Due to Amygdala Temporal Lobe Dysfunction
The effects of temporal lobe and amygdala injuries and abnormal activity on sexual and violent behavior are reviewed and an illustrative forensics and diagnostics case study is presented. Injuries to and abnormal activity involving the temporal lobes and amygdala can be localized through neuropsychological testing, and are associated with profound alterations in all aspects of emotion, sexuality, aggression, and personality. Patients may become explosively violent whereas others may behave in a sexually bizarre and sometimes indiscriminate hypersexual fashion. Temporal lobe and amygdala injuries are also associated with memory loss, prosopagnosia, emotional and environmental auditory agnosia, a heightened startle reaction, and excessive orality. In rare instances, as in the case presented here, patients may develop the entire spectrum of symptoms associated with temporal lobe and amygdala dysfunction including homicidal hypersexuality.
Due to Amygdala Temporal Lobe Dysfunction
It is well established that the amygdala and temporal lobes subserve various aspects of sexuality, memory, and emotional, perceptual, and motivational functioning, including feeding, fighting, fleeing, fear reactions, and facial recognition (Davis, Walker, & Lee, 1997; Gloor, 1992; Halgren, 1992; Joseph, 1992, 1998, 1999a,b,c,d; LeDoux, 1996; MacLean, 1990; Rolls, 1984; Hasselmo, Rolls, & Baylis, 1989; Rosen & Schulkin, 1998).
For example, the amygdala is sexually dimorphic (Nishizuka & Arai, 1981, 1983), and depth electrode stimulation, tumors, or seizure activity involving the amygdala or overlying temporal lobe, can trigger sexual excitement, hypersexuality, and male vs female physiological and behavioral-sexual responses, including penile erections, ovulation, uterine contractions, lactogenetic responses, and orgasm (Blumer, 1970; Currier, Little, Suess, & Andy, 1971; Freemon & Nevis,1969; Gloor, 1986, 1992; MacLean, 1990; Remillard, 1983; Shealy & Peel, 1957). Moreover, depth electrode or abnormal activity in these structures have been reported to trigger anger and rage, coupled with lip retraction and the baring of teeth followed, in some cases, by acts of extreme savagery (Devinsky & Bear, 1984; Egger & Flynn, 1963; Gunne & Lewander,1966; Mark, Ervin & Sweet, 1972; MacLean, 1990; O'Keefe & Bouma, 1969; Schiff, Sabin, & Geller, 1982).
These sexual or violent behaviors may be directed at something real, or, in the absence of an actual physical threat or sex partner, at someone imaginary (O'Keefe & Bouma, 1969; Schiff et al., 1982). 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, and further, further." Schiff et al., (1982) described a man who developed intractable aggression and became obsessed with sexuality following a severe head injury and the development of abnormal activity within the temporal lobe and amygdala.
In rare instances temporal lobe and amygdala abnormalities can trigger sexual behavior and violent rage reactions simultaneously; i.e. homicidal hypersexuality. As detailed below, "TL" developed temporal lobe epileptic seizures following a severe head injury and right temporal basilar skull facture. Immediately after he was released from the hospital, his family noted that TL had undergone a drastic personality change. He became indiscriminately hypersexual, exposing himself and making aggressive sexual overtures toward his mothers and sisters, and suffered attacks of explosive rage. Although attempts were made to treat these aberrant behaviors medically, this was to no avail, and he finally committed an act of extreme sexual savagery. TL brutally beat and strangled his mother to death, in the middle of the day, in between music lessons as one of her students waited outside, and then sexually assaulted her body.
TL readily admitted guilt when arrested, and tried to joke with the interviewing officers, repeatedly spoke of sex, made sexual advances to a nurse, but also frequently apologized for what he had done, repeating in an embarrassed, sometimes silly yet chastised voice: "I feel like such an asshole." TL admitted being sexually attracted to his mother, and further admitted that he attacked her, knocked her to the floor, and throttled her with left hand while savagely beating her in the face and mouth with his fist (spraining his hand, and destroying her face). TL reported he removed her clothes, and then sexually molested the body by kissing and licking her breasts and performing cunnilingus. However, he states he was unable to engage in sexual intercourse because he had become impotent. When the interviewing officers informed him that his mother was dead, he was surprised, and then stated in a dissociative manner: "Oh, what are her music students going to do now?" When the officers accused him of stealing money from his mother's purse, he suddenly became enraged.
After his arrest, TL was housed in the main jail and almost continually behaved in a labile, irrational, enraged, hypersexual, and sometimes silly, childlike fashion. He frequently cursed, threatened and screamed at officers and staff, and would kick and pound on the doors and walls. However, immediately following these episodes he would suddenly become apologetic and childlike, and/or hypersexual and would proposition female staff as well as make up grandiose delusions regarding his accomplishments, wealth or prowess as a lover.
This examiner was appointed by the Santa Clara County Superior Courts, at the request of his attorney, to perform a forensic neuropsychological evaluation of TL for the purposes of determining competency and sanity at the time of offense. During the course of our initial interview TL repeatedly made sexual comments including graphic descriptions of sex acts he claimed to have performed on family members and female guards. He also manifested a hightened startle reaction and appeared to frequently get irritable and angry. When I asked him why he had been arrested, he put his hand over his mouth and giggled: "I killed mom." When I asked if he had removed his mother's clothes after beating her to death, he quite suddenly flew into an uncontrolled rage, and tried to leap across the interview table as he screamed: "I'll rip your fucking head off...." Fortunately, he was chained to his chair. He quickly calmed down, underwent a remarkable personality change, and became meek and apologetic, stating: "I'm sorry. I'm a gentleman. I'll be good... I'm a gentleman." Other than behaving in a silly, labile, hypersexual, and sometimes hostile manner, and making, on occasion, grandiose confabulatory remarks, he generally cooperated with this examiner.
During our second interview, TL claimed he had no memory of having met me. He even commented about having lost his temper with "the other doctor." It is noteworthy that his two sisters independently reported instances in which he failed to recognize them when he approached them on the street.
History Post Head Injury
"TL" suffered a severe head injury at age 15 when he was thrown from a horse and slammed his head against a tree. He immediately lost consciousness and remained in a coma for two months during which he twice developed "spiking fevers." X-Rays indicated a basilar skull fracture and fracture of the right temporal bone. Upon awakening he was partially paralyzed on his right side and demonstrated severe memory loss, right sided visual and hearing problems as well as speech and language difficulties; the latter of which gradually resolved. In addition, he developed partial complex, temporal lobe epilepsy, and suffered occasional grand mal seizures. His temporal lobe epilepsy was controlled with Dilantin.
Upon his return home family noted a remarkable personality change and stated "he was no longer the same person." TL became emotionally labile, easily irritated, and sometimes childlike, and consistently displayed disinhibited and inappropriate sexuality as well as difficulty controlling his temper. Over the next several years he increasingly suffered explosive rage reactions that frequently resulted in physical violence against adults, children, and pets. He also began exposing himself and masturbating, and sexually propositioning or sexually touching his sisters and mother as well as female strangers.
According to family and medical records, TL became preoccupied with sex and repeatedly and incessantly made overt verbal and physical sexual advances to female strangers, friends and family members and would attempt to fondle, kiss, and even bite them passionately. He would also intrude into the bedrooms of female family members, proposition them for sex, and would expose himself and masturbate. He allegedly sexually molested a 12 year old girl and was no longer allowed to ride the bus to school due to his propensity for sliding his hands beneath the buttocks or between the legs of female passengers. He later began having frequent sex with prostitutes and would bring them to his place of employment (his father's used car lot) where he would have intercourse in the parking lot. This incessant sexual activity, coupled with his rage ractions, led to his dismissal.
TL was described as increasingly suffering explosive rage reactions "over nothing." He would shake and "vibrate" with rage and anger. These fits of rage eventually escalated into physical violence, and he would slap, push, and strike friends, family and their children, or engage in acts of animal cruelty; after which he would often panic and run away and then undergo a remarkable personality change and behave as if he had no memory of his outbursts, or he would become childlike and apologetic.
As his family no longer felt safe, he was forced to move into his own apartment. However he was soon evicted due to his inappropriate sexual behavior and as he physically assaulted a security guard. Several weeks later he attacked a supermarket security guard, beating and wrestling him to the ground. He was arrested for battery but bail was posted and he was later released. Several evenings later he confronted, began screaming at, and then assaulted several police officers who had stopped his car which he had been driving erratically and with his automobile lights off. He was admitted for a 72 hour psychiatric observation. Six weeks later, he attacked his mother during the middle of the day, between music lessons, as a student waited outside. He shoved his mother to the floor, and strangled her as he beat her to death with his fist. He then removed her clothes and sexually assaulted the body.
METHOD & RESULTS
IQ. TL was administed the WAIS-R and obtained a Verbal IQ of 67 (1.5% rank), a Performance-perceptual IQ of 80 (9% rank) and a Full Scale IQ of 72, which placed him in the Borderline range of intellectual ability, and at the 3% rank. A considerable degree of subtest variability was noted within the Performance measures (range: 3-9) and Verbal measures (range: 2-7). These results were interpreted as indicative of bilateral cerebral dysfunction.
Verbal & Visual Memory. TL was administered the Wechsler Memory Scale. As based on the Russell (1975) norms, it was determined that immediate and short-term (30-minute delayed) memory for complex verbal narratives was moderately to severely disturbed. Immediate memory for complex visual-pictorial stimuli was found to be severely disturbed, whereas short-term visual memory was non-existent, as he not only claimed to be unable to recall any of the items, but was only able to pick out one of the 3 items when offered multiple choices that included items from the Bender Gestalt. As complex verbal memory is associated with the left temporal lobe, whereas visual-pictorial memory is linked to the right temporal lobe (Cohen & Eichenbaum, 1994; Delaney, Rosen, Mattson, & Novelly, 1980; Evans, Heggs, & Hodges, 1995; Frisk & Milner, 1990; Joseph, 1996; Kimura, 1963), bilateral temporal lobe dysfunction is indicated with the right temporal lobe more severely affected than the left. However, as amygdalectomized patients perform more poorly on tests of visual-spatial than on verbal memory (Andersen, 1978; Jacobson, 1986; Tranel & Hyman, 1990), and as those with right sided amygdala destruction show even greater deficits (Anderson, 1978) amygdala and right amygdala dysfunction is also indicated.
Prosopagnosia & Emotional Faces Recognition. Because TL failed to recognize this examiner or his sisters, he was administered a test of facial memory, and was shown, one at a time, 4 pictures of faces (two men, two women) which he was encouraged to examine. After a five minute delay he was shown 16 pictures, 4 of which were the faces he had previously viewed. TL was unable to recognize or identify the original four; which is a profound disturbance. Normal performance is 90% to 100% correct (Joseph, unpublished norms). TL was also presented with a profile and full-face picture of himself. He failed to recognize his face in profile, but after approximately a 30 second delay he indicated that the full facial picture was familiar. He then smiled and acknowledged that it was a picture of himself. He was also shown a picture of his attorney whom he had met with over two dozen times. He was unable to recognize the picture of his attorney. Difficulty or an inability to recognize faces is referred to as "prosopagnosia" and is associated with temporal lobe and amygdala dysfunction (Andersen, 1978; Evans et al., 1995; DeRenzi; 1986; Jacobson, 1986; Joseph, 1988a, 1996; Tranel & Hyman, 1990).
In addition, TL was shown pictures of 16 faces each of which displayed either happiness, sadness, anger, or a neutral face (Joseph, 1986a). TL was asked to indicate the emotion depicted. TL identified the correct emotion of only 5 of the 16 pictures, whereas a score of 14 to 16 is considered normal. These deficits are associated with temporal lobe and amygdala dysfunction (Cancelliere & Kertesz, 1990; Joseph, 1988a, 1996). Indeed, the temporal lobes and amygdala contain neurons which respond selectively to faces, and which can differentiate between male and female faces and the emotions they convey (Halgren, 1992; Hasselmo, Rolls, & Baylis, 1989; Morris, Frith, Perett, Rowland, Young, Calder, & Colan; 1996; Rolls, 1984). In fact, the normal human amygdala typically responds to frightened faces by altering its activity (Morris et al., 1996), and if damaged the ability to recognize faces is severely compromised (Andersen, 1978; Jacobson, 1986; Tranel & Hyman, 1990).
Emotional & Environmental Sound Recognition. TL was administered an emotional sounds recognition test which is sensitive to right temporal lobe dysfunction (Joseph, 1986a; see also Cancelliere & Kertesz, 1990; Heilman, Bowers, Speedie, & Coslett, 1984). This tests consists of 16 prerecorded sentences stated in either a happy, sad, angry or neutral tone. He was also administered an environmental sounds recognition test (Joseph, 1988b) consisting of 20 brief sounds such as birds singing, a creaky door opening, etc. He performed exceedingly poorly on both, correctly recognizing (respectively) only 52% and 48% of the items. Normal performance is 90% correct (Joseph, 1988b; see also Cancelliere & Kertesz, 1990; Heilman, et al., 1984)
As failure to recognize emotional and environmental sounds is associated with an injury to the amygdala (Joseph, 1992; Scott et al., 1997) as well as the right hemisphere and right temporal lobe (Cancelliere & Kertesz, 1990; Heilman et al., 1984; Joseph, 1988a) these deficits were interpreted as indicative of amygdala and right temporal lobe injury.
Assessment of Frontal Lobe Functioning.
TL was administered several neurobehavioral measures sensitive to frontal lobe functioning due to his tendency to sometimes make confabulatory delusional remarks and to sometimes behave in a labile, jocular, sexually disinhibited fashion--behavior patterns also associated with damage to the frontal lobes (Fuster, 1997; Joseph, 1986b, 1988a, 1996, 1999e; Luria, 1980).
These tests included the Wisconsin Card Sort (WCS), the Luria 3-step (L3S) which involves making rapid alternating sequential movements of the hands against the table top and in the air "fist-edge-palm" (Luria, 1980, p. 424), and two perseverative graphic writing tasks, e.g. "mnmnmn" (see Joseph, 1996, pp 416-418; Luria, 1980, p 224). TL was able to easily solve all three categories on the WCS, committing a total of 7 errors. He was unable to perform the L3S with either hand. Across perseverative graphic writing tasks micrographic and macrographic reponses were noted, but no perseverations. On the WAIS-R, digit span--a measure of attention and concentration (functions associated with the frontal lobes, Fuster, 1997; Joseph, 1996, 1999e)-- he obtained a raw score of 5 and a scaled score of 2 (severe disturbance). Hence, although the WCS was normal and there was no evidence of perseveration, frontal lobe abnormalities are indicated as based on the L3S and the micrographic and macrographic response tendencies (Joseph, 1996, pp 413-419; Luria, 1980).
EEG, SPECT, MRI. By history, temporal lobe seizure activity was repeatedly documented. Following his arrest, and upon the request of this examiner, TL was administered an EEG, MRI, and a brain SPECT scan. Several EEG's were administered, and revealed theta slowing over the left temporal lobe and intermittent spiking over the right temporal lobe. The SPECT revealed decreased perfusion and severe, extensive, and widespread atrophy and abnormal activity of the right lateral and inferior-anterior-medial temporal lobe, including the amygdala. The MRI indicated bilateral temporal lobe as well as frontal lobe atrophy.
DISCUSSION & CONCLUSIONS
TL suffered a temporal and basilar skull fracture at age 15 and was unconscious for two months. He subsequently developed partial-complex, temporal lobe epilepsy, underwent a dramatic personality change, and was "no longer the same person." He became sexually preoccupied, inappropriately sexually aggressive, and would expose himself and proposition family members and female strangers.
He also demonstrated explosive rage reactions coupled with physical violence, after which he would panic, flee and then undergo a remarkable, sometimes childlike personality change during which he would apologize or act indifferently or in a jocular fashion as if he had no memory of the incident. He became increasingly hypersexual and violent, and sexually molested or attacked family, friends, children, and female strangers including two security guards and police. TL subsequently strangled and beat his mother to death with his fist, and then sexually assaulted her body.
TL also demonstrated extreme orality both before and after his arrest, biting his mothers and sisters, and eating excessive amounts of food. Within one year he in fact gained over 75 pounds, increasing his weight by almost 50%. In addition, TL's sisters report that he failed to recognize them when he met them on the street. He also failed to recognize this examiner, a picture of his attorney, or a picture of himself in profile. In addition he demonstrated a heightened startle response and confabulatory tendencies. Neuropsychological assessment demonstrated severe disturbances of immediate and short-term verbal and visual memory, and severe facial as well as auditory emotional recognition deficits. These disturbances were interpreted as indicating abnormalities of the temporal lobes and amygdala. EEG and SPECT exams indicated considerable atrophy and abnormal activity of the right lateral and inferior-medial temporal lobe, including the amygdala, and MRI indicated bilateral temporal lobe atrophy. Hence, the neuropsychological findings are consistent with the neuroanatomical and neurophysiological evidence, and these findings are consistent with anecdotal observations suggestive of temporal lobe and amygdala abnormalities.
Hypersexuality, rage reactions, prosopagnosia, severe memory loss, agnosia for emotional and environmental sounds, extreme orality, a heightened startle reaction, and panicking/running/fleeing behavior are stereotypically associated with amygdala and temporal lobe abnormal activity and injury (Andersen, 1978; Blumer, 1970; Chen & Forster, 1973; Currier et al., 1971; Devinsky & Bear, 1984; Egger & Flynn, 1963; Freemon & Nevis, 1969; Gloor, 1992; Halgren, 1992; Jacobson, 1986; Joseph, 1998, 1999a,b,c; Mark et al., 1972; Remillard, 1983; Sethi & Raio, 1976). Humans with an abnormally activated or severely injured amygdala may expose their genitals, masturbate in public, become hypersexual, 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).
Although homicidal hypersexuality is rather rare, hypersexuality and paroxysmal episodes of aggression and violent rage have been repeatedly observed following injury, seizures, neoplasm, or electrode stimulation of the amygdala and temporal lobe (Blumer, 1970; Devinsky & Bear, 1984; Egger & Flynn, 1963; Joseph, 1996; Mark et al., 1972; Schiff et al., 1982; Trimble, 1991). Indeed, the amygdala is a major component of the corpus and limbic striatum and can trigger running, kicking, punching, and flailing (Heimer & Alheid,1991; Joseph, 1996; MacLean, 1990; Mogenson & Yang, 1991).
Moreover, the amygdala is sexually dimorphic and when activated can trigger sexual behaviors even in the absence of a partner (Currier et al., 1971; Freemon & Nevis, 1969; Gloor, 1992; Halgren, 1992; Remillard, 1983; Shealy & Peel, 1957). Although some patients become impotent (Taylor, 1971; Toon, Edem, Nanjee, and Wheeler, 1989) others experience an increase in sexual feelings, and then act on it in an inappropriate and indiscriminate manner (Blumer, 1970; Trimble, 1991). They may masturbate and expose themselves in public, seek sex with family members, repeatedly purchase prostitutes, and engage in intercourse with members of their own sex or even animals (Blumer, 1970; Davies and Morgenstern, 1960; Joseph, 1996; Kolarsky, Freund, Macheck, and Polak, 1967; Mesulam,1981; Schenk & Bear, 1981; Terzian and Ore, 1955).
TL's frequent shifts in mood and personality are also indicative of temporal lobe abnormalities (Devinsky & Bear, 1984; Mesulam,1981; Schenk & Bear, 1981; Trimble, 1991). In some cases involving temporal lobe seizure activity, these rather sudden mood changes and alterations in personality are so dramatic patients may appear to be suffering from a multiple personality disorder (Drake, 1986; Mathew, Jack, & West, 1985; Mesulam,1981; Schenk & Bear, 1981; Fichtner, Kuhlman, & Hughes,1990). It has been reported that patients may shift from one personality to another following a seizure or with increases in temporal lobe activity (Mesulam,1981; Schenk & Bear, 1981).
Moreover, with bilateral surgical removal of the amygdala, not only does all aspects of personality, sexuality, and social emotional functioning become bizarre and abnormal, but patient's may no longer recognize friends, family, and loved one's (Lilly, Cummings, Benson, & Frankel, 1983; Marlowe, Mancall, & Thomas, 1975; Terzian & Ore 1955), and display clear deficits in the recognition of faces (Andersen, 1978; Jacobson, 1986; Tranel & Hyman, 1990). As noted, TL failed to recognize his sisters, this examiner, a picture of himself or his attorney, and was unable to recognize pictures of faces he had been instructed to examine just minutes before.
These abnormalities of cognition, memory, and perception, and in particular, the hypersexual and hyperaggressive personality changes, including the savage murder and sexual assault on his mother, are in all respects a composite of those symptoms stereotypically associated with injuries and abnormal activity of the temporal lobes and amygdala.
It is noteworthy, however, that TL also demonstrated behavioral and speech abnormalities associated with the frontal lobes, including lability, confabulatory speech, and disinhibited (sexual and aggressive) behavior (Fuster, 1997; Joseph, 1986b, 1988a, 1996, 1999e; Luria, 1980). Moreover, although there was no evidence of perseveration, he also performed poorly across a number of neurobehavioral measures sensitive to the functional integrity of the frontal lobes, and an MRI indicated frontal (as well as temporal lobe) atrophy. Given that disturbance of the frontal lobes can result in disinhibition and difficulty inhibiting impulses (Fuster, 1997; Joseph, 1986, 1999e; Luria, 1980), and as TL often behaved in a disinhibited and labile manner, it thus appears that TL was also unable to inhibit the homicidal hypersexual impulses generated by his damaged and abnormally active temporal lobes and amygdala. In fact, following massive frontal lobe lesions, frontal lobotomy, or in cases of right frontal lobe seizures, patients not uncommonly engage in inappropriate sexual activity including exhibitionism, gential manipulation, and public masturbation (Joseph, 1996, 1999e).
One patient, after a right frontal injury began patronizing up to 4 prostitutes a day, whereas his premorbid sexual activity had been limited to Tuesday evenings with his wife of 20 years (Joseph, 1988a). In these later instances, however, changes in sexuality appear to be secondary to temporal lobe-amygdala involvement and a loss of frontal lobe inhibitory restraint (as well as loss of judgment or concern for long-term consequences) such that patients act on their impulses without thinking. In this regard, it appears that TL was beset not only with abnormal amygdala and temporal lobe activity thereby giving rise to abnormal hypersexuality and aggressiveness, but that due to his frontal lobe injury he was unable to inhibit these impulses. In consequence, he repeatedly molested or sexually propositioned female strangers and family members, attacked police officers, and as these injuries appear to have become progressively more severe (due to the seizure activity and degeneration in the amygdala temporal lobe), he savagely murdered his mother during the middle of music lessons, and then sexually assaulted her body.
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