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Limbic System - Neural Bases Of Behavior

structures hippocampus amygdala gyrus region stimulation hypothalamus brain hippocampal emotional

of the temporal lobes. Their observations attracted much attention because of the alterations of emotional aspects of behavior which developed. Further observations were soon made by Kluver and Bucy (26, 27) and others. Normally wild and irascible Rhesus monkeys became tame and docile. They appeared to be "psychically blind" in that they no longer discriminated between objects which are potentially dangerous and those that are useful. They tended to smell, mouth, and attempt to ingest whatever small objects came their way. They made repeated unsuccessful attempts to ingest an inedible object, such as a nail, as though their capacity to remember was impaired. A great increase in sexual activity was noted, but tended to be poorly differentiated in that the monkeys attempted to copulate with monkeys of either sex and with different species of animals. Similar observations have been made on other experimental animals such as cats and dogs. The fully developed syndrome is only seen when the lesions are bilateral and extensively involve paleocortical structures. The paleocortex corresponds roughly to the medial surface of the cerebral hemispheres (Fig. 8).

Curiously, at about the same time as the original report of Kluver and Bucy, Papez (42) independently proposed a theoretical model of the neurophysiologic substrate of emotion which involved many of the same forebrain structures. Although the Papez theory was based on the rather unsystematic observations and incomplete data available at the time, much evidence has subsequently accrued in support of it.

Before discussing Papez' notion of a limbic system or visceral brain, the neuroanatomic structures believed to be important in emotional behavior will be described. There is some disagreement as to what structures should be included in such a system, but most investigators would include the deep structures shown in Figure 8 and the limbic lobe. The latter is the part of the paleocortex which forms a ring or margin (limbus) around the brain stem. It consists of the cingulate gyrus; isthmus, the narrow strip between the cingulate and hippocampal gyrus; the hippocampal gyrus; and the uncus, the eminence near the tip of the hippocampal gyrus (Fig. 8). Of the deeper structures shown in Figure 8, the most important are the amygdala, hippocampus, fornix, mammillary body, and septal region. The amygdala is an almond-shaped nucleus underlying the uncus near the tip of the hippocampus. The hippocampus is an elongated mass of gray matter deep to the hippocampal gyrus. The fornix is a curved fibrous tract extending from the hippocampus to the mammillary body, a portion of the hypothalamus. The septal region forms that part of the wall of the telencephalic hemispheres which lies above the optic chiasm, below the anterior commissure, and anterior to the lamina terminalis.

Papez (42, 43) speculated that these phylogenetically old structures are concerned with emotions and behaviors, such as searching for food and fight or flight in the presence of danger, which ensure the satisfaction of basic biologic needs. Specifically, he proposed a neurophysiologic circuit by which emotional coloring may be added to cognitive processes, a neocortical function, and appreciated subjectively as emotion. The course of impulses goes as follows: Hippocampus > Fornix > Mammillary Body > Anterior ThalamicNuclei > Cingulate Gyrus > Neocortex On the contrary, psychic activity may activate limbic system structures and produce the various behavioral and autonomic manifestations of emotion by a reverse circuit: Neocortex > Cingulate Gyrus > Isthmus > Hippocampal Gyrus >Hippocampus > Fornix > Mammillary Body > Hypothalamus Since the circuit may have reverberatory properties, the emotional concomitants of an experience might be intensified by a continued action between neocortical (cognitive) and limbic system (motivational) structures.

MacLean (31, 32, 33, 34) elaborated the Papez theory and proposed the term visceral brain. He subsumed the various functions of the system under two broad categories: those concerned with self preservation and those relating to preservation of the species. The first would include alimentary functions, such as searching for food and chewing, and defense functions, such as rage when attacked. Preservation of the species would include grooming and copulatory behavior.

MacLean emphasized also the role of the visceral brain in the regulation and interaction of complex autonomic, endocrine, and skeletal muscle activities. Thus, the system would be intimately involved in the pathogenesis of psychophysiologic reactions. These are illnesses characterized by physiologic disturbance, with or without permanent structural change, in which emotional factors play a significant etiologic role. Examples are some cases of peptic ulcer, essential hypertension, and tension headaches. There is some experimental evidence for these relationships. For example, direct electrical stimulation of the amygdala of cats is reported to produce marked increases in the acidity, volume, and pepsin content of gastric secretions which is sufficient, in many instances, to produce erosions and hemorrhage (52). A rise in systolic blood pressure has been reported in humans on stimulation of the fronto-temporal region in man (6).

It has been evident from some of the earliest investigations of the limbic system that specific complex functions cannot be ascribed to single structures considered in isolation. As other parts of the brain, the complex functions subserved by the visceral brain are the result of various structures acting in concert. Nevertheless, clues are provided as to the contribution of various parts to the system as a whole by experiments which focus on one or another anatomic structure. A comprehensive review of this literature is not possible, but the salient features of some of these structures will be described.

The hypothalamic region of the diencephalon is an area of gray matter in which 16 to 18 discrete nuclei are discernible in man. The hypothalamus is primarily concerned with the integration of emotional behavior. Through its rich connections with other neural structures it is important in the regulation of autonomic nervous activity. Through its connections with the pituitary, the "master gland" of the endocrine system, the hypothalamus exerts a profound influence on endocrine balance. For example, tumors of the hypothalamus are sometimes associated with precocious sexual development, a consequence of disproportionate release of gonadotropic hormones from the anterior pituitary. In addition, lesions of various hypothalamic nuclei areappetite, emotionality, wakefulness, and temperature regulation.

Electrical stimulation of the amygdala most commonly produces reactions of attention, fear, and rage which, to some extent, tend to occur in that order as the intensity of stimulation is increased. Similar reactions have been observed in human subjects as well (20). These changes are accompanied by intense visceral alterations in respiration, blood pressure, heart rate, gastrointestinal motility, and so forth. Destructive lesions of the amygdala produce marked behavioral changes only when bilateral. Typically, animals become tame and docile and show a peculiar hypersexuality. The latter consists not only in increased mounting and associated sexual behavior peculiar to the species but also in the lack of discrimination of sexual object, as was described earlier in the Kluver - Bucy syndrome (50).

The complexity of the problem and the interrelatedness of the amygdala with other neural or endocrine structures is apparent from other experiments. For example, these behavioral changes are seen in adult cats with bilateral amygdala lesions but not in kittens, suggesting that a certain level of neuroendocrine maturation is necessary for the effects to be manifest (23). Further, the placid animal produced by bilateral amygdalectomy can be converted into a "vicious" and "rageful" animal if an additional lesion is produced in the ventromedial nucleus of the hypothalamus (50). Some of these latter observations suggest that the effects of amygdalectomy are related to the disruption of amygdala-hypothalamus-brain stem connections rather than disruption of the hippocampus-fornix system. This is supported by the well-defined anatomic connections between amygdala, hypothalamus, and brain stem. In contrast, the anatomic connections recognizable between amygdala and hippocampus are less distinct (24). Further evidence of the amygdala-hypothalamus relationship is given by an experiment of Egger and Flynn (9). They report that the attack behavior elicited by hypothalamic

Septal Region

The anatomic boundaries of the septal region were described earlier. It is not to be confused with the septum pellucidum to which it is basal and anterior. Electrical stimulation of some nuclei in this region is strongly reinforcing in a great variety of experimental animals. Alertness and subjective reports of "good feelings" have been reported in human subjects stimulated in this region. The Tulane group headed by R. G. Heath (15) reports that stimulation in the septal region may give relief from severe pain due to cancer and rheumatoid arthritis. The relief may persist for several hours after the stimulation is terminated.

Experimental lesions in the septal region are reported to interfere with conditioned responses. Rats fail to respond to a stimulus which previously elicited a conditioned emotional response of the fear or anxiety type (5). However, there is no interference with the acquisition of conditioned fear responses of the same kind.

Hippocampus

The term hippocampal gyrus refers to the fifth and most medial convolution of the temporal lobe. The hippocampus, or Ammon's horn, is an elongated aggregate of gray matter which lies beneath the hippocampal gyrus. It has somewhat poorly defined connections with the amygdala, which lies immediately anterior to it, and well-defined connections with the fornix with which it is continuous caudally (Fig. 8).

Efforts to establish the functions of the hippocampus have been frustrating (14). Some investigators have remarked that its functions appear to change with each new experiment. This is particularly true of observations on human subjects with electrical stimulation of the hippocampus (41). Rage reactions have been reported to follow bilateral hippocampal lesions in both cats and dogs (4). Others report docility and hypersexual behavior reminiscent of amygdaloid lesions (24).

Kaada (22) reported electrical stimulation of the hippocampus in conscious cats to produce quick glancing and searching movements suggestive of psychic or sensory experiences of some kind. By and large, however, electrical stimulation of the hippocampus in both conscious human patients and experimental animals has yielded minimal or inconsistent results with respect to somatomotor, autonomic, and psychic changes (14).

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