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MATERNAL & EARLY ENVIRONMENTAL INFLUENCES ON

EMOTIONAL, SEXUAL, AND NEUROLOGICAL DEVELOPMENT Part IV
by Rhawn Joseph, Ph.D.

NORMAL & ABNORMAL AMYGDALA DEVELOPMENT,
By Rhawn Joseph, Ph.D.

Reprinted from Neuropsychiatry, Neuropsychology,
Clinical Neuroscience, 3rd Edition
(University Press),

By Rhawn Joseph, Ph.D.

NORMAL & ABNORMAL AMYGDALA DEVELOPMENT

The amygdala although first fashioned during the first two months of fetal development, remains exceedingly immature for the first several years after birth, and thus highly vulnerable to stress-induced neuroplastic changes, including those experienced during adulthood (Joseph, 1998b, 1999b,d). Developmentally, however, this structure does not begin to demonstrate "experience-expectancies" until around the second month of post natal development.

However, as different regions within the amygdala (and other forebrain structures) also begin to develop at different rates, some amygdala capabilities appear in advance of other, including, for example, the ability to attend to the human face. Hence, due to the maturation of a few precocious feature detecting neurons which selectively respond to facial and auditory-emotional stimuli the newborn displays a tendency to attend to and seems to prefer facelike to nonfacial stimuli (Carpenter, 1974; Goren, Sarty, & Wu, 1975). In consequence, for the next several critical months, the amygdala requires considerable exposure to facial stimuli. If the infant is reared in a maternally neglectful environment, with a mother than does not make face-to-face and eye-to-eye contact, these experience-expectant neurons will atrophy and die thus profoundly affecting the development of appropriate social behaviors including memory for faces (e.g., Jacobson, 1986; Tranel & Hyman, 1990).

Specifically, beginning around 8 weeks, and as the medial amygdala begins to mature (Langworthy, 1937; Yakovlev & Lecours, 1967), the infant becomes exceedingly socially oriented, and will coo, goo, phonate, and babble in response to smiling faces, and will selectively search out and focus on the eyes of their caretaker (Sroufe, 1996). These emerging social behaviors can be directly attributed to the amygdala as well as the overlying (partly contiguous) temporal lobe. Both structures contains neurons which selectively respond to smiles, to the eyes, and which differentiate between male and female faces and the emotions they convey (Hasselmo, Rolls, & Baylis, 1989; Morris, Frith, Perett, Rowland, Young, Calder, & Colan, 1996; Rolls, 1984).

For example, the left amygdala can determine the direction in which someone else is looking, whereas the right amygdala becomes activated when making eye to eye contact (Kawashima et al., 1999). Moreover, the normal human amygdala typically responds to frightened faces by altering its activity and in fact increasing its activity as the facial expression changes from a smile to fear (Morris et al., 1996). In response to facial and eye-to-eye contact, the amygdala can trigger, via the corpus striatum (basal ganglia) and brainstem, eye-to-eye contact and a variety of facial expressions including the smile or the face of fear (e.g., Chen & Forster, 1973; Offen, Davidoff, Troost, & Richey, 1976; Sethi & Rao, 1976).

Hence, around 2-months of age, as the amygdala and its facial-detecting neurons begin to develop, the infant increasingly stares into the eyes of others, and begins to recognize and will orient toward familiar faces (e.g. Sroufe, 1996). By 6-months it can discriminate between male and female faces, and by 9 months can easily discriminate between different facial expressions (e.g. Caron, Caron & Myers, 1985; Carpenter, 1974; Spitz & Wolf, 1946)--functions associated with the amygdala.

Moreover, these facial-detecting-neurons are richly interconnected with yet other amygdala-temporal lobe neurons concerned with auditory perception and social emotional functioning, including those which can trigger a smiling, laughing, and even a crying and sobbing response (Chen & Forster, 1973; Offen et al., 1976; Sethi & Rao, 1976). Hence, emotiona and face-to-face and eye-to-eye activation of the amygdala can also trigger smiling and social behavior.

Thus the early maturation of certain specialized amygdala-temporal lobe neurons which are selectively sensitive to human faces is an exceedingly adaptive development as it promotes social emotional face-to-face, vocal interaction, and the formation of emotional attachments. Again, however, if the infant is raised in an environment where the mother or primary caretaker fails to provide sufficient face-to-face stimulation, these neurons will fail to develop normally thus profoundly affecting all aspects of social affective behavior. Consider, for example, some of the classic signs of autism. The autistic child refuses to make eye-to-eye contact--and limbic system abnormalities have been associated with deprivation induced-autistic behavior in primates (Heath, 1972). This is not to imply that insufficient mothering is the cause of human autism, (though in some cases that may be true), but rather that insufficient mothering can damage the limbic system and produce autistic behaviors (see below).

INDIVIDUAL DIFFERENCES IN SOCIAL-CONTACT SEEKING

As detailed in chapters 13 and 25, the limbic system is sexually differentiated, including the amygdala, which in turn is reflected by sex differences in social inclinations. Some infants are less interested in making eye-to-eye and face-to-face contact, particularly boys as compared to girls. Indeed, baby boys show as much interest in a bulls eye as they do the human face, whereas little girls not only prefer looking at faces but begin to do so at an earlier age (Lewis et al., 1968). Likewise, whereas there are mother who love to hold, touch, stare at, play and vocalize with infants, including those infants who are not all that responsive to this stimulation, there are also mothers who are indifferent or only inconsistently provide this type of contact--which may be the residue of their own insufficient mothering and face-to-face contact when they were infants. If these latter mother-types are paired with an infant that is also not very responsive to face-to-face stimulation, these women will be even less inclined to provide this type of input which in turn results in insufficient stimulation and neural death or atrophy. In consequence, these children will develop a range of subtle to profound social emotional disturbances. As demonstrated in human (Lilly et al., 1983; Marlowe, Mancall, Thomas, 1975; Terzian & Ore, 1955) and non-human subjects (Kling, 1972; Kling & Brothers 1992; Kraemer, 1992), injury to or destruction of the normal amygdala will abolish almost all aspects of social-emotional behavior, for normally this is the most socially and emotionally responsive structure of the entire brain (see chapter 13).

AMYGDALA SOCIAL-EMOTIONAL MATURATION

As the amygdala matures over the course of the first 8 months of development, the infant becomes increasingly social, may gaze into the eyes and smile at anyone, and will vocalize and seek to make contact even with complete strangers (Bronson, 1974; Charlesworth and Kruetzer, 1973; Schaffer, 1966; Spitz & Wolf, 1946; Waters, Matas, & Stroufe, 1975). Likewise, infants less than 6-months of age will readily accept mother substitutes.

However, by 8-12 months, as the amygdala, cingulate and other forebrain nuclei reach advanced stages of maturation (Benes, 1994; Joseph, 1992, 1999b; Yakovlev & Lecours, 1967), infants increasingly become upset at the prospect of maternal separation (Ainsworth et al., 1978; Bowlby 1969, 1982; Schaffer, 1966; Spitz, 1946). They also begin to experience and vocalize fear and separation anxiety (Bronson, 1972; Emde, Gaensbauer, & Harmon, 1976; Sroufe & Waters, 1976). Fear, of course, is associated with the amygdala (Davis et al., 1997; Gloor, 1992; Halgren, 1992; Rosen & Schulkin, 1998), whereas activation of the anterior cingulate can produce infantile behavior, anxiety, and a separation cry (Devinksy, Morrell, & Vogt,1995; Jurgens, 1990; MacLean, 1990).

By nine months, 70% of children may respond aversively if a stranger approaches, whereas by 10 months they might cry out (Bronson 1974; Schaffer, 1966; Waters et al., 1975). By 1 year 90% of children may respond aversively to strangers (Schaffer, 1966). Instead, they increasingly bond to their mothers and are more likely to restrict their smiling and socializing to familiar faces and specific members of their family (Sroufe, 1996).

In this regard, the immature amygdala initially promotes indiscriminate socializing as it in fact requires this stimulation in order to develop normally,. Later, the maturing amygdala, in conjunction with the cingulate, septal nuclei and other forebrain structures, acts to promote the formation of specific and intense attachments. This is accomplished at first through expressions of joy and eye-to-eye facial contact which reinforces maternal behavior, and later via the generation of fear and separation anxiety which promotes close maternal contact and the formation of specific and enduring attachments (Joseph, 1992a, 1999b). In this regard the slow and differential rate of amygdala, cingulate, and septal maturation (see below) is exceedingly adaptive, such that emotions which restrict social tendencies appear only after the infant has received considerable social and emotional stimulation, and has already formed a generalized attachment to the primary caretaker. Again, however, if these neurons are not provided sufficient social, emotional and face-to-face stimulation during early development, they may lose the capacity to respond to these social signals such that all aspects of social, emotional, and even sexual behavior become exceedingly abnormal.

AMYGDALA DESTRUCTION AND AMYGDALA DEPRIVATION

Because limbic nuclei and subdivisions within these nuclei mature at different rates and differentially contribute to the experience and expression of emotion, they are also differently affected depending on if or when they are deprived of normal experience. For example, humans and non-human primates who are neglected and deprived of sufficient social and emotional contact during the first six months of postnatal development exhibit symptoms which are basically identical to those following bilateral amygdala destruction.

For example, monkeys deprived for the first three months of development become severely self abusive, withdrawn, and bizarre, and will withdraw and scream if touched or approached (Harlow & Harlow, 1965a,b). Those deprived for 6 months become severely autistic, and any desire for social contact is completely extinguished (Harlow & Harlow, 1965a,b). Similarly, human infants placed in foundling homes soon after birth and who are reared under deprived conditions for 6-months or more, become extremely bizarre, autistic, withdrawn, mute, self-stimulating and self-abusive, and will withdraw or respond with "blood curdling screams" if approached (Goldfarb, 1943, 1945, 1946; Koluchova,1976; Spitz 1945, 1946).

Likewise, if the amygdala is destroyed, emotional functioning becomes exceedingly abnormal, and social behavior is essentially abolished. Among humans (Lilly et al., 1983; Marlowe et al., 1975; Ramamurthi, 1988; Scott, Young, Calder, Hellawell, Aggleton, & Johnson, 1997; Terzian & Ore, 1955) and non-human primates and mammals (Kling, 1972; Kling & Brothers 1992; Kluver & Bucy, 1939), bilateral injuries or destruction of the amygdala significantly disturbs the ability to determine, discern, or identify the motivational and emotional significance of externally or internally occurring events, to accurately perceive social-emotional nuances conveyed by others through gesture, voice, or facial expression, or to select what behavior is appropriate given a specific social context. Animals or humans with bilateral amygdaloid destruction become pathologically shy, respond in an emotionally blunted manner, and seem unable to discern the social, emotional or motivational characteristics of what they see, feel, hear, and experience.

Even with mild injuries they may be unable to determine if others are behaving in a friendly or unfriendly fashion are are unable to feel liked or experience affection. Like those who are not necessarily neglected but who receive insufficient mothering and social stimulation, with mild amygdala injuries the individual may become shy and feel awkward and uncomfortable when around others.

Since the human amygdala (and the forebrain) remains relatively immature for the first two months of postnatal development (Yakovlev & Lecours, 1967), likewise, emotional and social neglect experienced and limited to this early age, is not as destructive as compared to those neglected later in life (Langmeier & Matejcek, 1975). Likewise, amygdala injury during the first several months does not appear to be as disruptive as damage experienced later--a function of neuroplasticity and the ability of other brain tissues to acquire displayed functions and associated (and still intact) neural pathways (see below).

However, when the amygdala is injured later in life, the resulting social-emotional agnosia will even abolishes any emotional feeling for loved ones (Lilly et al., 1983; Marlowe et al., 1975) including, in one case, the patient's mother with whom he had been exceedingly close (Terzian & Ore, 1955). As described by Terzian and Ore (1955) the patient became extremely socially unresponsive, preferred to sit in isolation, well away from others, and demonstrated extreme and indiscriminate orality.

Among primates who have undergone bilateral amygdala removal, a dense social-emotional blindness becomes readily apparent. In several studies it was found that once these amygdalectomized primates were released to their social group, they were unable to comprehend emotional or social nuances and had little or no interest in social activity and persistently attempted to avoid contact with others (Kling, 1972; Kling & Brothers 1992; Jonason & Enloe, 1972). If approached they would withdraw. If followed they would flee. Among adults with bilateral amygdala lesions, total isolation was preferred.

Even maternal behavior is severely affected. According to Kling (1972), amygdalectomized mothers would bite off fingers or toes, break arms or legs, and behaved as if their "infant were a strange object to be mouthed, bitten and tossed around as though it were a rubber ball".

The behavior of mothers with bilateral amygdala destruction is in fact almost identical to the "maternal" behavior of mothers who had been raised in isolation. As described by Harlow and Harlow (1965, pp. 256-257, 259): "After the birth of her baby, the first of these unmothered mothers ignored the infant and sat relatively motionless at one side of the cage, staring fixedly into space hour after hour. As the infant matured desperate attempts to effect maternal contact were consistently repulsed... Other motherless monkeys were indifferent to their babies or brutalized them, biting off their fingers or toes, pounding them, and nearly killing them until caretakers intervened. Despite the consistent punishment, the babies persisted in their attempts to make maternal contact."

As noted, infants reared under deprived conditions also exhibit behavior which is also identical to that of adult animals who have suffered bilateral amygdala destruction. This includes not only social withdrawal and self-abusive behavior, but a tendency to seek out painful and dangerous external stimuli (Langmeier & Matejcek, 1975), such as repeatedly touching and mouthing a burning flame (Kluver & Bucy, 1939; Melzack & Scott, 1957). These deprived behaviors are identical to those following amygdala destruction and/or amygdala-straital abnormalities, as early emotional deprivation damages the immature amygdala as well as the amygdala-striatum--structures involved in the motoric expression of affective behavior.

THE AMYGALA-STRIATUM AND ABNORMAL AFFECTIVE-MOTOR STEREOTYPIES

Infants who experience even short term deprivation may begin to develop perseverative and self-abuse motor stereotypies where they pinch the same piece of skin until it bleeds, repeatedly bang their head, or simply and repeatedly produce the same movements of their legs, arms, hands or fingers.

These abnormalities appear to be a direct consequence of the effects of deprivation on the development of the amygdala as well as the striatum and associated structures such as the subthalamic nucleus, which are intimately interconnected. As detailed in chapters 12, 16, the amygdala forms the bulbous tail of the corpus striatum (caudate, putamen), whereas the limbic striatum (nucleus accumbens, substantia innominata, olfactory tubercle) is considered part of the "extended amygdala." If activated by the amygdala, the striatum and subthalamus may induce smiling, frowning, as well as trigger a variety of stereotyped, perseverative, and ballistic motor actions such as running, kicking, flailing, and punching, or conversely "freezing" in reaction to extreme fear.

Like the amygdala, the striatum begins to myelinate and metabolism begins to increase around the 2nd to 3rd postnatal month (Chugani, 1994; Yakovlev & LeCours, 1967), the age at which infants display "true emotions" and true smiles. However, the striatum does not approximate adult levels of myelination until 2-4 years and does not complete this developmental cycle until 8 years of age (Yakovlev & Lecours, 1967). As the striatum matures brainstem reflexes are replaced or hierarchically subsumed by more purposeful and goal directed behaviors such as rolling from prone to supine and back again (Capute et al., 1984; McGraw, 1969) as well as rocking and kicking (Piaget, 1952; Thelen, 1982), and the infant engages in a wider range of perseverative rhythmical motor stereotypies ("secondary circular reactions," Piaget, 1952), such as bouncing, swaying, kicking, waving, and banging (Thelen, 1982). As based on parallels and correlations with striatal (and medial forebrain) development (see below), it appears these stereotypies are an indication of increasing, albeit immature striatal (as well frontal) influences over brainstem motor functioning (for related discussion see Chugani, 1994; Gibson, 1991), as the striatum and subthalamus are directly implicated in the production of rhythmic, perseverative, ballistic, and stereotyped behaviors involving the legs, arms, hands, face and head (Crossman et al., 1987; MacLean, 1990; Rauch, Jenike, & Alpert, 1994).

Specifically, rhythmical stereotypies tend to emerge around 10-12 weeks of age, and then peak in intensity and frequency between 26-42 weeks of age (Thelen, 1982), thus paralleling striatal maturation (see also Chugani, 1994). As the striatum (and medial and motor frontal areas) reach advanced levels of maturation around one year of age, likewise, these motor stereotypies begin to rapidly decrease in frequency, particularly those stereotypies which are triggered by kinesthetic stimulation or when the infant is in a non-alert state (Thelen, 1982).

The production of these perseverative stereotypies, therefore, are indications of striatal immaturity. However, because of striatal (and amygdala) immaturity, lack of sufficient stimulation can injure this portion of the brain, even slowing the rate of myelination, which in turn can increase the frequency of perseverative stereotyped movements. Conversely, just as myelination is an indication of functional efficiency, and just as increased (versus restricted or abnormal) stimulation in early infancy can increase the rate of myelination (Langworthy, 1937), infants who receive considerable stimulation display a reduced frequency of rhythmical stereotypies (Thelen, 1982).

In consequence, if the infant is severely deprived of social emotional and physical stimulation, the frequency of rhythmical stereotypies may become exaggerated to the point where they become self-abusive (Bowlby, 1982; Harlow & Harlow, 1965a,b; Langmeier, & Matejcek, 1975; Spitz, 1945, 1946). Unmothered infants may spend hours engaged in obsessive, repetitive, stereotyped and bizarre self-stimulating movements; i.e. rocking, head banging, or pinching precisely the same piece of skin until sores develop--behaviors which appear to be a direct consequence of environmental damage inflicted on the immature and experience-expectant striatum and amygdala.

Again, however, it must be emphasized that the degree of any subsequent abnormality depends on the nature, degree, and extent of the maternal deprivation or abuse the infant is subjected to.

NEGLECT, STRESS, THE AMYGDALA, & NEUROCHEMICAL LESIONS

Deprivation and neglect is exceedingly stressful (Bowlby, 1960, 1982; Pankseep, Normansell, & Herman, 1988; Kraemer, 1992; Rosenblum, Coplan, & Friedman, 1994; Rots, et al., 1995; Suchecki, et al., 1993; Spitz, 1945, 1946). Even temporary periods of isolation or maternal separation may trigger significant fluctuations in neurotransmitters such as norepinephrine (NE), serotonin (5HT) and dopamine (DA), and promote the secretion of enkephalins and corticosteroids (Kehoe, Clash, Skipsey, & Shoemaker, 1996; Kraemer 1992; Pankseep et al., 1988; Rosenblum et al., 1994).

For example, normally NE is exceedingly important in maximizing neural growth and neuroplasticity (Kasamatsu & Pettigrew 1976; Pettigrew & Kasamatsu 1978), not only during the early stages of development (Johnston 1988; Parnavelas et al. 1988), but following traumatic experiences and brain injuries sustained as an adult. For example, immediately following a brain injury, NE secretion is rapidly increased which acts to promote plasticity, synaptic development, and thus functional recovery. If deprived of NE, functional recovery is retarded (see Parnavelas et al. 1988).

In the developing nervous system, NE also acts to suppress the establishment of irrelevant neural networks and pathways, while simultaneously stabilizing and/or promoting the growth and formation of relevant synaptic circuits (see Bear & Singer 1986; Pettigrew & Kasamatsu 1978). Similarly, NE has been shown to inhibit or suppress irrelevant background activity, while simultaneously enhancing evoked responses in both inhibitory and excitatory circuits associated with the processing of relevant environmental input (Foote et al. 1983).

The NE neurotransmitter system is also directly implicated in modulating the stress response, and in fact stress increases NE turnover in the amygdala (Tanaka, Kohno, Nakagawa, et al. 1982), a structure which is also directly implicated in modulating the stress response, becoming highly active under conditions of emotional and physical stress (Henke, 1992; Ray, Henke, & Sullivan, 1987; Roozendall, Koolhaas and Bohus, 1992). In fact, the release of NE serves a neural protective function within the amygdala (Glavin, 1985; Ray et al., 1987b), preventing damage to this structure, or the development of abnormal kindling activity under conditions of stress and high arousal.

However, under conditions of repetitive stress, NE levels may be depleted and opiates may be secreted which also exert an inhibitory effects on the release of NE (Izquierdo & Graundenz 1980). Unfortunately, NE depletion, excessive amygdala activation, and opiate release, can lead to permanent structural and functional alterations within infant and adult amygdala neurons, effecting their neocortical interconnections, postsynaptic densities and in the size of the presynaptic terminals as well as their capacity to process and transmit information (e.g. Cain 1992; Racine 1978). With repeated instances of activation or heightened activity, an abnormal form of neuronal platicity and a lowered threshold of responding also results. These changes are associated with increases in the size of the evoked potential amplitudes and can give rise to epilptiform after discharges, seizures and convulsions, as well as induce kindling (subseizure activity) within the amygdala (Cain 1992; Racine 1978).

Unfortunately, adverse early environmental influences can induce significant alterations and even exaggerations of the NE response (Rosenblum et al. 1994), followed by reductions in NE, even when the trauma is mild and/or involves varying degrees of neglect (Higley et al. 1992), or even following brief periods of maternal separation (Kraemer et al. 1989). Indeed, among its many diverse functions, NE appears to be directly involved in the experience of separation anxiety from the mother (Pankseep et al. 1988).

For example, it has been shown that if a primate mother is periodically prevented from responding or attending to her infant, the infant will suffer significant reductions in NE activity (Kraemer et al. 1989). Moreover, these infants in turn become less securely attached, more easily frightened and startled, are less social or independent and display significant NE-related abnormalities. According to Rosenblum et al. (1994) infants reared under these mildly stressful conditions display responses similar to those seen in humans suffering from post traumatic stress disorder.

Presumably, these stress related disturbances involving the NE (and 5HT) systems, particularly when experienced during infancy, abnormally influences neuronal and synaptic development thereby producing a functional lesion as well as abnormal neural circuitry. Given that the limbic system (e.g. amygdala) is also effected by stress, emotional trauma, as well as alterations in NE and 5HT, abnormalities in the development of associated limbic system circuitry may also be adversely impacted, such that they display abnormal neuroplasticity and excessive activity including kindling. Moreover, heightened activity within the immature amygdala or septal nuclei, may also induce the growth of additional dendrites which in turn act to attract axons from alternate sites (e.g. Raisman 1969). In consequence, abnormal neural networks and pathways may be formed between nuclei that "normally" do not directly interact. Conditions such as these could predispose the individual to behaving or reacting abnormally and to processing and even storing information in an abnormal fashion.

As noted, under stressful conditions not only the amygdala and septal nucleus, but the hypothalamus and hippocampus may be injured (see chapter 30). However, if these structures including the hippocampus become abnormal, not just the ability to perceive and express emotion or to feel securely attached, but the capacity to remember those who are emotionally significant may be disrupted (Gloor, 1997; Kling & Brothers, 1992; Lilly, Cummings, Benson, & Frankel, 1983; Terzian & Ore, 1955). In fact, stress induced injury to the amygdala and hippocampus can produce an amnesia so profound that personal identity, and memory for friends and loved ones may be erased (chapter 30).

Consider, for example, those individuals who have undergone the surgical resection of the (presumably normal) amygdala and hippocampus. They not only become emotionally placid and unresponsive, but lose the ability to establish new and long term personal relationships (Aggleton, 1992). As demonstrated in the famous case of H.M. who underwent the surgical removal of the right and left amygdala and hippocampus (Milner, 1970), although Brenda Milner has worked with him for over 25 years she is an utter stranger to him. Likewise, injuries localized to the amygdala can result in an inability to recognize faces (Jacobson, 1986; Tranel & Hyman, 1990) or maintain emotional attachments (e.g. Terzian & Ore, 1955), whereas bilateral hippocampal ablation results in an inability to establish new emotional attachment or relationships.

EMOTIONAL STRESS, SEXUAL ABUSE & ABNORMAL AMYGDALA DEVELOPMENT

The amygdala is implicated not only in the mediation of almost all aspects of emotion and affective motor behavior, but sexuality (Davis et al., 1997; Gloor, 1992, Halgren, 1992, Kling and Brothers, 1992; LeDoux, 1996; Rosen and Schulkin, 1998). In fact, the primate amygdala is sexually differentiated such that there are male and female pattern of amygdala neural organization which in turn is determined by the presence or absence of steroidal hormones early in development (Nishizuka and Arai, 1981, 1983).

The amygdala and hypothalamus are intimately interconnected, and as noted, electrical stimulation of the sexually dimorphic hypothalamus will induce sexual posturing including clitoral swelling, penile erection, and pelvic thrusting coupled with an explosive discharge of semen (Lisk, 1967, 1971; MacLean, 1973). Likewise, activation of the amygdala can produce penile erection (Kling and Brothers, 1992; MacLean, 1990; Robinson and Mishkin, 1968; Stoffels et al., 1980) sexual feelings (Bancaud et al., 1970; Remillard et al., 1983), sensations of extreme pleasure (Olds and Forbes, 1981), memories of sexual intercourse (Gloor, 1986), as well as ovulation, uterine contractions, lactogenetic responses, and orgasm (Currier, Little, Suess and Andy, 1971; Freemon and Nevis,1969; Remillard et al., 1983; Shealy and Peel, 1957).

Since the amygdala has the capacity to selectively respond to male vs female faces and the emotions they convey, and as this structure is directly implicated in sexuality, presumably the amygdala can respond to these physical features by inducing sexual arousal. Moreover, in response to direct sexual stimulation, the amygdala, in conjunction with the hypothalamus can induce penile or clitoral erection, pelvic thrusting, ovulation, ejaculation, and thus the entire human sexual response.

Because of their involvement in all aspects of sexuality and the sexual response, complete destruction of the hypothalamus can eliminate sexual behaviors in total (Everitt and Stacey, 1987), whereas damage or destruction of the human and non-human primate amygdala may result in bizarre sexual changes, such as continuous masturbation and indiscriminate, often hypersexual hetero- and homosexual behaviors including attempts at sex with inanimate objects (Kling and Brothers, 1992; Kluver and Bucy, 1939; Pribram and Bagshaw 1953; Terzian and Ore, 1955). Hypersexuality following amygdala injury has been documented among numerous species, including cats and dogs (Kling and Brothers, 1992).

Humans with an abnormally activated or severely injured amygdala may expose their genitals, masturbate in public, and attempt to have sex with family members or individuals of the same sex (Blumer, 1970; Kolarsky, Freund, Macheck, and Polak, 1967; Terzian and Ore, 1955). Moreover, abnormal activity involving the amygdala (and overlying temporal lobe) has been associated with the experience of orgasm (Backman and Rossel, 1984; Warneke, 1976) and the development of hyposexuality (Taylor, 1971; Heirons and Saunders, 1966; Toon, Edem, Nanjee, and Wheeler, 1989), hypersexuality (Blumer, 1970) as well as homosexuality, transvestism, and thus confusion over sexual orientation (Davies and Morgenstern, 1960; Kolarsky et al., 1967). In fact, abnormal- or seizure activity within the amygdala or overlying temporal lobe may induce an individual to engage in "sexual intercourse" even in the absence of a partner.

For example, Currier and colleagues (1971, p. 260) described a female temporal lobe seizure patient who was "sitting at the kitchen table with her daughter making out a shopping list" when she suffered a seizure. "She appeared dazed, slumped to the floor on her back, lifted her skirt, spread her knees and elevated her pelvis rhythmically. She made appropriate vocalizations for sexual intercourse such as: It feels so good...further, further."

As will be detailed below, sexual abuse can also induce the development of sexually abnormal behaviors which are identical to those associated with abnormal amygdala activity and injury. This association is not coincidental, for repeated instances of abuse and other forms of abnormal environmental input can induce amygdala abnormalities, including the development of kindling and seizure activity as well as abnormal neuroplastic where inappropriate and abnormally active synaptic connections are formed.

If the amygdala is injured, becomes excessively active, or develops abnormal kindling or seizure activity, emotionality and sexuality may become abnormal (Kling and Brothers, 1992; Remillard et al., 1983; Terzian and Ore, 1955). For example, patients may demonstrate hypo- or hypersexuality, or develop severe depression, anxiety, fear, or rage reactions--abnormalities and symptoms identical to those exhibited by adults and children who have been severely sexually abused (Courtois, 1995; Beitchman, Zucker, Hood, DACosta, Akman and Cassavia, 1992; Finkelhor, 1988; Harper, 1993; Simons and Whitbeck, 1991).

In fact, not just sexuality, but emotion and personality functioning are significantly altered with amygdala destruction (Lilly, Cummings, Benson and Frankel, 1983; Marlowe, Mancall and Thomas, 1975; Terzian and Ore 1955). Those suffering from abnormal activity involving the amygdala and overlying temporal lobe, may experience severe depression, fear, anxiety, and rage as well as dramatic alterations in personality (Devinsky and Bear, 1984; Egger and Flynn, 1963; Gloor, 1992, 1997; Halgren, 1992; LeDoux, 1996; Mark et al., 1972; Mesulam, 1981; Trimble 1991). They may become severely withdrawn and contemplate or successfully commit suicide. In some cases, these mood swings and personality changes are so dramatic patients appear to be suffering from a multiple personality disorder. In fact, increases in temporal lobe activity and blood flow changes have been documented among patients diagnosed with multiple personality disorder (Drake, 1986; Fichtner, Kuhlman, and Hughes,1990; Mathew, Jack and West, 1985; Mesulam,1981; Schenk and Bear, 1981), which is significant as the medial temporal lobe is not just contiguous with but part of the medial amygdala.

SEXUAL ABNORMALITIES AND SEX ABUSE

It is now well established that children who were severely sexually abused may develop a broad range of emotional, sexual, and cognitive abnormalities (Becker, Skinner, Abel, and Chirchon, 1986; Beitchman et al.,1992; Brown and Finklhor, 1986; Courtois, 1995; Harper, 1993), including, while still children, inappropriate and hypersexualized behavior (Deblinger, McLeer, Atkins, Ralphe and Foa, 1989; Friedrich, Urquiza and Beilke, 1986; Harper, 1993; Kohan, Pothier and Norbeck, 1987; Lusk and Waterman, 1986; Pomeroy, Behar and Stewart, 1981). Children who are sexually abused sometimes become sexually precocious and behave in a sexual manner with friends, school mates, and sometimes adults. They may fequently pull down their pants, or pull up their skirt and expose their genitals as well as play with the genitals of friends or allow them to play with theirs. They may also sexually act out what has happened to them with adults and may in fact solicit sexual abuse. Moreover, although removed from the home and hospitalized or placed in foster care, severely sexually abused children may behave seductively, expose themselves and masturbate with objects, aggressively solicit sex, and become angry or enraged when their sexual advances are thwarted (Kolko, Moser, and Weldy, 1988; Mannarino and Cohen, 1986; Mian, Wehrspann, Klajner-Diamond, Lebaron and Winder, 1986).

Sometimes, however, after being abused children may seek out more abuse. For example, children who are neglected or physically abused, may find sexual interactions with an adult to be a satisfying method of obtaining love and emotional comfort, a sense that someone cares about them (Finkelhor, 1979; Landis, 1956). However, they may also begin to associate love with being abused, or abuse with sexuality and orgasm. As such, they may then act in an abusive manner with others or solicit abuse in order relive the familiar of the long ago, and to obtain the satisfaction they associate with sexual fulfillment and love, and to achieve an orgasm; that is, they seek out those who will abuse them.

Yet others may become exceedingly fearful, withdrawn, anxious, severely depressed, and suicidal as well as hypersexual (Kolko et al., 1988; Livingston, 1987). These and related sexual emotional abnormalities may persist into adulthood.

Women with a history of severe childhood sexual abuse (CSA) may become promiscuous, engage in prostitution, and/or experience confusion over sexual orientation, or complain of hyposexuality, frigidity, and fear of sex and of men (Alexander and Lupfer, 1987; Becker, et al., 1986; Fromuth, 1986; Meiselman, 1978; Simons and Whitbeck, 1991; Stein, Golding, Siegel, Burnam and Sorenson, 1988; Tsai, Feldman-Summers and Edgard, 1979; Wind & Silvern, 1992). Promiscuity, even among those who dislike sex, is not uncommon, and a significant percentage of these women are more sexually active than non-abused females (Alexander and Lupfer, 1987; Fromuth, 1986; Tsai, et al., 1979; Wind and Silvern, 1992). A significant minority also tend to associate with men who will beat or sexually exploit them, and/or they engage in behaviors which increase the risk and which result in a higher incidence of being sexually assaulted and raped (Brown & Finkelhor, 1986; Gorcey et al., 1986; Russell, 1986). It has been found that between 40% to 60% of prostitutes report a childhood history of sex abuse (Silbert & Pines, 1981; see also James & Meyerding, 1977; Miller 1986; Weisberg, 1985).

However, there are also individual differences, and many women with a history of CSA deny any significant sexual pathology, or, as noted, complain of hyposexuality and loss of desire. Moreover, perhaps less than 10% admit to engaging in homosexual activities (Gundlach, 1977; Meiselman, 1978; Runtz & Briere, 1986), whereas bisexual activities among heterosexual women in the general population is rather common (see chapter 8). Moreover, there is no evidence to suggest that a majority of victims engage in prostitution; though a majority of prostitutes may well have been victims. Indeed, sexual as well as emotional disturbances such as excessive and chronic fear, depression, and anxiety, coupled with feelings of isolation, anger, and worthlessness are common (Herman & Schatzow, 1987; Murphy et al., 1988; Stein et al., 1988). Moreover, there is a high incidence of suicide attempts (Briere and Runtz, 1986; Bryer, Nelson, Miller and Krol, 1987), though not all investigators concur with this latter finding (e.g. Peters, 1988).

Likewise, a significant number of males with a history of CSA, report sexual disturbances (Finkelhor, 1979; Johnson & Shrier, 1985; Rogers & Terry, 1984), including hypo or hypersexuality, compulsive masturbation, and difficulty forming sexual relationships or performing adequately with a female sex partner (Duncan & Williams, 1998; Elliott & Briere, 1992; Hunter, 1991). Like their female counterparts, some sexually abused males may also experience confusion over their sexual identity or engage in homosexuality (Johnson and Shrier, 1985; Simari & Baskin, 1984). Finkelhor (1979) reported that males with a history of CSA are four times more likely than non-abused males to engage in homosexual activities. In addition, a significant relationship between CSA and teenage- or adult-onset pedophilia and violent criminal behavior has been reported (Haaspasalo & Kankonon, 1997; Knight & Prentky, 1993; Rubinstein et al., 1993; Watkins and Bentovim, 1992; Widom and Ames, 1994), including violence toward loved ones and intimate partners (Duncan and Williams 1998), including rape. And, as with women, men who were sexually abused suffer significant emotional problems, including depression, fear, anger, and anxiety, and not infrequently experience homicidal, suicidal, and self-destructive feelings (Mendel 1995; Urquiza and Capra, 1990; Watkins and Bentovim, 1992).

It is noteworthy that although men with a history of CSA often become exceedingly homophobic (Urquiza and Capra, 1990), there are also those who view the abuse as "positive" (Bauserman and Rind, 1997; Finkelhor, 1979; Laumann et al. 1994). In these latter instances, those who respond "positively" tend to have been "abused" by women rather than men, whereas some of those abused by men and feel positively about the experience, may well have been homosexual in orientation to begin with (e.g. Johnson and Shrier, 1985). Hence, although a significant number of males tend to be severely traumatized by CSA, others feel neutral or even positive and thus do not appear to be excessively stressed or upset by these experiences (for additional discussion see Bauserman and Rind, 1997). By contrast, the vast majority of females overwhelming tend to feel devastated and many forever have difficulty forming meaningful long-term relationships as they are plagued by feelings of loneliness and rejection even when they are truly loved.

THE SEXUAL SELF-DESTRUCTION OF "NEGLECTED" NORMA JEAN

It must be emphasized that there are varying degrees of sexual abuse and neglect. For example, a child who is beat, suffocated, tortured and repeatedly raped by a sadistic adult who then denies the abuse, and who repeatedly accuses the victim of manufacturing "false memories," will be affected much more severely and profoundly than a child who also repeatedly has sex with adults but who is instead provided with gifts, money, toys, clothes, as well as love and affection (Joseph, 1998b, 1999d). Hence, not only the age at which the child is abused, but the nature and degree of the abuse, coupled with other predisposing factors, all contribute to the resulting symptomology and the degree of damage to the limbic system (see below).

For example, some children may be neglected early in life and then sexually abused later in life which in turn will effect different limbic structures to different degrees. Moreover, and as noted, those who are neglected only to be sexually exploited, may discover that sexuality is a briefly satisfying means of escaping their loneliness and satisfying their cravings for affection. That is, children who are neglected or physically abused, may find sexual interactions with an adult to be a satisfying method of obtaining emotional comfort.

As also noted, injury or abnormalities involving the amygdala are associated with hypersexuality. Hence, children who are sexually abused sometimes become sexually precocious and behave in a sexual manner with friends, school mates, and sometimes adults. If they were also neglected as well as sexually abused, they may also sexually act out what has happened to them with adults and may in fact solicit sexual abuse as they find that sexual interactions with an adult to be a satisfying method of obtaining love, a sense that someone cares about them. Moreover, this inappropriate sexual behavior often continues well into adulthood, even if the victim claims that they do not obtain pleasure from sex. As noted above, they may become prostitutes, or seek anonymous sex from strangers of members of their own gender. And, if the sexual abuse was coupled with neglect, the victim may seek out those who will instill feelings of rejection as well as have sex with them. Indeed, they may feel rejected even by those who love them, and may be unable to obtain satisfaction from sex.

Hence, even when truly loved they may feel alone or rejected and neglected, such that they feel compelled to repeatedly seek a temporary sexual antidote to their depression and sense of isolation. Again, however, these feelings and behaviors, although "learned" are also neurologically based, for the same structures implicated in sexuality, abuse, and neglect (e.g., the amygdala) are also implicated in feelings of depression and become activated under conditions of isolation and emotional deprivation (see chapters 9, 13).

As an illustrative example, consider the case of Norma Jean. Norma's mother had been married and divorced twice and had several affairs before she was born. She had no idea who Norma's real father might have been.

Norma's childhood was a nightmare of neglect, abandonment, and rejection. Although she had a promiscuous past, Norma's mother was religiously superstitious and was consumed with fears regarding sins, some of which she claimed little Norma harbored in her soul. Norma's grandmother shared these beliefs and tried to smother little Norma to death when she was about 2 years old. Her mother also suffered from violent fits of rage and depression and frankly did not like being a mother. Hence, Norma was not just abused but severely neglected and her mother would often leave her with friends or relatives for days and weeks at a time. Finally, she put her little Norma in a foster home in order to free herself of the burden. After several months she reclaimed her.

This pattern of neglect, abuse, rejection, and abandonment was repeated for over a dozen years, during which Norma was placed in 10 different foster homes, including two years spent in the Los Angeles Orphan's Home. However, she was not just neglected and repeatedly abandoned, but was repeatedly sexually abused and raped and in fact became pregnant when she was 14 years old. Norma was allowed to have the baby and then it was taken away from her soon after birth. She never saw her son again.

When Norma turned 15, her current guardian presented her with the option of being returned to the orphanage (as she was planning on moving out of state) or marrying the son of her neighbor and best friend. Norma chose marriage. After a few years they divorced.

Over the next several years she "worked" as a prostitute even though she did not enjoy sex, but then obtained employment as a model, as she was very beautiful. Nevertheless, she continued her promiscuous ways, had numerous sexual affairs with strangers, maintained simultaneous sexual relations with several older men, but was unable to find the love and affection she craved. Indeed, although numerous men sought her affections, she nevertheless felt alone and rejected and suffered from severe depression and an overwhelming sense of insecurity. Although she claimed did not really enjoy sex, she continued to have numerous sex partners, allegedly repeatedly became pregnant, allegedly had at least12 abortions, was in and out of psychiatric treatment, married and divorced several very prominent and not so prominent men, made repeated suicide attempts, and abused alcohol and drugs. Surprisingly, she managed to forged a briefly promising and very successful career, but as her fame grew so did her depression, her sense of loneliness and feelings of rejections, as well as her frequency of her suicide attempts. She finally committed suicide (or was possibly murdered at the behest of the brothers "K") at the age of 36. They buried her under the name of Marilyn Monroe.

CHILDHOOD SEXUAL ABUSE AND THE AMYGDALA

Although there are exceptions, it is thus well established that CSA can significantly disturb all aspects of social, emotional, sexual, and personality functioning, with some females becoming so traumatized that they repeatedly dissociate and reportedly form multiple personalities (Putnam et al., 1986; Salama, 1980). However, although negative "conditioning," the "learning" of inappropriate behaviors, and "psychological" or unconscious conflicts regarding self-esteem and sexuality certainly contribute to the development of these disturbances, these same exact symptoms, including depression and suicidal ideation and successful suicide attempts, are associated with abnormalities involving the amygdala, and associated forebrain structures such as the hypothalamus, septal nuclei, and hippocampus--brain areas which can be injured by traumatic stress (Joseph, 1998b, 1999d; Lupien and McEwen, 1997; Sapolsky, 1996). In fact, the development of some of these abnormal sex-related behaviors may be due to abnormal stress-related learning occurring within the amygdala--abnormal learning associated with the abnormal neuroplastic changes and the establishment of inappropriate synaptic connnections.

Synaptic development is associated with learning and increased and repetitive instances of arousal and neural activity, coupled with alterations in NE and other neurotransmitters. However, whereas some structures implicated in learning and memory, such as the hippocampus, may cease to function or display synaptic growth under conditions of repetitive and high levels of arousal, especially if the arousal is stress-related (chapter 30), the amygdala is directly implicated in modulating behavioral and physiological changes in reaction to stress and becomes highly active when stressed or physically restrained (Henke, 1992; Ray et al., 1987a). The amygdala also becomes activated and may become potentiated or undergo neurplastic changes if the individual is experiencing fear or perceives frightening stimuli (Chapman, Kairiss, Keenan and Brown, 1990; Clugnet and LeDoux, 1990; Halgren, 1992; Morris et al., 1986). Likewise, the amygdala becomes highly active when experiencing sexual arousal or engaging in sexual behaviors (Kling and Brothers, 1992; Remillard et al., 1983). In consequence, if physically restrained, experiencing fear and engaging in sexuality simultaneously, those amygdaloid pathways which subserve these behaviors and the stress reaction may be abnormally activated and mutually potentiated, such that aberrant neuroplastic alterations are induced and abnormal pathways become established (chapters 2, 30). Victims become afraid when experiencing sex, or associate sex with pain, or become aroused when frightened or injured, and then seek out or engage in dangerous activities, etc; a possible function of abnormal associative learning and the possible establishment of aberrant neural pathways which link sex with fear or pain coupled with stress-induced abnormal amygdala activity.

In summary, just as those with histories of CSA may behave in a hyposexual or hypersexual manner, and display other sexual abnormalities, and just as they may become chronically and severely depressed, fearful, withdrawn, isolated, suicidal, self-destructive, angry, or enraged, identical disturbances are associated with abnormalities of the amygdala including even the development of multiple personality disorder. Again, these commonalities are not merely coincidental, for traumatic stress, including the stress of sexual abuse, can induce limbic system injury and seizure activity, and can promote abnormal stress-related neuroplastic changes and associated synaptic abnormalities particularly within the amygdala. In this regard, it is likely that the sexual abnormalities and long term sexual traumatization associated with severe sexual trauma, may be directly due to stress-related abnormalities induced within the amygdala as well as the hypothalamus.

STRESS, SEX, CORTICOSTEROIDS, AND AMYGDALA, HYPOTHALAMIC INJURY

Corticosteroids and other stress hormones are released as part of the stress and fight or flight response. However, under prolonged or repeated episodes of stress, these substances are released in such massive amounts that they may destroy neural tissue (Joseph, 1998b, 1999d; Lupien and McEwen, 1997; Sapolsky, 1996). Specifically, in response to fear, anger, anxiety, physical restraint, or severe sexual or emotional abuse, the amygdala becomes highly active (e.g. Henke, 1992; Ray et al., 1987a; Roozendall, Koolhaas and Bohus, 1992; Stevens et al., 1969). In addition, the hypothalamus secretes corticotropin releasing factor which activates the andenohypophysis which begins secreting ACTH which stimulates the adrenal cortex which secretes corticosteroids (e.g., Hakan, Eyle, and Henriksen, 1994; Roozendall, et al., 1992). These events, in part, appear to be under the modulating influences of neuropeptides, and aminergic transmitters including NE which also serves a neural protective function (Glavin, 1985; Ray et al., 1987b). That is, since NE can activate the hypothalamic, pituitary, adrenal system (HPA) thus inducing the secretion of corticosteroids, and as these stress hormones can suppress or injure neural tissue (Lupien & McEwen, 1997; Sapolsky, 1996), increases in NE also act to protect these neurons from the damaging effects of these transmitters (Glavin, 1985; Ray et al., 1987b). However, as stress increases or becomes prolonged, NE levels may eventually become depleted (Bliss, Ailion and Zwanziger, 1968; Glavin, 1985) which exposes neurons to the damaging effects of corticosteroids and related stress hormones and renders them susceptible to becoming suppressed, or developing abnormal activity and undergoing aberrant neuroplastic changes (chapters 2, 30).

As noted, if the hypothalamus and the HPA axis are injured, the result may be chronic depression and a host of related emotional abnormalities (see Carrol et al., 1976; Sachar et al. 1973; Swann et al. 1994). This includes a tendency to hyper secrete glucocosteroids and to maintain high levels of cortisol even under neutral conditions--thus continually suppressing or subjecting neural tissue to possible injury and reducing the ability to cope with stress.

However, because the amygdala and hypothalamus are sexually differentiated (Allen et al., 1989; Bleier et al., 1982; Nishizuka and Arai, 1981, 1983; Rainbow et al., 1982; Raisman and Field, 1973; Swaab and Hoffman, 1990) and as the male vs female pattern is dependent upon the presence of circulating steroids, not only might the hypothalamus become inadvertently effected and abnormally differentiated due to the hypersecretion of corticosteroids, but so too may the amygdala and amygdala pathways. As noted, it has been shown that the ventromedial and anterior nuclei of the hypothalamus of male homosexuals demonstrate the female pattern of development (Levay, 1991; Swaab and Hoffman, 1990). Likewise, the anterior commissure (which interconnects the right and left amygdala and inferior temporal lobes) has been found to be significantly larger in homosexuals and females, as compared to heterosexual males (Allen and Gorski 1992); findings, however, which may be due to genetics, or other unknown factors.

Coupled with animal studies which demonstrate that sex specific behaviors and cognitive activities can be enhanced or altered by steroids (Joseph et al., 1978; Reinisch & Sanders, 1992) or suppressed due to early environmental influences, including the stress of deprivation (Joseph, 1979; Joseph and Gallagher, 1980), and given that the sexual differentiation of the hypothalamus may be altered by steroidal manipulations (Raisman and Field, 1973), it can also be assumed that traumatic stress and the massive secretion of steroids, particularly during early sexual development, may alter the neural organization of these same structures. In consequence, sexuality, sexual orientation, as well as emotion, personality, including the ability to cope with stress may be disrupted and become abnormal among those who have been severely or repetitively sexually abused and traumatized.

SEPTAL DESTRUCTION AND SEPTAL DEPRIVATION

The amygdala maintains a mutually influential and counterbalancing relationship with the septal nuclei as both are richly interconnected via the stria terminalis axonal fiber bundle and both interact in regard to the hypothalamus and hippocampus. In general, the amygdala exerts inhibitory and excitatory influences on the septal nuclei, which in turn exerts inhibitory influences on the amygdala and both exert counterbalancing influences on the hypothalamus via the stria terminalis (see chapter 13).

For much of the first postnatal year, septal influences are relatively minimal as this nucleus matures and develops at a much later age than the amygdala (Brown, 1983; Joseph, 1992a, 1999b). In fact, the initial development of the septal nuclei is influenced if not triggered by the extended amygdala, the tuberculum olfactorium (Humphrey, 1967), and later, it is only upon the receipt of, and activation by amygdala afferent fibers that the septal nuclei begins to differentiate (Brown, 1983). Moreover, the myelination of the septal nuclei is "extraordinarily protracted" (Yakovlev & Lecours, 1967). Indeed the septal nuclei and septal pathways do not display a significant degree of myelination until around 4-months of age and takes well over 3 years to reach advanced stages of development (Yakovlev & Lecours, 1967).

These differential rates of septal vs amygdala maturation are exceedingly adaptive. For example, as the inhibiting septal nuclei develops, the indiscriminate contact seeking of the amygdala comes to be suppressed, inhibited, and sufficiently restricted so that a very narrow and intense attachment is fashioned in its place.

In addition, as the septal nucleus is associated with internal inhibition and oppositional feelings of negativity (Heath, 1976) including rage (Blanchard & Blanchard, 1968; Jonason & Enloe, 1972), the later maturation of this structure likely contribute to the oppositional and defiant childish attitude that emerges around age two: the so called "terrible twos." These behaviors do not promote intimate social interactions and are probably produced secondary to septal influences on the amygdala and hypothalamus as these latter structures commonly trigger rage reactions (see chapter 13).

Destruction of or injury to the septal nucleus eliminates in part those counterbalancing inhibitory influences exerted on the amygdala and hypothalamus. However, septal injury secondary to deprivation and abuse experienced later in development can also induce septal seizure-like activity (Joseph, 1999b). If the septal nucleus is injured or develops seizure-like activity and if the the amygdala is released from septal inhibitory activity, and as the amygdala promotes indiscriminate socializing, there results an extreme desire for social and physical contact coupled with aggressive, explosively violent, and bizarre behavior (Jonason & Enloe, 1972; McClary, 1966; Meyer, Ruth, & Lavond, 1978). That is, since the amygdala as well as the septal nuclues mediates aggressive and social behavior, and since septal destruction of injury results in amygdala disinhibition, the disinhibited amygdala (coupled with septal stressed-induced abnormalities) promotes aggressive, emotionally bizarre behaviors including an extreme desire for indiscriminate social stimulation; some of the same exact behaviors displayed by older infants and young children deprived of maternal contact.

With complete bilateral septal destruction (and amygdala disinhibition) the drive for social contact becomes irresistible and so intense animals will form attachments with species they normally avoid, fear or dislike. Rats with septal lesions will readily seek out rabbits and mice (whom they usually avoid) and will even hug and cuddle with creatures that might kill and eat them, including ill-tempered cats. Septally lesioned animals who are placed together will hug and cling tightly together, forming a squirming ball of living flesh (Jonason & Enloe, 1972; McClary, 1966; Meyer et al., 1978).

Among humans with right sided or bilateral disturbances in septal functioning, or in cases of septal or amygdala seizure-like activity, a behavior referred to as septal "stickiness" or "viscosity" is sometimes observed (Joseph, 1992, 1999b). Such individuals seek to make repeated, prolonged, albeit superficial and inappropriate contact with anyone, even complete strangers so as to tell them stories, jokes or incessantly pass the time. Moreover, they may become irritable, angry and upset if that person leaves or attempts to break off contact; behavior somewhat similar to a 6-month old infant, or animals with septal lesions.

So intense is the need for social contact following septal lesions, that if other animals aren't available, they seek out, cling to, and hug blocks of wood, old rags, or bare wire frames; behavior identical to that of deprived infants, as well as normal children who may form attachments to blankets or "Teddy bears."

However, although seemingly starved for social stimulation, septally lesioned animals and humans also become explosively violent (Jonason & Enloe 1972, MacLean, 1990; McClary, 1966; Meyer et al., 1978). This behavior is similar to that of humans who suffered maternal deprivation late in development (Goldfarb, 1945,1946; Koluchova,1976; Spitz, 1946). That is, these deprived children will display an insatiable need for social stimulation, but also behave in a socially bizarre, bullying, sadistic, and explosively violent fashion.

As noted, for the first 8 months the infant behaves in a socially disinhibited manner and will readily accept hugs and kisses even from complete strangers. As the septal nucleus matures, however, the contact seeking amygdala comes to be inhibited and the formation of loving attachments becomes restricted to the primary caretaker and significant others.

Nevertheless, because the septal nucleus matures at a later age it also becomes more vulnerable to the disruptive effects of neglect and abuse at a later age as well. In fact, Heath (1972) found that monkeys reared under deprived conditions displayed abnormal electrophysiological activity in the septal nuclei. That is, whereas the amygdala first becomes vulnerable to deprivation and abuse suffered during the first 2 to 8 months (and beyond), the septal nucleus (as well as other forebrain structures) becomes increasingly susceptible over the ensuing months and years. Hence, children who are deprived or isolated after the first 6 months or year of development display abnormalities which are identical to those following septal destruction.

For example, children placed in foundling homes for long time periods after they have reached 6 months of age sometimes respond to strangers with extreme social stickiness and persistently express an intense desire for social contact. They may hug, cuddle, and kiss indiscriminately, as well as behave in an exceedingly aggressive and explosively violent fashion (Goldfarb 1943, 1945, 1946; Langmeier & Matejcek, 1975; Spitz 1945). Those reared for the first 4 years under isolated conditions behave similarly (Koluchova, 1976 Langmeier & Matejcek, 1975). Likewise, those placed in an institution after age one display an insatiable need for attention and affection but behave in an aggressive, unfriendly, inappropriate and socially bizarre fashion (Goldfarb 1943, 1945, 1946 Langmeier & Matejcek, 1975).

As the septal nucleus, like the amygdala and hypothalamus, is also implicated in sexuality (MacLean, 1990), abnormalities in this structure can also produce abnormal sexual (as well as aggressive) behaviors. Because these structures are all vulnerable as well as immature, those abused or chronically stressed at an early age, may suffer HPA, amygdala, and septal injury, all of which can produce a constellation of social, emotional, and sexual abnormalities, the nature of which being determined by the degree, repetitive nature, and age at which the infant was traumatized. For example, children placed in foundling homes after they have reached six months or even one year of age, not only become pathologically shy, but also may respond to strangers with extreme stickiness and persistently express an intense desire for social cohesion, which in many cases may include bullying, and abnormal or inappropriate sexual behavior, including unsolicited hugging and kissing, touching and sucking on genitals, or exposing one's self and even urinating on other children (Goldfarb, 1945,1946; Koluchova,1976; Spitz, 1946). That is, they crave social stimulation while simultaneously behaving in a pathologically shy, withdrawn, bizarre, bullying, sadistic, and socially, emotionally, and sexually inappropriate and sexually aggressive fashion: behaviors which are identical to those following septal destruction and associated limbic abnormalities.

Consider, an illustrative case provided by Langmeier and Matejcek (1975, p. 41-42). "F.J. was an illegitimate child of a... mother... who concealed the fact she had a child. Up to almost two years of age the boy was left alone for days at a time, locked in her room, in complete isolation." At age two he came to official notice, was placed in foster care. He "cried all the time... and made only one meaningless sound... The boy veered from being very frightened of people to embracing and kissing everybody... He attacked other children... urinated on other children, touched their genitals and... wanted to kiss and cuddle."

THE UNABOMBER

"The many rejections, humiliations and other painful influences that I underwent have conditioned me to be afraid of people. This fear of rejection--based on bitter experiences at home and at school--has ruined my life, except for the few years that I spend alone in the woods, largely out of contact with people." Ted Kacynski.

Over the course of 17 years, Ted Kaczynski severely injured, maimed, or killed 27 people in 16 different bombings (Douglas, 1996; Graysmith, 1998). He had been living as a hermit and a recluse in a tiny plywood cabin in Montana, when he was arrested by FBI agents, on April 24, 1995. Described as "pathologically shy" Kaczynski was born on May 22, 1942, to Polish immigrants who eschewed learning, but who were otherwise, according to Kaczynski, emotionally cold, distant, and "rejecting" and who he "couldn't come to..." because they used him as a "defenseless butt." "The rejection I experienced even affected me physically," he complained in one letter to his mother.

According to his family, baby Ted has initially been the all American "bouncing... bundle of joy." However, around 9 months of age, he became severely ill with a dangerous case of the hives, was hospitalized and isolated, and even his parents were forbidden to make contact, to touch, hold, or hug him. This was "hospital policy" his mother was informed and sick children were to have "no visitors." There he remained, for over a month, and not once was she allowed to to touch, hold or comfort her son. According to his mother, after an initial protest phase, in which he cried incessantly and would stretch out his arms and plead and cry for her, he becoming increasingly listless, withdrawn, disinterested in and unresponsive to human contact, and "developed an institutionalized look." Thus he rapidly passed through all three stages associated with a condition Spitz referred to as "hospitalism."

For example, according to Spitz (1945, 1946) children between the ages of 6 months to 2 years, even if briefly isolated, would, within minutes, begin crying and screaming for their mothers. This was followed by a stage of despair in which they would cease to cry, lose interest in the environment and withdraw. In the final stage the children ceased to show interest in others and no longer responded to affection. Instead they became passive and unresponsive, sitting or lying quite still with a frozen expression, staring for hours at nothing (see also Bowlby, 1982). If the separation continued there was further deterioration, with children becoming ill or dying. Moreover, Spitz (1945, 1946) found that some children would quickly pass through all three phases, sometimes within a few days, and that those who experienced long-term separations often became permanently emotionally and even sexually abnormal.

However, Ted was not merely isolated, he was placed in full body restraints, and was pinned to his hospital bed with splints, spread eagle and completely naked. Hospital personnel felt that full restraint was necessary so as to prevent him touching his sores, or rubbing off the ointments and dislodging the compresses. As noted above, the amygdala becomes excessively active not only when stressed, but when stressed by physical restraint.

After Ted returned from the hospital all aspects of social and emotional functioning became bizarre. He ceased to respond to affection or social stimulation and became pathologically shy, severely withdrawn, and unable to relate. According to his mother, he was "no longer that happy, bouncing, joyous baby, but a little rage doll that didn't look at me... that was slumped over--completely limp... like a bundle of clothes."

Ted never recovered, and instead remained "always apart, aloof, alone." At age three when he was placed in nursery school, his teacher explained to his mother that "he will not play with other children." As he grew older, his remain isolated and alone, and if visitors arrived at his home, he would withdraw to his bedroom and lock the door. Throughout his undergraduate and graduate college days, Ted continued to avoid others, failing or refusing to acknowledge greetings even from those sharing his dorm at the University of Michigan. He would sweep past them, and quickly close the door to his room.

Although socially retarded, Ted was described as brilliant and a mathematical genius. After graduating from Harvard with a BS, he went on to the University of Michigan and published several papers in prestigious math journals. In 1976, his doctoral thesis on "Boundary Functions" won the annual Sumner Meyers Prize for best doctoral thesis. However, Ted was offered a professorship at Berkeley even before he obtained his Ph.D (Douglas, 1996).

Once at Berkeley, he continued to live the life of a recluse, avoiding human contact, refusing to look at his students, and often ignoring even their questions while he lectured facing the blackboard. He also became increasingly sexually confused and even sought a sex change operation. Nevertheless, he also craved social stimulation which he expressed through his voluminous writings, but when he personally interacted with others, including family or members of the opposite sex, he would react in a bullying, sadistic, and angry fashion often becoming profoundly enraged.

According to his brother, Ted Kaczynski "through the years has shown sudden and unpredictable mood swings, a preoccupation with disease, extreme phobias, compulsive thinking and an inability to let go of minutia. One senses a psyche that feels itself terribly isolated and threatened by the world, tormented by its own complexity, unable to hold things in their proper perspective or to find comfort, security, or rest in itself."

Indeed, Ted himself admitted that his entire life he has felt "always under stress."

As noted, not all humans or animals react the same to stress, abuse, or insufficient social stimulation, as there are individual, gender, and other predisposing factors which differentially contribute to the outcome. In the case of Mr. Ted Kaczynski, it is noteworthy that he complained that his mother had always been emotionally cold and distant. In addition, his father committed suicide, and his brother David, also briefly lived as a recluse, in a hole in the ground, twenty miles from the nearest road. When it rained, or got too cold, David would pull a tarp over the hole to keep out the weather. In this regard, it could be argued that Ted Kaczinsky was already at risk and was predisposed to suffer catastrophic consequences from the brief period in which he was completely isolated around 9 months of age. Nevertheless, in this regard, Mr. Kaczynksi also developed and forever displayed the characteristic symptoms associated with septal and amygdala abnormalities secondary to insufficient maternal and social-emotional stimulation during infancy (Joseph, 1999b).

Although Mr. Kaczynksi developed sexual problems, there is no evidence of sexual abuse in his early history. Of course neglect and isolation coupled with physical restraint, like sexual abuse, is exceedingly stressful, and may induce, to varying degree similar sexual and social-emotional problems due to the damaging effects on the limbic system.

Of course, it would be expected those who are neglected, deprived of sufficient mothering, and who are also sexually abused, would be even more severely and profoundly affected that Mr. Kaczyksi. Although also harboring murderous or at least aggressive and violent impulses, in cases of neglect and sexual abuse, symptoms associated with "sexual traumatization" would likely predominate.

THE CASE OF THE HETERO/HOMOSEXUAL TRANSVESTITE RAPIST AND PEDOPHILE

Children who are sexually abused sometimes become sexually precocious and behave in a sexual manner with friends and school mates. They may fequently pull down their pants, or pull up their skirt and expose their genitals as well as play with the genitals of friends or allow them to play with theirs. They may also sexually act out with adults, or once they become an adult, they may sexually act out with children, or with individuals and in situations which are associated with the original sexually traumatizing experiences--a function of the abnormal activation of those structures involved not only in stress and sexuality, but memory.

Moreover, as noted, males with a history of CSA are four times more likely than non-abused males to engage in homosexual activities (Finkelhor, 1979); disturbances also seen with amygdala dysfunction. In addition, a significant relationship between CSA and teenage- or adult-onset pedophilia and violent criminal behavior has been reported (Haaspasalo and Kankonon, 1997; Knight and Prentky, 1993; Rubinstein et al., 1993; Watkins and Bentovim, 1992; Widom and Ames, 1994), including violence toward loved ones and intimate partners (Duncan and Williams 1998), including rape--and violence including sexual violence is also associated with abnormalities involving the amygdala, as well as the septal nuclei.

As noted, the amygdala becomes activated when stressed, and when subject to physical force, threat, when engaged in sex acts, or all of the above. The amygdala, as well as the hypothalamus, may also become abnormally sexually differentiated in response to abusive, stressful, and in reaction to sexually stressful and abusive episodes repeatedly experienced early in life. In addition, the septal nuclei may be adversely affected. Due to the consequent neuroplastic alterations induced (including those which are learning-related) a range of bizarre sexual and aggressive abnormalities may ensue, again depending on the nature, repetitiveness, and age at which the abuse was suffered.

Moreover, as the amygdala is associated with the production not only of sexual behavior, but sexual imagery and affective memories, and as the septal nuclei interacts with the hippocampus (as does the amygdala) in learning and memory (see chapter 14), the combined abnormalities involving these structures may result in the uncontrolled and obsessive production of bizarre sexual thoughts and fantasies. Hence, a child who was repeatedly sexually abused may frequently think and fantasize about what happened, or he/she may act out the abuse with others, and, depending on the nature of the early sexual abuse, may seek out abusive homosexual or heterosexual relationships and/or fantasize about engaging in abnormal sex acts--behaviors, thoughts, and fantasies which may persist into adulthood.

Consider, for example, a 36 year old burglar I was appointed to evaluate by the Santa Cruz County Superior Courts, in California. "Allen" had been charged with 11 counts of burglary, but oddly, he had only stolen women's clothing; items that he could have easily purchased from any store. Like many burglars he admitted that breaking into homes was sexually arousing, and like many burglars he felt compelled to masturbate and to ejaculate on the bed or clothing of the victim. However, unlike other burglars, "Allen" would first put on the clothing of his female victims, usually panties and bra, and would then proceed to ejaculate.

Allen claimed that he felt an irresistible compulsion to commit burglaries and to steal and wear women's clothes. In fact, he been discharged from the Army for dressing in women's clothing, and for exposing his penis to other soldiers when dressed in this fashion. Allen in fact had frequently engaged in homosexual acts while dressed as a woman, and had sex with numerous little boys while so attired.

Allen was not purely a homosexual transvestite with a compulsion to steal and expose himself and to have sex with little boys, for he was also sexually attracted to women. Indeed, he fantasized about raping women while dressed in sexy panties, bra, and women's clothing, stalked women while dressed in women's clothing, and in fact raped several different women while so attired, after encountering them alone in various laundry mats.

Disgusted and repelled as well as uncontrollably aroused by his compulsions and behavior, Allen realized that he was "sick" and that his acts could only be committed by a "very sick person" and he made several suicide attempts and frequently slashed and cut his own body. After he was finally arrested, he made several more suicide attempts and slashed his body.

Although there was likely a genetic component to his behavior (or at least a genetic predisposition), Allen was also an obvious product of his early rearing environment which was characterized by maternal neglect and severe sexual abuse. Born out-of-wedlock in a state mental hospital to a schizophrenic mother, he was placed in and out of various foster homes only to be returned to his mother every time she was discharged from the hospital. Finally, at age three, when it became clear to the authorities that Allen was being profoundly neglected, he was placed in yet another foster home where he was then repeatedly sexually abused and raped by his homosexual "foster" father. His "foster" parents, however, obtained a particularly perverse pleasure in forcing Allen to dress as a girl, incuding bra and panties, his "foster" mother sometimes applying makeup and lipstick. Moreover, while Allen was costumed in female attire his "foster" mother would sometimes watch or even hold him down while his "foster" father orally raped and sodomized him. According to Allen, his earliest memories were of being dressed in girl's clothes and being sodomized and "forced to suck dick."

Apparently this nightmare of oral rape and sodomy continued on a daily basis for two years, at which point he was returned to his mother at age five. However, because his mother was still psychotic and was not providing him with care, he was finally declared a ward of the state. Allen spent the next 13 years living in various foster homes under varying conditions of neglect and emotional and sexual abuse. Indeed, he states that although he hated what had happened to him when he was regularly raped as a child, and although he felt sexually attracted to girls and women, that he nevertheless felt a compulsion to secretly wear bra and panties and would solicit sex from older and younger boys as well as an occasional man--behaviors that led to his discharge from the army, and to his sexual crimes against women while dressed as a girl.






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