into delinquency in adolescence and criminal behavior in adulthood, and included impulsive aggressive and nonaggressive forms of antisocial behavior. Both also had autonomic deficits, poor decision-making skills, and deficits on learning from feedback. Yet again we see that triad of traits that Antoine Bechara and Antonio Damasio clearly documented in those suffering prefrontal damage in adulthood—psychopathic behavior, autonomic impairments, and reduced somatic markers.
I know what you’re thinking. The clear limitation is that we are dealing with only two cases—one case more than the one presented by Phineas Gage. However, another laboratory reported on nine cases of children who suffered frontal lesions in the first ten years of life.22 All nine suffered behavioral problems after the injuries, with seven of the nine developing conduct disorder. Even in the case of the remaining two, they both exhibited either impulsive, labile behavior or uncontrollable behavior.
These cases, when taken together, strongly suggest that damage to the prefrontal cortex can directly lead to antisocial and aggressive behavior. It’s an important point. Brain-imaging research showing that murderers and those with antisocial personalities have prefrontal abnormalities demonstrate that a relationship exists. But do prefrontal structural and functional impairments cause crime and violence—or does violence cause the brain impairment? Violent offenders get into fights, and so can acquire “closed” head injuries: the skull is not broken but there is internal damage to the brain. It’s certainly possible, yet neurological case studies showing that prefrontal impairments in infancy, adolescence, and adulthood are later followed by antisocial, aggressive, and psychopathic-like behavior are telling. They provide striking support for a causal explanation flowing from prefrontal impairments to a disinhibited personality to violence.
DIGGING DEEPER INTO THE PREFRONTAL CORTEX
We have seen from MRI studies that antisocial individuals in the community have structural brain impairments. We have also seen from the clinic that patients with head injuries causing prefrontal structural damage develop antisocial behavior and a loss of somatic markers, resulting in poor decision-making and maladaptive social behavior. We were therefore finding interesting similarities between our antisocial temp workers and the neurological clinical cases of Antonio Damasio and his colleagues. We were excited by these initial findings and wanted to dig deeper into these parallel findings from community to clinic. Two specific issues came to the fore.
First, the autonomic, emotional impairments in the head-injured patients of Damasio and Bechara raised the question of whether or not our antisocial temp workers also showed somatic marker impairments. This was a hypothesis that we tested out. As you may recall from chapter 4 we put our subjects through a stress task in which they had to talk about their worst faults. As pointed out by Damasio, this is a very appropriate task in the context of the somatic-marker hypothesis because it elicits secondary emotions—embarrassment, shame, guilt—that are the province of the ventral prefrontal cortex.23
We found that our antisocial, psychopathic subjects not only had a significant volume reduction in prefrontal gray matter, but also showed reduced skin conductance and heart-rate reactivity during the social stressor task. Sure enough, they did lack somatic markers, just as Damasio’s prefrontal patients did. Furthermore, when we divided our antisocial group into those with particularly low prefrontal gray volumes and those with near-normal volumes, we found that it was the former group—those with the structural prefrontal impairment—who particularly showed somatic-marker deficits.24 We were finding an interesting convergence of somatic-marker impairments, prefrontal structural deficits, and antisocial behavior that bore a striking resemblance to the findings on Damasio and Bechara’s patients.
The second issue concerned the localization of the structural impairment. Where exactly within the prefrontal cortex did our antisocial, psychopathic individuals have reduced gray-matter volume? Damasio had written an editorial on our original findings, posing the question of whether in future work the deficit may be localized in orbital and medial sectors of the prefrontal cortex.25 Recall that the tamping rod entered underneath Phineas Gage’s eye and traveled straight up his prefrontal cortex. Hanna Damasio had demonstrated from her careful and rigorous reconstruction of the tamping-rod accident that the damage to Gage’s brain was localized to the ventral and orbitofrontal part—the lower region—and also the medial or middle part of the prefrontal cortex.26 What would we find if we made a more detailed analysis of the precise location of the prefrontal volume reduction in our antisocials?
Dividing up the sectors of the prefrontal cortex involved much more complex sulcal landmark identification and tracing of slices; it took us literally years to complete, but eventually we got there. You can see in Figure 5.4, in the color-plate section, what we did. You are looking head-on at one of our antisocial subjects, and we are taking a slice through the frontal cortex. From top to bottom, moving from twelve o’clock to six o’clock, these regions consist of the superior
frontal gyrus, middle frontal gyrus, inferior frontal gyrus, orbitofrontal gyrus, and the ventromedial area.27 In which sector did we see a significant volume reduction in those with antisocial personality disorder?
Three of the five sectors turned up trumps. As Antonio Damasio would have predicted, antisocial individuals showed a 9 percent bilateral reduction in the orbitofrontal gyrus, together with a 16 percent reduction in the volume of the right ventromedial prefrontal cortex. It is structural impairment to the ventral region of the prefrontal cortex that seems to be particularly implicated in antisocial, psychopathic behavior—the same brain region devastated by the tamping rod on that fateful day for Phineas Gage in 1848.
The third sector provided us with a different but complementary perspective to consider. Our antisocial subjects had a 20 percent volume reduction in the right middle frontal gyrus. In chapter 4 we discussed how neuropsychological research had demonstrated poorer “executive functioning” in antisocial and psychopathic individuals—reduced ability to plan ahead, regulate behavior, and make appropriate decisions. The brain areas classically associated with these executive functions lie in the dorsolateral prefrontal cortex. “Dorso” refers to top and “lateral” refers to side—so “dorsolateral” is the upper, side part of the prefrontal cortex. If you look at Figure 5.4, that’s exactly where the middle frontal gyrus is located. And if we look further into the functioning of this brain area, impairment in antisocial offenders makes quite a lot of sense.
Let us consider some of the normal functions of the middle frontal region that have been gleaned from functional-imaging and brain-lesion studies—functions that could well be impaired in offenders. First, the middle frontal gyrus, which makes up Brodmann areas 9, 10, and 46, is part of the neural circuitry that subserves fear conditioning.28 We saw earlier that criminals and psychopaths have poor fear conditioning. Second, it plays a role in inhibiting behavioral responses,29 and we know that offenders frequently show disinhibited, impulsive behavior.30 The middle frontal gyrus is also involved in moral decision-making,31 and offenders have impaired moral judgment and break moral boundaries.32 It is further involved in choosing delayed rewards as opposed to immediate rewards,33 and it is well documented that offenders are less able to delay gratification.34, 35 It is activated by empathy to pain stimuli,36 and antisocial individuals lack empathy.37 This prefrontal subregion is also activated when we look inward and evaluate our own thoughts and feelings.38 Offenders are characterized by a lack of insight into the harm they perpetrate on people around them.39
Clearly the middle frontal gyrus, which is significantly compromised in those with antisocial personality disorder, is heavily involved in cognitive, affective, and behavioral characteristics that antisocial individuals are deficient in. These deficiencies in turn contribute to their antisocial tendencies. We can complete the circle from brain structure to functional deficiencies to antisociality.
In a similar vein, there is more to the ventral region of the prefrontal cortex than effective decision-making. We know that it is involved in controlling and correcting punishment-related behavior,40 and in what neuropsychologists call “response perseveration.”41 And yes, recidivistic offenders are revolving-door guests in prisons. They seem unable to learn from their mistakes. They keep on making the same behavioral responses that resulted before in punishment and prison—what psychologists call perseveration.42 Fear conditioning is another process governed by the ventral prefrontal cortex, and we have seen that offenders have deficits in this area.43 The ventral area has also been implicated in compassion and care for others,44 as well as sensitivity to others’ emotional states.45 Let’s face it, we all know that criminals and psychopaths are not the most caring people in the world.46 As with the middle frontal gyrus, insight47 and behavioral disinhibition48 are also subserved by this ventromedial region. Offenders are disinhibited and psychopaths lack self-insight. Interestingly, the ventral prefrontal cortex also helps to reduce negative emotions during parent-child interactions,49 and offenders were likely as children to have thrown temper-tantrums with their parents. Emotion regulation is another ventral prefrontal function,50 and emotional dysregulation characterizes impulsively aggressive individuals.51
Taking both dorsal and ventral structures together, there are quite compelling reasons to believe that structural impairments to these regions can give rise to a constellation of social, cognitive, and emotional risk factors that predispose someone to antisocial behavior and an antisocial personality. The fact that both ventral and middle frontal brain regions contribute to some of the same functional risk factors for antisocial behavior—poor fear conditioning, lack of insight, disinhibition—highlights the salience of these well-replicated neurocognitive risk factors. It also tells us that an outcome of antisocial behavior may be especially likely when both of these regions are structurally compromised.
So far we have dug deeper into the prefrontal cortex and discovered that the ventral and middle frontal gyrus are the key culprits when it comes to crime. But these brain areas are guilty not only of their crimes as charged. Our next level of probing of the prefrontal cortex will implicate these same subregions in a different but equally fundamental societal question—why are men more violent than women?
MALE BRAINS—CRIMINAL MINDS
There’s no escaping the fact. Men are meaner than women. But why? Sex differences in crime and violence have traditionally been put down to sex differences in socialization. If you have a little girl, you give her a doll to look after. If you have a little boy, you give him a toy gun to shoot other kids with. We socialize boys and girls differently, and that’s why boys bully more than girls. It’s seemingly that simple. But have the social scientists really got it right?
An answer can be found by exploring the geography of the prefrontal cortex. What I never told you about in our temp study is that we started off testing women as well as men. But we soon gave up trying to recruit female felons. You women out there are the wonderful angels that make the world go round. It’s we men that maketh mayhem. We had recruited just seventeen women in our sample and we were finding that they were not giving us a lot in terms of crime and violence. Plus, our money for the study was tight. So when the going got tough, we dumped the dames and recruited the tough guys. That was a mistake in retrospect, but we still had just enough women in our sample to test a controversial counterhypothesis to differential socialization as a cause of sex differences in crime. Could it be that there are fundamental brain differences between men and women that explain why men commit more crime?
We compared men with women on prefrontal brain volumes. Men had a 12.6 percent volume reduction in the orbitofrontal gray compared with women.52 That’s the underneath part of the prefrontal cortex. Men with reduced ventral gray were more antisocial than men with normal ventral gray volumes. We’ve seen that already, but what was new in our analyses was that women with reduced ventral gray volumes were more antisocial than women with normal gray volumes. We get the same brain effect in antisocial women that we find in antisocial men. Hold these findings in your prefrontal cortex’s working memory for a minute.
Men, of course, were found to be more antisocial and criminal than women, replicating a worldwide finding. No big deal. But what if we look again at this sex difference in crime, this time controlling for the sex difference in ventral gray volume? If we make men and women statistically the same in terms of their ventral volume, we cut the sex difference in crime by 77 percent.53 So more than half of the reason men and women differ in crime seems to be because their brains are physically different.
I’m not saying that all the difference in crime between men and women can be put down to the brain. And I’m certainly not saying that we should ignore differences in socialization and other social and parenting influences. But what I am arguing is that there are fundamental neurobiological differences between men and women that can help explain the gender difference in crime. It’s also striking that we find sex differences in the
very same frontal sectors that are linked to antisocial behavior—men and women did not differ in prefrontal sectors that are not related to crime.
These findings do not come out of the blue. Sex differences in prefrontal gray have been documented in several other MRI studies. One imaging study found a 16.7 percent reduction in orbitofrontal volumes in men compared with women.54 Three other studies have found this same sex difference,55 including one large study of 465 normal adults.56 Men have also been reported to show lower activation of the orbitofrontal cortex compared with women when performing a wide variety of cognitive and emotional tasks, including verbal fluency,57 working memory,58 processing threat stimuli,59 and working memory during a negative emotional context.60 Men simply have different brains from women, and it’s pointless to cover up and ignore these fundamental sex differences.
THREE CHORDS OF CAUTION
The position so far looks like this: We’ve seen that offenders have structural impairment to the prefrontal cortex. We’ve also seen that they have poor functioning of this same brain region. We documented in a meta-analysis of forty-three brain-imaging studies of offenders involving 1,262 subjects that these structural and functional prefrontal deficits are replicable findings.61 The structural prefrontal impairment partly explains the sex difference in crime. It’s hard to escape from the conclusion that impairment to this brain region—through either environmental or genetic causes or both—predisposes some to an antisocial, disinhibited, impulsive lifestyle.