Amygdala And Temporolimbic Cortex Regulation Of Aggression

In contrast to the hypothalamus, the amygdaloid complex is reciprocally connected with multiple cortical sensory systems capable of conveying highly processed information regarding the external world. Rich connections are established with a variety of both unimodal and polymodal sensory regions, such as the perirhinal cortex and the superior temporal sulcus, allowing convergence of information from visual, auditory, tactile, and gustatory cortices. The basolat-eral amygdala receives extensive projections from unimodal visual cortices in the inferotemporal cortex (such as area TE in primates) that are specialized for recognizing objects such as faces in central vision. Extensive intrinsic connections within the amygdala promote further coordination of sensory information.

Important outputs from the amygdala in primates are to the hypothalamus, through the stria terminalis and ventral amygdalofugal pathway; to brain stem centers controlling heart rate and respiration through the central nucleus projection pathway; and to the extrapyramidal motor system, especially the ventral striatum, also through the stria terminalis and ventral amygdalofugal pathway.

The amygdala appears to provide a critical link between sensory input processed in the cortical mantle to produce a model of external reality and hypotha-lamic and somatomotor centers evoking pain, fear, and other basic drive-related emotions. Many observations in animals and humans suggest that a fundamental function performed by the amygdaloid complex and related temporolimbic structures is linking perceived objects with appropriate emotional valences. The result is a qualitative steering of behavior rather than quantitative regulation of threshold. On the basis of prior experience, sensory-emotional associations direct consummatory behavior to appropriate targets in the external world.

The importance of the amygdaloid complex in the recall of the affective signficance of stimuli is demonstrated by the drive-object dysregulation of the Kluver-Bucy syndrome observed in animals when the amygdala (and often overlying temporal neocor-tex) are removed bilaterally. Monkeys with such lesions engage in a continuous olfactory and oral exploration of their environment in which each object evokes the same response of tasting and sniffing as though the monkeys had never encountered it. The animals fail to distinguish food from inedible objects and eat metal bolts and feces as readily as normal dietary items. Animals have difficulty distinguishing appropriate from inappropriate sexual partners; similarly, lesioned cats will attempt copulation with chickens or other animals. These results suggest that lesioned animals cannot identify particular objects as being appropriate or inappropriate to satisfy hypotha-lamic drives.

The effects of bilateral amygdalectomy on aggressive behavior are consistent with such a hypothesis. Amygdala removal results in taming and placidity in most animals. Objects that previously evoked signs of fear or provoked attack appear to lose their past associations. Monkeys no longer behave aggressively toward experimenters, becoming docile and easy to handle. Unilateral amygdalectomy with lesions of all commissural pathways produces taming when stimuli are presented to the operated hemisphere but appropriate hostile responses when the stimuli are displayed to the unoperated hemisphere. However, amygdalect-omy in submissive monkeys has led to a maintained or increased level of aggression, consonant with the view that the fundamental effect of amygdalectomy on aggression is not a change in aggressive threshold but a modification of previously acquired patterns of linking stimuli with aggressive responses. Fundamentally appetitive drives, such as feeding and reproduction, are released onto inappropriate targets. An instrumental drive such as aggression is no longer elicited or suppressed according to past, learned responses of the animal.

In humans, extensive bilateral temporolimbic damage produces behavior that is similar to that of lesioned monkeys, frequently accompanied by amnesia, aphasia, and visual agnosia (Fig. 2). Patients may engage in indiscriminate oral and tactile exploration of their environment (hyperorality and hypermetamor-phosis) and change their sexual preferences. Affected individuals exhibit a flattened affect and report diminished subjective emotional responses to stimuli. Aggressive behaviors become uncommon, and apathy with lack of either strongly positive or negative responses becomes the rule. In one series of 12 patients with acquired Kluver-Bucy syndrome, placidity was noted in all. Functional imaging and lesion studies in humans suggest that the amygdala plays a critical role in processing of perceived threat stimuli. Fearful responses to threatening faces and objects are diminished in individuals with lesions largely confined to the amygdala bilaterally. A group performing bilateral amygdalotomies in aggressive patients reported that among 481 cases, approximately 70% showed a reduction in either restlessness or destructiveness, and one-half of these remained placid even when purposefully provoked.

The first reported case of the Kluver-Bucy syndrome in humans illustrates the characteristic clinical picture. A 19-year-old man sequentially underwent left

Figure 2 Bilateral temporolimbic lesions from herpes simplex encephalitis producing Kluver-Bucy syndrome including hypoaggression (passivation). This 42-year-old man was apathetic, indifferent, and impassive. In addition, he constantly manipulated and frequently mouthed objects, made sexual propositions to staff, especially men (prior to his illness he had been heterosexual), and exhibited severe anterograde amnesia and visual agnosia. CT axial images demonstrate large right temporal and smaller left mesial temporal hypodense lesions (reproduced with permission from S. Bakchine, F. Chain, and F. Lhermitte, 1986, Rev. Neurol. 142, 126-132. © Masson Editeur).

Figure 2 Bilateral temporolimbic lesions from herpes simplex encephalitis producing Kluver-Bucy syndrome including hypoaggression (passivation). This 42-year-old man was apathetic, indifferent, and impassive. In addition, he constantly manipulated and frequently mouthed objects, made sexual propositions to staff, especially men (prior to his illness he had been heterosexual), and exhibited severe anterograde amnesia and visual agnosia. CT axial images demonstrate large right temporal and smaller left mesial temporal hypodense lesions (reproduced with permission from S. Bakchine, F. Chain, and F. Lhermitte, 1986, Rev. Neurol. 142, 126-132. © Masson Editeur).

and then right temporal lobectomies for treatment of a refractory seizure disorder accompanied by frequent outbursts of violent behavior. Following the second operation, he demonstrated dramatic behavioral changes, including compulsive manual manipulation of objects in the environment, insatiable appetite, sexual exhibitionism with frequent masturbation, severe retrograde and anterograde amnesia, and prosopagnosia. The reporting physicians were particularly surprised by a new placidity and the resolution of his previously aggressive behavior:

He no longer manifested the slightest rage reactions toward the nurses and doctors, upon whom, before the second operation, he used to rush as soon as they came into sight. The patient, on the contrary, now assumed an extremely childish and meek behavior with everyone and was absolutely resistant to any attempt to arouse aggressiveness and violent reactions in him.

Related, modality-specific alterations in aggressive responding appear when bilateral lesions spare the amygdaloid complex but selectively interrupt pathways linking unimodal cortical sensory processing areas with the temporolimbic region. Stimuli presented solely within the sensory modality disconnected from the amygdala then fail to evoke learned associations, but stimuli that may be processed through other sensory channels elicit normal responses. One reported case of modality-specific limbic disconnection concerned a 39-year-old college graduate who suffered severe brain injury in a motorcycle accident. Computed tomography (CT) scans demonstrated bilateral cerebral hemorrhages in the inferior occipitotemporal region, interrupting visual input to polar and mesial temporolimbic structures. In addition to right hemi-paresis, left hemidystonia, and prosopagnosia, he exhibited visual hypoemotionality—a diminished ability to react affectively to visual stimuli. A former assistant city planner, he was no longer moved by aesthetic differences between buildings. He ceased hiking because he now found natural scenery dull. He complained of total loss of emotional reaction to seeing attractive women in everyday encounters and to erotic visual stimuli. However, he maintained a strong interest in music, to which he listened almost constantly. He could be sexually aroused by verbal-auditory stimuli and derived pleasure from touching and being touched. This modality-specific limbic disconnection extended to fear and aggressive responses. In laboratory testing, when exposed to a series of slides, he rated as neutral and unemotional threatening images such as a gun and a snake, which normal controls scored as negative and highly arousing.

An intriguing contrast to the behavioral alterations that result from removal of the temporal lobes is provided by a far more common clinical condition, temporal lobe epilepsy, in which abnormal neuronal excitability develops within temporolimbic cell populations. Within the temporal lobe, the amygdaloid complex is particularly sensitive to the phenomenon of kindling, in which repeated stimulation of neurons leads to a progressive lowering of the threshold for discharge. Because many processing pathways converge on the amygdala, activity of epileptic foci throughout and beyond the temporal lobe can affect amygdalar excitability. The resulting enhancement of amygdaloid activity may, in a general sense, be the converse of the decreased activity underlying Kluver-Bucy syndrome.

In normal animals, individual amygdaloid neurons respond selectively to biologically significant food and social stimuli. Kindling may lead to long-term changes in limbic physiology that alter and enhance aggressive and other emotional responses to both drive-related and neutral stimuli. Rather than losing previously acquired associations between sensory stimuli and drives, some temporal lobe epilepsy patients appear to forge new, fortuitous associations. Rather than a lack of emotional response to stimuli, they exhibit deepened and generalized affective associations.

Interictal behavioral changes consistent with this model have been observed in a subset of patients with temporal lobe epilepsy. These individuals exhibit a cluster of interictal behaviors that have been labeled the Geschwind-Gastaut syndrome, encompassing deepened emotions, a sensitivity to moral issues, often with religious and philosophical preoccupations, and hypergraphia—a tendency to write about these subjects at great length. As a consequence of strongly felt emotions, these individuals may become highly sensitive to slights or violations of principle and experience intense anger. These patients' strong moral and philosophical beliefs often preclude violent acts. However, if they do act aggressively, their behavior typically is performed in clear consciousness and often followed by sincere regret.

In an illustrative case, a 40-year-old man developed complex partial seizures in his 20s, characterized by fear followed by flushing, tachycardia, and loss of consciousness. He had suffered febrile seizures in childhood. Electroencephalography (EEG) showed bilateral temporal discharges, and pneumoencephalo-graphy demonstrated a dilated temporal horn of the left lateral ventricle. His interictal behavior was remarkable for extreme seriousness with virtually no sense of humor and a sensitivity to infractions of minor military procedures. When fellow servicemen light-heartedly violated minor rules, he would attempt to reason with them. However, he became incensed by their failure to appreciate his concerns, and brawls often ensued. The patient was enraged when sentenced to a military stockade for 1 week, especially because his elaborate ethical justification for his actions was not taken seriously. To indicate his anger, he destroyed plumbing fixtures in his cell and subsequently threatened to kill the magistrate whom he believed had treated him unfairly.

Following release and neuropsychiatric treatment, his temper became better controlled as he developed strong religious and philosophical convictions that prohibited violence. Nonetheless, several years after overt violent behavior had ceased, he told an examiner, "I have more of a problem with anger than anybody I have ever met in my life.'' He described a constant internal tension between feelings of being treated unjustly and a sincere desire not to harm another individual. Other aspects of his behavior consistent with the interictal behavior syndrome included evangelical religiosity, extensive and detailed writing, and inappropriately prolonged encounters with fellow patients and caretakers (enhanced social cohesion/ viscosity).

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