PMID 15642645 — A neurobiological perspective on attachment problems in sexual offenders and...
thin_results R=488w / 3¶ | figs=4 Arani
TITLE
[1] 23w A neurobiological perspective on attachment problems in sexual offenders and the role of selective serotonin re-uptake inhibitors in the treatment of such problems
ABSTRACT
[1] 225w This paper describes what is currently known about attachment from the development, social-cognitive and biological literatures and outlines the impact on organisms given adverse development experiences that can have an effect upon attachment formation in childhood across these three literatures. We then describe the effects that dinsecureT attachment styles arising in childhood can affect brain chemistry and brain function and subsequently adult social/romantic relationships. In the paper, we note that a number of sexual offenders report adverse childhood experiences and that they possess attachment styles that, taken together, make it likely that they will either seek out intimate attachments in ways where they will have sex with children, perhaps confusing sex with intimacy or in aggressive ways as particularly happens with men who sexually assault adult women. The last section of the paper describes chemical treatment for sexual offenders, focusing on the use of selective serotonin re-uptake inhibitors (SSRIs). We note evidence for the role of SSRIs in promoting more social/affiliative behaviors and speculate on the effects that SSRIs have in the treatment of sexual offenders by targeting areas of the social brain. Here, we would argue that it would be useful to carry out treatment where there is a combination of SSRI treatment (to promote more prosocial feelings and behaviors) in conjunction with therapy that typically addresses thoughts and behaviors, i.e., cognitive-behavioral therapy/schema-focused therapy.
INTRO
[1] 204w Recent thinking in the area of sexual abuse is that sexual offenders, in general, have deficits in four areas of functioning: (1) (deviant) sexual interest/deviant arousal; (2) attitudes supportive of sexual assault; (3) socioemotional functioning problems and (4) self-management/general self-regulation problems (Thornton, 2002). Cognitive-behavioral treatment has been shown to be quite good at addressing these four areas of functioning except it has been found that, for most pedophilic/fixated offenders, many hundreds of hours of therapy are needed to produce any shifts at all in socioemotional problems, such as levels of inadequacy, distorted intimacy balance (feeling that emotional intimacy is easier with children than adults), aggressive thinking, callous/unemotional traits and emotional loneliness (Beech, Fisher, & Beckett, 1999). Such problems are clearly important risk factors in the future commission of sexual offenses (Thornton, 2002). According to Ward and Siegert (2002), the primary cause of such interpersonal functioning problems is insecure attachment in childhood and subsequent adult attachment problems (Ward, Hudson, & Marshall, 1996). Adult attachment style is a relatively enduring set of characteristics for making sense of one's life experiences (Young, Klosko, & Weisharr, 2003). Hence, the attachment problems underlying these socioemotional problems are a set of enduring interpersonal difficulties for a number of sexual offenders.
[2] 186w A history of poor attachment has been widely noted in sexual offenders' histories (Becker, 1998;Browne & Herbert, 1997;Marshall, Serran, & Cortoni, 2000). Awad, Saunders, and Levene (1984), for example, reported that some parents of adolescent sex offenders were rejecting, abusive or emotionally detached. Craissati, McClurg, and Browne (2002) in a review of the literature found that family backgrounds of sexual offenders are typified by neglect, violence and disruption. Rejection has also been described as a developmental marker for the likelihood of somebody becoming a sexual abuser in that Marshall (1989) noted that derratic and rejecting parenting behaviors, which alienate the children from the possibility of forming secure attachment bonds, distinguish the family context in which sexual offenders grow upT (p. 497). While Smallbone and Dadds (1998) found that poor paternal attachments predicted sexual coercion in adulthood and that a poor relationship with one's mother was predictive of general antisocial behavior. It is noteworthy that Hanson and Bussie `re (1998), in their metaanalytic review of variables related to sex offender recidivism, found that a negative relationship with mother was the only developmental variable related to subsequent recidivism.
[3] 125w Attachments are thought to lead to positive emotional states such as joy, when attachments are renewed and security, when the attachment bond is maintained (Ward et al., 1996). Ward et al. note that negative emotional states can occur when attachments are threatened or lost. As for a link between vulnerability factors and sexual offending, attachment problems may lead offenders having difficulties in forming relationships with age appropriate adults (Marshall, 1989). Marshall et al. (2000) note that individuals with insecure attachment are more likely to evidence poor coping strategies. Burk and Burkhart (2003) outline a clear etiological relationship between disorganized attachment-where the individual has had to cope with a frightened or frightening caregiver such that they have not developed or adequately internalized self-regulatory skills-and sexual offending.
[4] 150w The genesis of adult attachment problems, according to Bowlby (1969Bowlby ( , 1973Bowlby ( , 1980)), is that adverse experiences with primary caregivers have an influence upon the development of the internal working models of self and others (Bowlby, 1969, p. 80). The essential components of such an internal model include memories of attachment-related experiences, beliefs, expectations and attitudes about relationships, as well as plans and strategies for achieving attachment-related goals (Collins & Read, 1994). Ward et al. (1996) note that the developmental bond to the primary caregiver during a child's early years constitutes the first stage of the attachment process. Childhood attachment relationships, whether positive or negative, provide a template for future interactions and relationships with others. Ward et al. argue that this is how expectations are developed in that individuals dmay see themselves as worthy and deserving of other's attention, or conversely as worthless and undeserving of attentionT.
[5] 143w The internal working model is also postulated to have an effect upon future romantic relationships in that types of adult attachment styles have been found to be related to the quality of emotional relationships (Hazan & Shaver, 1987). Those who had a secure (positive) attachment style were found to hold more positive attitudes about interpersonal relationships than the more distant style of romantic attachment in those who had a more avoidant (insecure) attachment style. Marshall, Hudson, and Hodkinson (1993) note that childhood attachment difficulties can lead adults to seek emotional intimacy through sex, even if they have to force a partner to participate. Craissati et al. (2002) comment that, if an individual has a history of poor attachment, they may try to suppress their own negative attachment experiences through substance misuse or dissociation, which again can be seen as precursors to offenserelated activity.
[6] 120w Although the biological basis of attachment has been extensively examined both in human and animal analogs, this literature is barely mentioned by those describing attachment problems in sexual offenders. Therefore, we would argue that it is important to look at this literature as it may advance the notion of treating sex offenders with extensive socioemotional problems as the putative underlying neurobiological problems caused by poor attachment and associated abuse and neglect could act as a block to treatment. It is also possible that such problems could be ameliorated by drug treatment, which then leads to the possibility that current therapy for sexual offenders' problems could be more effective than it is currently. Therefore, the aims of this paper are threefold:
[7] 122w (1) to describe development of attachment in humans and to outline the literature that has described how problematic attachment styles can arise in childhood and how these translate into a style of interpersonal functioning that can lead to problematic sexual relationships and in some cases play causal role in sexually abusive behaviors; (2) to provide a description of the biological basis of attachment and how adverse childhood events such as abuse and neonatal stress can have effects on brain function and brain chemistry; (3) to examine what the impact of drugs that are beginning to be used in sexual offender therapy, specifically, selective serotonin re-uptake inhibitors (SSRIs), and whether these drugs are having an effect in brain neurobiology that underlies social attachment.
[8] 359w Secure attachment is where parenting/caregiving is sensitive and responsive and where the child appears to miss the parent on separation, greets parent on reunion and returns to play. Two types of insecure attachment were also originally identified by Ainsworth et al., these are the following: Avoidant where the style of parenting is rejecting or interfering and where the child shows little distress on separation, actively avoids or ignores parent on reunion; and Ambivalent where the style of parenting is inconsistent and the child is highly distressed by separation, seeks contact on reunion but cannot be settled and clings to or attacks the parent. More recently, a third insecure style has also been described by Crittenden (1985), which is a combination of Avoidant/Ambivalent styles. This style has been found to be associated with parental maltreatment (Carlson, Cicchetti, Barnett, & Braunwald, 1989;Van Ijzendoorn, Schuengel, & Bakermans-Kranenberg, in press) or parents who have experienced an unresolved loss or trauma of their own (Ainsworth & Eichberg, 1991;Main & Hesse, 1990). Hence, it is argued that the parenting style is frightening or frightened so that the child becomes caught in a conflict where their usual source of security has become a source of fear. This style has also been labeled as Disorganized/Disoriented (Main & Hesse, 1990) in that it is thought that children with this attachment style are unable to develop an organized strategy to deal with the opposing tendencies to move towards or away from the parent. Grossman and Grossman (1990) note that this attachment style results in a child who is unfriendly, dependent, moody and low in self-esteem. Kraemer (1992) notes the disruption of an infant's attachment system, whether caused by neglect, abuse or other factors, is likely to be recapitulated when the child becomes an adult. We will now examine how attachment styles, generated in childhood, present themselves over the course of an individual's life span. (2003) suggests that the following adult attachment styles map onto those in childhood as shown in Table 1. A Secure/Autonomous adult attachment style emerges from the secure attachment style in childhood. Their evaluation of attachment-related experiences is found to be consistent, whether favorable or unfavorable.
[9] 48w A Dismissing attachment style found in adults is said to arise from having an avoidant attachment style in childhood. Adults with this view of the world emphasize achievement and self-reliance at the expense of intimacy, that is, there is a denial of attachment and a counterdependence (Feeney, 2003).
[10] 58w A Preoccupied attachment style found in adults is the product of an ambivalent attachment style in childhood. An individual with this style of attachment is described as being preoccupied by past attachment relationship/experiences, are overly dependent upon others and can be ambivalent and preoccupied (Feeney, 2003) in relationships such that they can present as angry, passive or fearful.
[11] 139w An Unresolved/Disorganized attachment style identified in adulthood (Main, Kaplan, & Cassidy, 1985) emerges from a disorganized attachment style in childhood. In a review of studies linking attachment classification to psychopathology, Dozier, Stovall, and Albus (1999) concluded that dunresolved status is the most over represented state of mind among persons with psychiatric disordersT (p. 515). It has been found that there are particular similarities between the likely consequences of attachment disorganization described above and the diagnosis of Borderline Personality Disorder (BPD) in DSM-IV-TR (American Psychiatric Association, 2000). BPD is characterized by an unstable sense of self, intense and unstable interpersonal relations (especially a fear of abandonment), emotional volatility, impulsivity and dissociation. BPD is also associated with a history of abuse (Herman, Perry, & Van der Kolk, 1989). We will now examine how these adult attachment styles operate in romantic situations.
RESULTS
[1] 130w Evidence that use of SSRIs, such as Prozac (Fluoxetine Hydrochloride), Luvox (Fluvoxamine Maleate), Seroxat (Paroxetine Hydrochloride) and Zoloft (Sertraline Hydrochloride) may be useful in the treatment of sexual offending has been accumulating over the last few years. SSRIs are so termed to contrast them with agents which inhibit the re-uptake of 5HT as part of a much more widespread effect on neurotransmitters. Serotonin-active drugs have been found to be useful in the treatment of major depression, anxiety disorders, pain disorders and premature ejaculation (Adi et al., 2002). Research has also investigated the effects that SSRIs have upon social attachment behaviors. For example, young human adults treated with the SSRI Paroxetine were found to show increased social affiliation primarily by reducing indices of hostility and negative effect (Knutson et al., 1998).
[2] 243w The number of reasonable studies that has demonstrated reductions in sexual offending behavior through SSRI treatment are thin on the ground because, although Kafka (2003) notes that there are now over 200 examples of the positive uses of SSRIs for the treatment of paraphilias (deviant sexual urges) or paraphilic disorders, most of those reported are single case studies (Adi et al., 2002). Adi et al. (2002) carried out a systematic review (Cochrane, 2001) looking for evidence in good outcome studies. In this study, there were a number of rigorous inclusion/exclusion criteria in identifying outcome studies that included any SSRIs currently available. 3 Studies comprising individual case reports were excluded from the analysis. Outcome measures considered from the studies included were reported rate of recidivism, level of aggressiveness, reduction in sex drive, penile measure of male erection in response to fantasies or photographic and video stimuli using the penile plethysmograph. Studies that had any directly/ indirectly related sexual behavior outcomes were also considered in the review. From their review, Adi et al. found that only nine studies could be considered of reasonable quality, and none had been conducted using a randomized control trial methodology. Outcomes were universally psychometric measures whose change was generally examined in the short term. It should be noted that no attempt was made to directly assess the impact of SSRIs on recidivism in any of the studies. The studies that Adi et al. reported on are shown in Table 2.
[3] 115w It can be seen from Table 2 that the areas where improvements were found were the following: decreases in deviant fantasies (Bradford, 1995;Greenberg, Bradford, Curry, & O'Rourke, 1996;Perilstein, Lipper, & Friedman, 1991), reductions in unconventional/abnormal/paraphilic sexual behaviors (Fedoroff, 1995;Kafka, 1994;Kafka & Hennen, 2000;Kafka & Prentky, 1992) and reductions in obsessions/compulsions regarding aberrant sexual behavior (Coleman, Gratzer, Nesvacil, 3 Excluding those compound drugs that inhibit both the re-uptake of serotonin and noradrenaline. & Raymond, 2000;Stein et al., 2002). Therefore, the real benefits of this approach appear to be the decrease in the motivation/compulsion to engage in deviant fantasies/behaviors (Kafka, 2003), and, in some cases, it would appear without any decrease in nonparaphilic behaviors, although adverse effects
CONCL
[1] 164w This paper has attempted to bring two strands of work together, attachment theory and brain neurobiology, to understand the putative socioemotional problems that a number of sexual offenders may have. We have examined the literature on the neurobiology of social attachment, where a number of investigations have been carried out looking at the effects of brain biochemistry on levels of social attachment often using animal analogs. Here, we have been particularly interested in the evidence of what happens to the brain if neglect and abuse has occurred as these are striking features in the histories of many sexual offenders who report poorly attached relationships with their parents. Such events can cause very real changes to brain function and brain biochemistry. Next, as the use of SSRIs have been reported to be useful in the reductions of problematic thoughts, feelings and behaviors in sexual offenders, we have examined what effects SSRIs have upon brain neurobiology, particularly, functions that have been disrupted by abuse and neglect.
[2] 171w Evidence suggests that child sex offenders report high levels of emotional loneliness/fear of intimacy/ isolation than nonoffenders, this pattern is most pronounced in preferential fixated offenders who report high levels of emotional isolation and low mood (Bumby & Hansen, 1997;Fisher, Beech, & Browne, 1999;Garlick, Marshall, & Thornton, 1996); SSRIs have been found to successfully target such problems (i.e., Kuzel, 1999). Kafka (2003) notes that the ability of SSRIs to diminish sexual appetitive behavior can be potentially dtherapeuticT for those individuals with dsexual appetitive disinhibition or hypersexuality.T It should also be noted that level of impulsive problems (which have been implicated in sexual offending, i.e., Prentky, Knight, Lee, & Cerce, 1995) has been found to be reduced by the administration of SSRIs (Kafka, 2001) to sexual offenders with such problems. Therefore, it could be argued that raising synaptic 5HT levels by the administration of SSRIs will have a range of beneficial effects upon the brain in the sex offender in that 5HT mediates effects upon social behaviors by a variety of mechanisms.
[3] 189w We would also note that chronic administration of SSRIs, in common with other classes of antidepressant drugs, and electrocompulsive treatment has also been found to increase the levels of brain-derived neurotrophic factor (BDNF) (Duman, Heninger, & Nestler, 1997;Duman, Malberg, & Thome, 1999;Nibuya, Morinobus, & Duman, 1995). BDNF confers neuroprotective actions on specific populations of neurons. These include hippocampal, striatal and mesencephalic dopaminergic neurons (Hyman et al., 1991;Righi, Tongiorgi, & Cattaneo, 2000;Ventimiglia, Mather, Jones, & Lindsay, 1995). BDNF also increases the levels of neurogenesis which is known to continue in the dentate gyrus and subventricular zone of adults, including humans (D'Sa & Duman 2002;Hellsten et al., 2000;Jacobs, van Praag, & Gage, 2000;Malberg, Eisch, Nestler, & Duman, 2000;Scott et al., 2000), this results in an increased neuronal plasticity and consequently an increased capacity for behavior to be modified. Furthermore, raised 5HT levels could act to increase affiliative behaviors secondary to increasing oxytocin and vasopressin release. We would argue that the potential for SSRIs to induce neuronal plasticity could facilitate the brain being dnudgedT into a more dnormalT state of functioning in sexual offenders, given the number have experienced adverse development difficulties.
[4] 176w Taken together, these findings suggest the possibility of developing novel treatment strategies, especially if SSRI treatment was carried out in conjunction with the type of cognitive-behavioral therapy that has been reported to be effective in the treatment of sexual offenders (Friendship, Mann, & Beech, 2003;Hanson et al., 2002). The employment of SSRIs might also be useful as an adjunct to schemabased interventions that are beginning to be used for sexual offenders, particularly in the U.K. Prison Service (Mann & Beech, 2003). This approach addresses enduring personality characteristics and deficits arising from childhood problems such as abuse, neglect and insecure attachment. By increasing affiliative thoughts and feelings-in effect promoting more prosocial feelings in sexual offenders while at the same time decreasing aggressive thoughts and feelings-may increase the impact of therapy. Such changes may explain the findings reported in Table 2 because if sexual offenders are starting to think/feel more prosocially, then they may be less likely to be motivated or have a desire to entertain/engage in or fantasize about paraphilic sexual behaviors (Ward, Polaschek, & Beech, 2005).
UNMAPPED
[1] 276w This part of the paper describes how attachment relationships are formed. The first section describes the literature that describes how intimate pair (attachment) bonds are formed between infants and their primary carers and describes how problematic attachment styles can arise through inconsistency in primary attachment figures' behaviors. The second section describes how different attachment styles laid down in infancy translate into adult interpersonal functioning. The third section describes how these styles of interpersonal functioning translate into adult intimate/sexual relationships. The fourth section describes the empirical work that has found a relationship between problematic adult intimate/sexual relationships and sexual offending. While the final section describes work that suggests that problematic attachment may in part be an explanatory model of the etiology of sexual offending. (1995) notes the following principles about attachment: (1) the earliest attachments are usually formed by the age of 7 months; (2) nearly all infants become attached; (3) attachments are only formed to a few people in the child's life at that time; (4). These selective attachments appear to be derived from social interactions with primary attachment figures; (5) they lead to specific organizational changes in an infant's behavior and brain function. Studies of young children using dthe strange situationT task, a laboratory-based observation procedure examining the child's responses to two brief separations from and reunions with their primary attachment figures (Ainsworth, Blehar, Waters, & Wall, 1978), indicate that there is more than one way by which a child relates to their primary caregiver which are believed to represent strategies for maintaining proximity to the caregiver with difficult and, in some cases, problematic, parenting styles. The identified attachment styles in children are the following:
[2] 127w Romantic attachment did not become an active area of research until a series of studies reported by Hazan and Shaver (i.e., Hazan & Shaver, 1987). Here, Hazan and Shaver argue that romantic love can be regarded as an attachment process in which romantic love is da biosocial process by which affectional bonds are formed between adult lovers, just as affectional bonds are formed earlier in life between human infants and their parentsT (p. 511). Here, Hazan and Zeifman (2003) note that adult sexual partners at the beginning of a relationship will spend a great deal of time din mutual gazing, cuddling, nuzzling, suckling, and kissing. In the context of face-to-face, skin-to-skin, belly-to-belly contact and the touching of body parts,T which can also be observed in mother-infant relationships.
[3] 76w There is evidence in the biological literature for the continuity of the attachment process in that the chemical basis for the effects of close physical contact may be the same for lovers and mother-infant pairs. Nelson and Panksepp (1998), for example, note that the neural mechanisms, which underlie attachment, are organized into a dsocially directed motivational systemT within the brain. This neural system emerges in infancy and continues to modulate affiliative behaviors throughout the life span.
[4] 396w Hazan and Shaver also note that relationships between appropriate others can be conceptualized by the three attachment styles, originally reported in the infant literature: secure, avoidant and ambivalent. Furthermore, they argue that these styles map onto styles of romantic attachments, as reported by Lee (1973), where secure attachment relates to a combination of what Lee called derosT (passionate love) and dagapeT (selfless love); avoidant attachment (dismissing in adulthood) relates to a style of romantic attachment termed dludusT (game-playing love); and ambivalent attachment (preoccupied in adulthood) relates to dmaniaT (possessive love). Levy and Davis (1988) have reported evidence for this notion, finding that secure attachment was positively related to passionate and selfless love and negatively related to game-playing love; avoidant attachment was positively related to ludus and negatively to eros; while ambivalent attachment was positively related to mania. Ward et al. (1996) have also described how different attachment styles can lead to different ways of interacting in sexual relationships. Here, they note that securely attached individuals have high selfesteem and view others as warm and accepting, such that their interpersonal strategies frequently result in high levels of intimacy in close adult sexual relationships. Those with a dismissing style place a great deal of value on remaining independent and invulnerable to negative feelings and therefore are more likely to be actively hostile in their interpersonal style such that they typically do not engage in close emotional relationships. Feeney, Noller, and Patty (1993) reported that dismissing individuals had more accepting attitudes towards casual sex than other attachment groups, while Brennan and Shaver (1995) found that such individuals are much more likely than secure/autonomous individuals to endorse the idea that sex without love is pleasurable and engage in done-night stands.T Ward et al. note that preoccupied individuals have a sense of personal unworthiness; this, coupled with their positive views of others, leads them to seek the approval of others. Hence, such individuals will be sexually preoccupied to meet their strong needs for security and affection, which is unlikely to lead to a satisfactory sexual relationship. Unresolved/disorganized individuals will seek intimacy in relationships, but fear of rejection means that they will keep partners dat a distance.T According to Ward et al., they are not actively hostile in their interactions with others but may express aggression indirectly. This fear of rejection and avoidance of closeness will lead them to seek impersonal sex.
[5] 29w In the next part of this section, we will examine how some of the evidence, which suggests that problematic attachment styles can translate into a vulnerability to sexually offend.
[6] 163w Although insecure attachment is hypothesized to be a vulnerability factor for criminality in general (Ward et al., 1996), Marshall (1989) was one of the first to suggest that insecure attachment in childhood would lead to difficulties establishing intimate adult relationships and the pursuit of intimacy through inappropriate sexual behavior. Craissati et al. (2002) found that an daffectionless controlT style of parenting was reported as being highly prevalent by sexual offenders. They also report some evidence suggesting that low parental care was associated with subsequent childhood abuse. Physical and sexual abuse are also highly likely to occur when there is home life characterized by poor parental relationships and there is a history of parental aggression, alcohol abuse and criminality (Dhaliwal, Gauzas, Antonowicz, & Ross, 1996;Langevin, Wright, & Handy, 1989;Weeks & Widom, 1998). Smallbone and McCabe (2003) found that sexual offenders who reported an insecure attachment style were found also found to more likely report being sexually abused than those with a secure attachment were.
[7] 260w Extending Marshall's (1989) ideas, Ward et al. (1996) proposed that the three insecure attachment styles would be related to different types of sexual offending. Here, they argued that individuals with a preoccupied style will tend to seek approval from others and sexualize attachment relationships and may therefore engage in sexual contact with children; individuals with a dismissing style will be more likely to demonstrate hostility to others, making them likely to offend violently against adult women; individuals with a fearful/disorganized style would choose to seek intimacy through impersonal sexual encounters. Using the Relationship Scales Questionnaire (Griffin & Bartholomew, 1994), Ward et al. found some indication that attachment insecurity was associated with specific type of sexual offending. Specifically, child abusers were more likely to report having a preoccupied fearful attachment styles compared to rapists, violent offenders and nonviolent offenders. In contrast, rapists were more likely to report a dismissing style than child abusers and nonviolent offenders. However, there was no difference in level of dismissing style of attachment in rapists and violent nonsexual offenders, while Van Ijzendoorn et al. (in press) report high rates of unresolved and dcannot classifyT responses in a forensic psychiatric population of men convicted of a range of violent and sexual offending in comparison to a nonclinical sample. Similarly, Fonagy et al. (1996) compared the attachment styles of those who had committed violent crimes (i.e., rapes and murders) with those who had committed nonviolent crimes (i.e., property offenses). Here, they found that the more serious offenders reported more disturbed attachment often accompanied by a history of abuse.
[8] 86w Therefore, some evidence has been found for the hypothesis of a poor attachment history being an important developmental variable associated with subsequent abuse. However, it would be fair to say that this is only one aspect related to subsequent offending, with the strongest evidence currently relating to child abusers being more likely to have a preoccupied attachment style, whereas a dismissing or disorganized attachment style may predispose individuals to serious sexual or violent offending in later life perhaps dependent upon other factors such as environmental triggers.
[9] 571w Marshall and Barbaree (1990) proposed that the sexual abuse of children occurs as a consequence of a number of interacting distal and proximal factors. Specifically, Marshall and Barbaree's theory suggests that individuals experiencing developmentally adverse events (i.e., poor parenting, inconsistent/harsh discipline and physical and sexual abuse) are much more likely to exhibit distorted internal working models of relationships, particularly-with respect to sex and aggression-resulting in poor social and self-regulation skills from an early age. Kraemer (1992), in his description of the psychobiology of attachment, notes that socially deprived individuals may fail to acquire the critical aspects of social cognition as they develop. Here, he notes that dsocial cognitionT is described in the literature as, among other things, the awareness of nature of one's relations with others and an awareness of the emotions and motivations of others. For such individuals, the transition into adolescence is a particularly critical period. It is at this stage that individuals are most receptive to acquiring life-long sexual scripts, preferences, interests and attitudes. Furthermore, the massive increase of sex hormones during this period increases the salience and potency of these sexual cues. If an individual comes from an adverse background and therefore is already predisposed to behaving in an antisocial manner, the pubertal release of hormones may serve to fuse sex and aggression and to consolidate or enhance already acquired sexually abusive tendencies. Marshall and Marshall (2000) specifically suggest that the origin of sexual offending behavior lies in the poor quality of attachment the perpetrator has had in his childhood with his primary caregivers. This may be due to a number of reasons, including sexual, emotional, physical abuse, rejection, lack of support, emotional coldness, disruptive experiences and so forth. Such poor attachment with primary caregivers leaves the individual more open to suffer sexual abuse from others as children due to lack of care, vulnerability and emotional need. Marshall and Marshall proposed that such lack the selfconfidence to initiate relationships with appropriate others. High levels of masturbation in adolescence, coupled with this lack of self-confidence, may lead these individuals to engage in sexual fantasies that incorporate elements of power and control. These fantasies may become more deviant over time. Such fantasies and low levels of social competence lead to a ddisposition to offend,T and such a disposition may be acted upon if the right circumstances to offend occur coupled with ddisinhibiting factorsT such stress and alcohol. Ward and Siegert (2002) suggest that a low level of interpersonal functioning underpinned by insecure attachment and subsequent problems establishing satisfactory relationships with adults (Ward et al., 1996) is one of five primary pathways to sexually offend against children. Hence, the attachment problems underlying this risk domain must be seen as an enduring set of interpersonal difficulties (Beech & Ward, 2004;Ward & Beech, 2004). According to Ward and Siegert, attachment difficulties are causal for the type of offender whose primary problem is a low level of interpersonal functioning in that there will be substitution of children for adult sexual partners, which will be accompanied by distorted thoughts and beliefs concerning the rights or entitlement of the offender to have sex with whom he pleases. This will result in sexual arousal in the context of a sexual encounter with a child and possibly perceived intimate and dlovingT emotions on the part of the offender accompanied by an attempt often to create an adult-like relationship with the child, in effect confusing sex with intimacy.
[10] 26w We will now examine what is currently known about the neurobiology of attachment and what happens to brain function and neurochemistry when adverse childhood experiences occur.
[11] 187w In the biological literature, there is a general assumption that a mechanism underlying attachment is common to all of the following: infant to mother, mother to infant, female adult to male adult and male adult to female adult, and that social attachment is viewed as biologically adaptive (Simpson, 2003). Nelson and Panksepp (1998) note that the neural mechanisms which emerge in infancy continue to modulate affiliative behaviors throughout the life span. Therefore, dysfunction of the attachment system will potentially result in problems in both early development and adulthood. The behaviors associated with attachment appear to be encoded in a region-specific manner in discrete areas of the midbrain. These systems are principally controlled by elements of limbic system. As Kraemer (1992) notes, dsensorimotor systems are also habit and memory systems their functional status and lability are regulated, in part, by biogenic amine systems.T Therefore, developing neurobiological systems probably underlie attachment systems, with the associated constraints on development imposed by such development in the developing brain. Kraemer notes that the intertwined development of neural and social functions can sometimes go wrong when the quality of infant-caregiver bonds are poor.
[12] 114w We will now examine the biological basis of infant-mother, infant-father and romantic attachment in more detail where we note the importance of the role of peptides, oxytocin and vasopressin, which are strongly implicated in the brain mechanisms which underlie the formation and expression of attachment (see reviews by Carter, 1998;Young, 2002). We then describe how adverse childhood experiences can directly have effects upon these mechanisms as well as how the stress caused by such abuse histories can have its effects upon neurobiology. Then, we examine the effect that serotonin has upon attachment behaviors. The final part of this section briefly describes what is currently known about the relationship between serotonin level and sexual functioning.
[13] 189w Various limbic structures have been implicated as forming critical parts of the biological substrates underlying mother-infant attachment behaviors. For example, scanning studies of mothers listening to young infants crying have revealed activation in the cingulated gyrus, hypothalamus and lateral septum as well as parts of the prefrontal cortex and thalamus (Lorberbaum et al., 2002). Oxytocin acting on limbic structures may underlie certain aspects of attachment formation and associated behaviors. The density of oxytocin receptors rises rapidly around the time of birth in limbic structures, which are associated with maternal behavior. 1 In keeping with this, oxytocin release, both hormonally and centrally, increases around birth and the subsequent nursing period in various animal species (Keverne & Kendrick, 1994). Manipulations of oxytocin levels can have dramatic effects upon maternal behavior in animal experiments. For example, peripheral injections of oxytocin decreases female infanticide and increases maternal behavior in virgin wild house mice (McCarthy, Bare, & Vom Saal, 1986). Similarly, centrally released oxytocin at the time of birth, in both female rats and sheep, results in the suppression of avoidance of infants and the emergence of nurturing behavior (Young, Wang, & Insel, 1998).
[14] 99w Centrally acting oxytocin can affect other behaviors associated with attachment, including anxiolytic and antinocioceptive (antinoxious) effects. For example, massage-like stroking leads to long-term antinocioceptive effects due to activation of oxytocin system (Lund et al., 2002), while oxytocin release during lactation may induce calmness and a tendency to social interaction (Holst, Uvnas-Moberg, & Petersson, 2002;Uvnas-Moberg, 1998;Uvnas-Moberg, Johansson, Lupoli, & Svennersten-Sjaunja, 2001). In humans vaginal birth and breast-feeding, which are both associated with increased oxytocin release, are correlated with behavioral changes, including good attachment formation between infant and mother (Nissen, Gustavsson, Widstrom, & Uvnas-Moberg, 1998;Sjogren, Widstrom, Edman, & Uvnas-Moberg, 2000;Uvnas-Moberg, 1998).
[15] 239w Infant-mother attachment has been extensively studied in rodents, where distress in the neonates of some species can be quantified in by the emission of ultrasonic vocalizations (Winslow et al., 2000). Separation from the mother leads to a generalized pattern of distress in young rats, which is characterized by increased vocalizations, increased activity and increased cardiac output. If prolonged or repeated, this separation results in decreased oxytocin activity and decreases the secretion of growth-related enzymes and heightened responsiveness of the hypothalamic-pituitary-adrenal axis, the latter effect leading to abnormal corticosteroid reactivity (Henry & Wang, 1998). Oxytocin is critically involved in mediating this type of attachment in both rats and voles.foot_0 Oxytocin also acts on olfactory neural structures in rodent neonates so as to enable odor preferences for the neonate's mother (Kendrick et al., 1997;Nelson & Panksepp, 1996). Administration of oxytocin antagonists blocks the acquisition of a maternally associated odor preference in young rat pups due to prevention of morphological changes in the olfactory bulb (Dluzen, Muraoka, Engelmann, & Landgraf, 1998). The release of endogenous opiates in neonatal rodents is also involved in the formation of odor preferences. Place preferences can be formed by the action of similar neurobiological mechanisms (Liberzon, Trujillo, Akil, & Young, 1997). Oxytocin can also elicit analgesic effects. Some of these effects appear to be opiate-independent and involve interruption of ascending nocioceptive information at the level of the dorsal horn of the spinal cord (Robinson et al., 2002).
[16] 98w Analgesia in neonatal rodents is also associated with social behaviors such as milk transfer and bodily contact with the mother (Nelson & Panksepp, 1998). Thus, milk infusion induces a dramatic behavioral activation in rat pups followed by reduced activity, analgesia and calmness. These effects may reflect the actions of endogenous opiates as well as oxytocin. Breast-feeding in human infants may also affect social behaviors in that it has been postulated that oxytocin may pass from mother to the human infant when breast-feeding. In this model, oxytocin would then act centrally to facilitate the formation of attachment (Carter, 1998).
[17] 262w The level of central oxytocin activity reflects in part the level of social activity. Thus, social isolation of neonatal rats leads to a reduction in oxytocin receptor binding (Nelson & Panksepp, 1998). Similarly, higher levels of oxytocin activity are seen in social species of vole, such as the prairie vole compared with solitary living species such as the montane vole (Insel, 1992). In keeping with these observations, centrally administered oxytocin results in a decrease ultrasonic vocalizations following isolation (Ferguson, Aldag, Insel, & Young, 2001;Insel & Winslow, 1991). Similar effects can be elicited with vasopressin (Ferguson, Young, & Insel, 2002;Winslow & Insel, 1993). Transgenic studies of mice with oxytocin genes removed have demonstrated that infantmother-separation-induced ultrasonic vocalizations are oxytocin-dependent (Ferguson et al., 2000;Winslow et al., 2000). Oxytocin appears to play a critical role in social recognition memory, a critical component of attachment behavior. Thus, oxytocin acting on the olfactory bulb in sheep leads to formation of olfactory memory for their own offspring during 2-to a 4-hour bonding window after birth and consequent preference for their own offspring (Kendrick et al., 1997;Levy, Kendrick, Goode, Guevaraguzman, & Keverne, 1995). Similar effects have been reported in rats (Engelmann, Ebner, Wotjak, & Landgraf, 1998). Vasopressin and noradrenalin and are also implicated in the process of social recognition memory as normal social recognition responses in male rats are blocked by oxytocin and vasopressin antagonists and noradrenergic depletions of the olfactory bulb (Dluzen, Muraoka, & Landgraf, 1998). Such depression in olfactory bulb noradrenalin content can result in cannibalism of rat pups (Calamandrei, Wilkinson, & Keverne, 1992;Dickinson & Keverne, 1988).
[18] 114w The literature contains relatively few references to the neurobiological basis of paternal-infant behavior. However, oxytocin and vasopressin are again implicated in this type of attachment behavior. Mating in prairie voles results in increases in vasopressin levels (Wang, Liu, Young, & Insel, 2000). Similarly, central infusion of vasopressin elicits paternal behaviors (Parker & Lee, 2001). Studies in the Californian mouse have shown that oxytocin levels in males rise soon after copulation. They remain elevated until some days after birth when they fall and remain low during lactation (Gubernick, Winslow, Jensen, Jeanotte, & Bowen, 1995). This may underlie some paternal behaviors, although the changes in oxytocin levels do not correlate with infanticidal behaviors (Gubernick et al.).
[19] 251w The development of adult-adult pair bonds is the least studied form of attachment from a neurobiological perspective probably because there is an absence of pair bonds in commonly used laboratory animals such as rats and mice (Insel & Winslow, 2004). There are strong species differences in strength and longevity of attachments formed between adults of opposite sexes following mating. Such differences can be readily seen in voles where there are striking differences between the aforementioned prairie and montane voles. The male prairie vole is a mouse-size rodent that lives across the American Midwest, partners for life and becomes highly aggressive after mating with respect to female and male intruders but not to the partner. This postmating aggression is not shown by the closely related polygamous montane voles, which share many features of nonsocial behaviors of the prairie vole but none of the latter's social behaviors. Therefore, this behavior is assumed to reflect a mate guarding strategy (Insel & Winslow, 1998). Such increases in aggressive behavior reflect the actions of oxytocin and vasopressin in conjunction with sex steroids. The two peptides are very similar in their chemical structure, with both being made up of nine amino acids, which control their production. Fisher, Aron, Mashek, Li, and Brown (2002) notes that the adult male/female attachment system is associated with these neuropeptides, while the sex drive (libido, lust) is associated with the estrogens and androgens, and the attraction system (infatuation) is associated with elevated levels of dopamine, norephinephrine and decreased levels of central serotonin.
[20] 267w Oxytocin and vasopressin are best understood by their actions as hormones. In this context, they are released by large neurons in specific parts of the hypothalamus (the supraoptic and paraventricular nuclei). They are transported to the posterior pituitary where they are released into the blood stream. The principle actions of oxytocin include the triggering of muscular contractions during birth and the release of milk during lactation. Vasopressin acts in periphery to increase blood pressure and exerts effects on cardiovascular function. It also acts on the kidney to conserve water and can accordingly be referred to as antidiuretic hormone. In addition to acting as hormones, oxytocin and vasopressin can act as neurotransmitters within the brain. They are accordingly referred to as neuropeptides. When acting in this manner, neurons with small cell bodies (parvocellular), located mainly within the hypothalamus and amygdala, release the neuropeptides into a variety of brain structures. These target structures lie mainly within the limbic system, parts of the olfactory system and brain areas associated with controlling the autonomic nervous system. These brain areas accordingly contain relatively high densities of oxytocin and vasopressin receptors (Ostrowski, 1998). Only one type of oxytocin receptor has so far been identified. However, three subtypes of vasopressin receptor have been defined. The V2 subtype is found exclusively in the kidney, the V1b in the pituitary and the V1a in the cardiovascular system and the brain (Carter, 1998). The release of the neuropeptides into the brain can occur both independently and coordinated with their release into the periphery. We will examine both the roles of oxytocin and vasopressin in romantic attachment behaviors.
[21] 153w The differential level of postmating aggression seen in the different species of voles is reflected in the distribution and densities of oxytocin receptors. The social living monogamous prairie vole has higher densities of oxytocin receptors than the solitary living polygamous montane vole (Insel & Shapiro, 1992;Young et al., 1998). The greater densities of these oxytocin receptors are particularly prominent in the prelimbic cortex, the nucleus accumbens and medial parts of the amygdaloid complex (Young, 2002;Young et al., 1998) and therefore may provide important information about the neurobiology of pair bonding (Insel & Winslow, 2004). The nucleus accumbens is strongly implicated in the neural mechanisms that underpin the reward systems in the brain, while the medial amygdala is involved in social recognition. Taken together, these observations lead to the prediction that, when female prairie voles mate, oxytocin is released, which activates the reward pathway, which conditions the female to the odor of her mate.
[22] 215w Several lines of evidence from animal work support these postulate roles for oxytocin and dopamine in the formation of attachments following mating. Oxytocin can facilitate partner preference formation in prairie voles (Lim, Murphy, & Young, 2004). For example, oxytocin infused in a female prairie vole results in preference for any male, which was present at the time of administration (Liu & Wang, 2003). Oxytocin acting in the amygdala is essential for the formation of social memory as the injection of oxytocin antagonists into this brain area blocks the formation of this specific form of memory (Ferguson et al., 2001;Winslow & Insel, 2002). Similarly, transgenic mice which overexpress oxytocin behave as if strange mice are familiar (Winslow & Insel, 2002;Young, 2002). Furthermore, oxytocin is strongly implicated with copulation itself. Vaginal stimulation results in the release of the peptide both from the pituitary and centrally, while both males and females show large surges in oxytocin at sexual climax (Blaicher et al., 1999;Caldwell, 2002). In rats, oxytocin infusion causes penile erection in male and lordosis (anterior curvature of the spine) in female rats (Albers & Bamshad, 1998;Benelli et al., 1994). Finally, the formation of partner preference is facilitated by D-2 dopamine agonists induced and attenuated by D-2 antagonists (Aragona, Liu, Curtis, Stephan, & Wang, 2003;Liu & Wang, 2003).
[23] 67w There is some evidence that the chemical basis for the effects of close physical contact may be the same for lovers and mother-infant human pairs. Oxytocin is released during suckling/nursing interactions and thought to induce infant attachment and maternal caregiving, and it is also released at sexual climax in humans and has been implicated in the dafterplayT (cuddling) that often follows sexual intercourse (Blaicher et al., 1999).
[24] 96w Vasopressin appears to play a strong role in males in both partner preference and postmating aggression. Vasopressin receptors are found in key limbic structures, the densities of which are testosterone-dependent. The specific anatomical distribution and densities of vasopressin receptors in voles reflect the mating habits of the species. Thus, the polygamous montane vole shows high densities of vasopressin in the lateral septum, accessory olfactory bulb and superior colliculus, whereas the monogamous prairie vole shows additionally high densities in the olfactory bulb, diagonal band, laterodorsal thalamus and ventral pallidum (Insel, Wang, & Ferris, 1994;Pitkow et al., 2001).
[25] 173w In some species, especially those that form longstanding postmating bonds, increased levels of aggression are seen in both sexes postcopulation (Carter, 1998). This may reflect the action of vasopressin on receptors in the ventrolateral hypothalamus, the presence of which is testosteronedependent (Delville, Mansour, & Ferris, 1996;Harrison et al., 2000), as is the synthesis of vasopressin itself (DeVries & Villalba, 1997). Chronic infusion of vasopressin elicits mate guarding in males prairie voles (Young et al., 1998). In contrast, infusion of a vasopressin antagonist prior to mating prevents the postcopulation-associated aggression (Insel & Winslow, 1998). These effects of vasopressin on aggression are mainly limited to monogamous species. For example, infusion of vasopressin in the polygamous montane vole results in increase self-grooming not increased aggression (Young et al., 1998). These effects of vasopressin on aggression can be influenced by neonatal exposure to the peptide. Thus, exposure of neonates to raised levels of vasopressin results in increased aggressive behavior and mate guarding when the animals reach adulthood through the formation of social attachments (Stribley & Carter, 1999).
[26] 153w The ventral pallidum is intimately connected with the mesolimbic dopamine system and is accordingly thought to play important roles in reward (Berridge, 1996). Activation of this system may underlie conditioning-like learning which leads to the formation of partner bonds (Pitkow et al., 2001). The role of vasopressin receptors in the formation of partner preferences has been demonstrated by prevention of postcopulation pair bonds in prairie voles following infusion of vasopressin antagonist (Winslow & Insel, 1993). Conversely, increasing vasopressin levels in the ventral pallidium by means of gene transfer techniques results in the formation of strong partner preferences in male prairie voles following overnight cohabitation with female without mating (Pitkow et al., 2001). The precise role that vasopressin plays in the formation of partner preferences is still to be determined, although it appears that the peptide plays an important role in the consolidation rather than the acquisition of social memory (Ferguson et al., 2000).
[27] 245w Adverse childhood experiences due to early interactions between primary carers and children are highly significant for later life, especially such adverse events as abuse history that produce biochemical changes in the limbic areas of the brain that modulate attachment behaviors as we have previously argued that the most salient biogenic amine system correlates of attachment are the oxytocin and vasopressin systems. However, the endogenous opioids, norepinephrine and dopamine have also been implicated (Carter, 1998). Treatment of neonatal animals with corticosteroids has been found to produce abnormal social behaviors in adulthood (Catalani et al., 2000). Corticosteroids can affect adult social bonds and reproductive behaviors potentially via an action upon oxytocin function. The corticosteroid system can also interact with the oxytocin and vasopressin systems (Griebel et al., 2002;Legross, 2001). Therefore, neonatal stress can result in long-term changes in the sensitivity of the oxytocin system (Carter, 1998), which has been found to play a significant role in the maintenance of both mother-child and romantic attachments. As noted earlier, high levels of licking and grooming by the mother of infant rats correlate with high levels of oxytocin receptor binding in adulthood and increased maternal care to their own offspring. Similarly, high levels of maternal licking and grooming of male pups results in increased vasopressin binding, especially in the amygdala (Francis, Young, Meaney, & Insel, 2002). Therefore, it could be argued that both adult to child and romantic relationships can be severely affected by a lack of a dlovingT upbringing.
[28] 240w The common biological mechanism that appears to underlie parent-offspring and adult-adult attachments, combined with the potential for permanent changes in the function of the attachment system, means that childhood events have an important influence upon adult (romantic) attachment behaviors and raises the potential for the propagation of socioemotional problems. As Bowlby (1982) noted that the disruption of the infant's attachment system, whether caused by neglect, abuse or other factors, is likely to be recapitulated when the child becomes a parent. Therefore, a mother who fails to form secure attachments with her offspring may be suffering from an oxytocin-related problem (Henry & Wang, 1998). Specifically, in animal analogs, the failure to form secure attachments in rats is responsible for reduced levels of licking and grooming by the mother of her offspring. Levels of this type of grooming behavior are correlated with the levels of oxytocin and vasopressin receptor binding in the pups (Champagne, Francis, Mar, & Meaney, 2003;Francis et al., 2002). Such changes in peptide function have been found to persist into adulthood, thereby leading to problems of a second generation of problematic attachment behavior (Champagne et al., 2003;Francis et al., 2002). In humans, this may lead to reduced oxytocin release in sexual climax in humans, which may be experienced as a mechanical unloving experience and may go someway to explaining why some individuals with insecure attachment styles (e.g., dismissive and disorganized individuals) regard sex without love as a pleasurable experience.
[29] 133w Biochemical changes due to adverse childhood experiences may also include corticosteroid-induced neuronal damage. These atrophic effects have been attributed to the neurotoxic actions of corticosteroids, which can result in dendritic atrophy of hippocampal neurons. Prolonged chronic stress, such as that induced by abuse as a child (or by prolonged military combat), is also associated with hippocampal atrophy (Sapolsky, 1997). Animal studies have demonstrated that administration of the synthetic corticosteroid, dexamethasone, has been shown to result in damage to both the hippocampus and the striatum, with the dorsomedial part being particularly vulnerable (Hassan, von Rosenstiel, Patchev, Holsboer, & Almeida, 1996;Haynes, Griffiths, Hyde, Barber, & Mitchell, 2001;Mitchell, Cooper, Griffiths, & Barber, 1998). These results suggest that the potential for stress to exert fairly direct affects upon the areas of the brain that modulate attachment behaviors.
[30] 268w Insecure parent-infant attachments would be expected to be stressful for the offspring particularly if the parent is regarded as frightening or fearful, as has been found in parents of children who have been found to have attachment disorganization. Kraemer (1992) notes that such deficits in social cognition cause the infant/juvenile to fail to solve social problems when demanded. He further notes that the individual as it matures will continue to be exposed to such duncontrollable, unavoidable and inescapable stressors.T It is important therefore to examine how stress affects the developing brain, of particular interest are measures of changes in the levels of corticosteroids as the release of these hormones rises following exposure to stressors. Corticosteroid responses have been used as an index of separation distress in animals (Carter, 1998). Rearing rats in isolation results in a marked behavioral syndrome (Heidbreder et al., 2000). This syndrome is characterized by locomotor hyperactivity (both spontaneous and conditioned) enhanced responses to novel environments, greater tendencies towards perseveration, deficits in prepulse inhibition and altered responses to opiate and dopaminergic drugs (Heidbreder et al., 2000). Comparisons between the effects of rats, which have experienced separation-induced stress and posttraumatic shock disorder, have also been made. Both are characterized by high levels of sympathetic output along with increased locus coeruleus activity, which may result in increased vigilance, tendency to dysphoria and disturbed sleep patterns (Henry & Wang, 1998). Prolonged and severe stress can result in dysfunctional control of corticosteroid release, whereby the steroid is no longer released in response to acute stressors. This blunted stress response may correlate with disrupted attachment behavior (Henry & Wang, 1998).
[31] 176w Lyons-Ruth and Jacobvitz (2003) note that blunted cortisol responses to stress may be another outcome of particularly deviant early attachment experiences. Kraemer and Clarke (1996) found that, compared to mother-reared monkeys, rhesus monkeys randomly assigned to a dpeer rearingT condition showed subsequent blunting of physiological responses to stress while still showing behavioral signs of disturbance. Acute social deprivation in animals induced by separation of offspring from the mother has been regarded as modeling some aspects of problematic attachment (Hall, 1998). Animals treated in this manner show elevated basal levels of corticosteroids as well as hypersecretion in response to stressors such as novel environments (Bartolomucci et al., 2003;Hall, 1998). Corticosteroid release is held in check by higher brain centers acting upon the hypothalamus, the principal one being a serotinergic pathway from the hippocampus (McEwen, 1999;Meijer & de Kloet, 1998). Stress in rodents induced by prolonged social isolation is accompanied by reductions in serotonin [5-hydroxytryptamine (5HT)] (Dalley, Theobald, Pereira, Li, & Robbins, 2002;Muchimapura, Mason, & Marsden, 2003). This reduction in serotonergic function may contribute to raised corticosteroid release.
[32] 180w Male adult prairie voles develop preferences for females that they have been exposed to during stress (Carter, Devries, & Getz, 1995;DeVries, DeVries, Taymans, & Carter, 1996). In contrast, stress in adult females interferes with the development of social preferences and the formation of partner preferences. Hertsgaard, Gunnar, Erickson, and Hachmias (1995) and Spangler and Grossman (1993) found that children classified as attachment disorganized were found to have significantly higher levels of salivatory cortisol compared to securely attached individuals when in response to a brief separation from primary caregivers, while Nachmias et al. (1996), using a similar paradigm, found that children with higher behavioral inhibition had higher posttest cortisol levels if they were classed as insecure. Carlson and Earls (1997) found that normal diurnal variation in cortisol secretion was altered among Romanian orphans. Carlson and Earls (1997) also found that the degree of cortisol elevation was related to decrements in infant development scales on a number of measures. According to Fox and Card (2003), the results of these and other studies illustrate that secure attachment acts as a buffer against stress.
[33] 124w There is evidence to show that highly traumatic childhood experiences can result in corticosteroid abnormalities, which persist into adulthood. For example, women with a history of childhood sexual and/or physical abuse exhibit increased pituitary-adrenal and autonomic activity in response to stress compared with controls (Heim et al., 2000). This abnormal corticosteroid response, which is accompanied by autonomic hyperactivity, probably reflects hypersecretion of corticosteroid releasing factor. This implies that corticosteroid releasing factor antagonists may have a role played in the treatment of psychopathological conditions related to traumatic childhood experiences (Heim et al., 2000). Treatment of neonatal animals with corticosteroids can likewise result in abnormal social behaviors in adulthood. Thus, the normally monogamous prairie vole shows increased preference for unfamiliar partners following postnatal treatment with corticosteroids.
[34] 114w The mechanisms by which childhood stressors can lead to long-term changes in behavior may include corticosteroid-induced neuronal damage. Prolonged chronic stress, such as that induced by abuse as a child or by prolonged military combat, is associated with hippocampal atrophy (Bremner et al., 1995(Bremner et al., , 1997;;Sapolsky, 1997). These atrophic effects have been attributed to the neurotoxic actions of corticosteroids resulting in dendritic atrophy of hippocampal neurons (McEwen, de Leon, Lupien, & Meaney, 1999;Sousa & Almeida, 2002). Similarly, the synthetic corticosteroid, dexamethasone, has been shown to result in damage to both the hippocampus and the striatum, with the dorsomedial part being particularly vulnerable (Hassan et al., 1996;Haynes et al., 2001;Mitchell et al., 1998).
[35] 119w The neuropeptide oxytocin and vasopressin systems can interact with the corticosteroid system (Griebel et al., 2002;Legross, 2001). These results suggest the potential for stress to exert fairly direct effects upon the mechanisms that underlie attachment. For example, neonatal stress can result in longterm changes in the sensitivity of the oxytocin system (Carter, 1998). Separation from the mother leads to a generalized pattern of distress in young rats, which is characterized by ultrasonic vocalizations, increased activity and increased cardiac output. If prolonged or repeated, this separation results in decreased oxytocin activity and decreases in the secretion of growth-related enzymes and heightened responsiveness of the hypothalamic-pituitary-adrenal axis, the latter resulting in abnormal corticosteroid reactivity (Henry & Wang, 1998;Nelson & Panksepp, 1998).
[36] 29w In the next part of this section, we will briefly examine the effect of 5HT upon brain function and behavior, in particular its relationship with oxytocin, vasopressin and corticosteroids.
[37] 495w In the human brain, 5HT-containing neurons are found mainly in the dorsal raphe nucleus of the brain stem. From this nucleus, the cells send out axons that end in serotonin-containing terminals innervating the diverse areas throughout the brain. These regions include the brainstem, the cerebellum, the hypothalamus, basal ganglia, hippocampus and associated limbic structures and the neocortex (Adi et al., 2002). 5HT levels mediate effects upon social behaviors by a variety of mechanisms. Levels of oxytocin and vasopressin are clearly dependent upon the level of 5HT (Insel & Winslow, 1998), while levels of corticosteroids have been found to be inversely correlated with 5HT (Chaouloff, 2000;Porter, McAllister-Wiliams, Lunn, & Young, 1998;Zhong & Ciaranello, 1995). However, there are indications in the animal literature suggesting that attachment behaviors depend upon 5HT levels. For example, it has been found that social grooming is 5HT-dependent (Insel & Winslow, 1998), while the administration of Paroxetine and amperozide (a 5HT2A receptor antagonist) increase social cohesiveness in male rats (Rademacher, Anderson, & Steinpreis, 2002). Furthermore, primate dominance hierarchies are based on 5HT, and the administration of 5HT agonists leads to dominance in the animal, given the agonists in unstable hierarchies. However, this is achieved by increased affiliative interactions, i.e., grooming rather than by aggressive behaviors (Raleigh, McGuire, Brammer, Pollack, & Yuwiler, 1991). Pearson (1990) and Kafka and Coleman (1991) were probably the first to suggest that problems in 5HT transmission underlie paraphilic/compulsive disorder, while more recently, Kafka (1997Kafka ( , 2003) ) makes a number of arguments to suggest that problems in 5HT function underlie deviant sexual behavior. Although each of the arguments on their own cannot be considered to be that strong, taken together, these would seem to suggest that these ideas should be examined more closely in that Kafka argues that (1) in animal work, there is evidence that decreased levels of 5HT may disinhibit or increase sexual appetitive behavior, while increased central 5HT activity may inhibit or reduce sexual appetitive behavior (Lorrain, Riolo, Matuszewich, & Hull, 1999); (2) pedophilia may be associated with a dysregulation of particular 5HT receptors in that some evidence has been found related to decreased activity of the serotonergic presynaptic neuron and an up-regulation of the postsynaptic 5-HT2A/2C receptors in this group (Maes et al., 2001); (3) there is some evidence that there is comorbidity of some psychiatric Axis I disorders, such as mood disorders, anxiety disorders, psychoactive substance abuse, conduct disorder and attention deficit hyperactivity and sexual offending; (3) there is some evidence that that there is a relationship between 5HT dysregulation and the specific dimensions of psychopathology (antisocial impulsivity, anxiety, depression and hypersexuality), these perhaps underpinning specific paraphilic disorders; (4) the treatment for Axis 1 disorders, typically by altering monoamine function, involving psychostimulants, neuroleptics or antidepressant medication would appear to have substantial effects upon human sexual functioning, including a reduction in sexual appetite, such effects typically being regarded as the dside effectsT of these types of medication (i.e., Montejo, Llorca, Izqierdo, & Rico-Villadermos, 2001).
[38] 244w Another argument has been made about the similarities between sexual offending and compulsive/ addictive behaviors. As noted in Sections 3.4. and 3.5, poor attachment in early childhood and consequent increased exposure to stressors result in reduced 5HT levels, oxytocin and vasopressin function and raised corticosteroid release, which can result in hippocampal and striatal damage. These complex neurobiological changes may lead the individual to be vulnerable to problematic compulsive/ addictive behaviors as an In support of this link, there are reports of raise CSF oxytocin levels in patients with obsessive-compulsive disorder (OCD), which correlate with symptom severity (Leckman et al., 1994). The relationship between oxytocin abnormalities and OCD is supported by observations of Prader-Willi syndrome. Patients with this genetic disorder have elevated levels of oxytocin and show OCD symptoms as well as mental retardation and appetite deregulation (Martin et al., 1998). OCD is thought to result from dysfunction of the striatum and its associated connections with prefrontal cortex (Rauch et al., 1997;Rauch & Savage, 1997;Rosenberg & Keshavan, 1997), and the dorsomedial striatum of the rat contains high densities of oxytocin receptors (Ostrowski, 1998). These observations have led to attempts to alleviate the symptoms of OCD by the intranasal administration of oxytocin-like drugs, although the results have been equivocal (Denboer & Westernberg, 1992;Epperson, McDougle, & Price, 1996). Similarities between OCD behaviors-where SSRIs are often the treatment of choice to alter the level of 5HT-and the behaviors of sex offenders have also been suggested (e.g., Bradford, 1999).
[39] 246w The idea of an obsessive-compulsive element to sexual offending has been elaborated by McConaghy (1993) in his behavior completion model. In this model, he notes that sexual offenders experience great difficulty when attempting to cease their deviant behaviors, which suggested to McConaghy that, in addition to sexual arousal, the general arousal systems of the brain are also involved. He notes that, when a behavior is regularly carried out, this activates a particular part of the brain representing that particular behavior. If this behavior is not completed, this causes the neural representation to stimulate the arousal system, leading the individual to experience increased tension and excitement. These feelings, according to McConaghy, drive an individual to complete such behaviors. He also notes that such behaviors have an evolutionary advantage in that they motivate individuals to complete behaviors that would normally be rewarding. However, in sexual offending, this does not confer any evolutionary advantage but may be one explanation for the compulsive nature of behaviors, which, for some sexual offenders, overrides their inhibitions to further offending. McConaghy notes the high level of sexual dysfunction from those who commit exhibitionist offenses to reports of those who commit very serious contact sexual offenses. From this theory, McConaghy, Blaszczynski, and Kidson (1988) carried out a trial using chemical treatment comparing imaginal desensitization and/or medroxyprogesterone (to reduce offenders' testosterone levels). However, McConaghy et al. reported no difference on outcome between the different treatment modalities in the reduction of anomalous sexual urges and behavior.
[40] 121w Therefore, the argument is that the neuropeptide oxytocin, as well as being involved in attachmentrelated behaviors, is implicated in addictive behaviors, which can have obsessive-compulsive components. The peptide has been implicated in the modulation of dopaminergic transmission in the limbic forebrain, which is strongly implicated in addiction (Kovacs, Sarnyai, & Szabo, 1998;Sarnyai & Kovacs, 1994). Oxytocin also acts centrally to limit the development of tolerance to both heroin and alcohol (Kovacs et al., 1998). Equally, alcohol can have effects upon oxytocin release. For example, alcohol inhibits suckling-induced oxytocin release in rats (Subramanian, 1999). Furthermore, chronic exposure to alcohol can lead to a direct neurotoxic action on vasopressin and oxytocin neurons (Madeira, Sousa, Lieberman, & Paulabarbosa, 1993;Silva, Madeira, Ruela, & Paula-Barbosa, 2002).
[41] 73w As noted earlier, levels of oxytocin and vasopressin have been found to be dependent upon the level of 5HT (Insel & Winslow 1998), while levels of corticosteroids have been found to be inversely correlated with 5HT (Chaouloff, 2000;Porter et al., 1998;Zhong & Ciaranello, 1995). Therefore, the final part of this paper examines drug treatment to target problematic behaviors in sexual offenders, with special reference to the use of SSRIs to mediate 5HT function.