Limbic System

The limbic system is a complex loop of neural structures and circuits involved in the expression and experience of emotions. This pervasive and influential system also plays an important role in learning and memory. The primary structures composing the limbic system include the amygdaloid complex, the septohippocampal system (septal area and hippocampus), the diencephalon (hypothalamus and thalamus), and the limbic cortex. The limbic system has been investigated primarily by observing the effects of intracranial electrical or chemical stimulation or ablation of target areas (Table 3.1).

The limbic system appears to have evolved out of primitive structures involved in the analysis (intensity, quality, and direction) and interpretation of olfactory information. This

Table 3.1. Behavioral and emotional effects produced by stimulating or destroying various limbic areas

Limbic areas

Stimulation

Destruction

Cingulate gyrus

Thalamus Paramedian Ventrolateral Midline Anterior Dorsomedial

Hypothalamus

Ventromedial nucleus

Dorsomedial Posterior area

Anterior area Lateral area

Amygdala

Septum

Tameness or aggression

Relaxation, sleep Affective aggression

Hypophagia

Affective aggression Alertness, excitement (dog)

Sleep (dog)

Quiet (predatory) attack; induces drinking and eating

Fear, wariness, affective aggression (dog)

Defecation, urination, tameness, hypersexuality

Fearlessness (dog)

Apathy

Docility

Rage

Hyperphagia, rage (dog), affective aggression

Inactivity, sleep (dog)

Reduced affective aggression, adipsia, asphagia (dog)

Tameness, docility, passiveness (dog)

Irritability, rage, reduced fearfulness (dog)

Source: From Swenson (1984) and Hoerlein (1971).

function of the limbic system is especially evident in reptilian species, in which the limbic system provides vital olfactory information regulating appetitive and sexual behavior, as well as various agonistic displays. In higher vertebrates like dogs, the limbic system has been diversified to serve a number of new and more complex emotional functions.

Among many other activities, interpretive olfactory functions are still performed by the amygdala. The amygdala is an almond-shaped complex of nuclei embedded in the white matter of the temporal lobe, just below the cortex and anterior to the hippocampus. The nuclei forming the amygdala are divided into three main groups: the basolateral nuclei (receive relayed sensory inputs from the thalamus as well as analyzed sensory inputs from the cortex), corticomedial nuclei (receive afferent inputs from the olfactory bulb and mediate higher cortical analysis of olfactory information), and the central nucleus (projects to the brain stem and hypothalamus and mediates the expression of fear). The amyg dala is interconnected with the hypothalamus by a bundle of fibers called the stria terminalis and a collection of fibers called the ventral amygdalofugal pathway.

In dogs and other mammals, the amygdala mediates the expression of fear and the modulation of aggression. Electrical stimulation of certain areas of the amygdala evokes intense vigilance together with generalized fear or rage reactions. On the other hand, surgical removal of the amygdala results in hyperac-tivity, marked hypersexual interest, compulsive orality, and a loss of fear and aggressiveness. Previously fearful or aggressive animals are "tamed" by amygdalectomy, allowing contact and petting without visible signs of nervousness or fear. Moyer reports a dramatic reduction in fear in an amygdalectomized rat:

Normal albino rats freeze and remain immobile in the presence of a cat even though they have had no prior experience with that animal. However, if the rat is amygdalectomized, its behavior in the presence of the cat is not inhibited and it approaches the cat without reluc tance. In one case an amygdalectomized rat climbed onto the cat's back and head and began to nibble on the cat's ear. The resultant attack by the cat only momentarily inhibited the rat, which again crawled back on the cat's back as soon as it was released. (1976:257)

Many neurons found in the amygdala exhibit a low threshold of excitability and are prone to seizure, with collateral cortical irradiation and possible loss of conscious awareness. Dogs undergoing psychomotor seizure activity may exhibit a pronounced and unpredictable pattern of periodic explosive aggression followed by disorientation. Seizure activity in the amygdala has been associated with the development of psychomotor epilepsy. With the use of electroencephalograms (EEGs), abnormal electrical activity has been identified in the amygdala of aggressive persons. It does seem reasonable that some seizure activity in the amygdaloid complex could result in heightened aggressiveness, vigilance, intolerance, disorientation, and the periodic exhibition of inappropriate explosive rage. A study by Holliday and coworkers (1970) of epilepsy in dogs confirms that epileptic dogs frequently exhibit collateral abnormal behavior (sometimes as their most prominent symptom), including episodic rage, voracious appetites or inappetence, inappropriate vocalizations, aimless pacing and circling, viciousness toward inanimate objects, intense fearful reactions, persistent licking movements, restlessness, and "apparent blindness." Although psychomotor seizure activity may be associated with collateral aggressive behavior (Borchelt and Voith, 1985), aggressive behavior is infrequently diagnosed as a direct symptom of organic disease (Parker, 1990).

Moyer (1976) reports several studies indicating that the amygdala plays an important role in the modulation of predation and other forms of aggression in various animal species, probably through the modulation of fear. Electrical stimulation of different areas of the amygdala either inhibits or excites predatory behavior. Similarly, other amygdaloid locations modulate (differentially inhibit or excite) irritable or fear-induced aggressive displays. For instance, lesions in the central nucleus produce a lower threshold for irritable aggression in dogs. Once provoked, such aggression appears to escalate quickly without signs of fear or escape. In dogs, the spontaneous attack that is observed in cats with identical amygdala lesions (such cats attack conspecifics without any provocation from the target) does not occur. Instead, dogs exhibit increasing signs of irritability and frustrative arousal that quickly builds up and finally precipitates a full-blown and intense rage response—an avalanche syndrome (Fonberg, reported in Moyer, 1976). These behavioral changes suggest that the central nucleus may exercise a strong inhibitory influence (fear) over affective-irritable aggression, with disinhibition occurring when it is damaged.

The amygdala works in conjunction with other limbic structures, cortical association areas, thalamic nuclei, hippocampus (providing memories and context specificity to fear responses), and basal ganglia (giving the amygdala effector access to species-typical motor programs). As noted above, the amygdala also forms direct and diverse connections with the hypothalamus, including hypothala-mic nuclei that control blood pressure, secretion of stress hormones, and the startle response (LeDoux, 1996). The majority of these projections are bidirectional with target structures projecting back to the amygdala, providing a switchboard of interchange between these various areas of the brain. The result is a system of checks and balances over amygdaloid functions, including the display of aggression and fearfulness. In addition to fear, the amygdala appears to play an important role in the mediation of social behavior and motivation. Fonberg and Kostarczyk (1960) observed various changes in the social motivation and behavior of dogs after lesion-ing the dorsomedial amygdala and/or the lateral hypothalamus. In addition to the expected loss of appetite, the dogs lost their ability to show normal social responsiveness to people, expressed no emotion, made no physical contact or effort to look at people, were unresponsive to petting and would often move away when being petted, lost their normal tail-wagging behavior, were easily distracted, were apathetic and slow moving, and, in general, were indifferent to the social environment. Apparently, the lesioned dogs lost their ability to derive pleasure from social interaction.

As is discussed in more detail later in this chapter, the amygdala appears to play a central role in emotional learning (LeDoux, 1994). This function is facilitated by a number of amygdala afferent inputs (basal and lateral nuclei) and efferent outputs (central nucleus) projecting to various somatomotor and autonomic areas controlling the expression of fear in the hypothalamus. The role of the amygdala in the classical conditioning of fear has been demonstrated in a variety of animals and situations (Davis, 1992). Most of these experiments have involved intracranial electrical stimulation or the lesioning of specific areas of the amygdala. Other studies have evaluated the effects of neurotransmit-ters, agonists, and antagonists on the learning of fear. For example, NE has been implicated in the learning of conditioned fear responses (Lavond et al., 1993). Injecting an NE antagonist (propranolol, a beta blocker) into the amygdala after avoidance training disrupts the subsequent performance of the previously learned avoidance task. Also, naloxone (an endogenous opioid antagonist) injected directly into the amygdala enhances the acquisition of avoidance behavior. The explanation for this improvement, however, does not rest on a direct effect of naloxone on amygdaloid activity but on an indirect causation involving the suppression of endogenous opioid activity. Apparently, endorphins interfere with the release of NE in the amygdala during avoidance training. Microinjections of an opioid agonist (levorphanol) also retard avoidance learning, providing additional support for the foregoing account. Ablation of the amygdala disrupts the acquisition and maintenance of avoidance learning. Previously learned avoidance responses are either quickly extinguished after amygdalectomy or may require greater aversive stimulation to be elicited (Thompson, 1967). On the other hand, stimulation of the central nucleus evokes many autonomic reactions correlated with fear: increased heart rate, respiration, and blood pressure. Such stimulation typically results in the inhibition of ongoing behavior and evokes various facial and motoric expressions associated with fear. The constel lation of fearful responses evoked by amygdaloid stimulation is innately programmed and not dependent on learning for its full expression. What is acquired or learned is the range of stimuli and situations able to elicit them.

Conditioned emotional responses are learned when a neutral stimulus (e.g., a tone) is paired with an unconditioned fear-eliciting stimulus (e.g., shock). After a number of pairings in which the conditioned stimulus (CS) and unconditioned stimulus (US) are presented in a close temporal order, the CS will gradually acquire the ability to elicit the fear response without the presentation of the US. This connection between the CS and the US appears to be mediated by the amygdala in conjunction with the thalamus and other related brain sites. Lavond and colleagues (1993) reported a series of studies showing that the classical conditioning of foot-shock reactions (freezing reactions and increases in blood pressure) depends on the participation of various ancillary structures involved in the process of associating conditioned and unconditioned stimuli. Animals with lesions to auditory nuclei projecting from the thalamus (medial geniculate nucleus) to the amygdala fail to learn tone-foot-shock associations but readily learn a light-foot-shock association. Similarly, animals with hippocampal lesions fail to acquire context-foot-shock associations but still learn the tone-foot-shock association. Efferent projections from the amygdala to the hypothalamus also play an important role in classical conditioning of fear reactions. Lesions of the hypothalamus result in both the elimination of conditioned freezing and conditioned blood pressure responses.

In addition to amygdala-hypothalamus interactions, the expression and experience of emotion appear to require the collaboration of several limbic areas, collectively referred to as the Papez circuit (see below). This process begins with emotionally primitive inputs originating in the hypothalamus. These emotional inputs are projected to the anterior thalamus, where they undergo further elaboration and are in turn relayed via the thala-mocortical pathway into the limbic cortex (e.g., the cingulate area). It has been speculated that the limbic cortex provides a kind of neural "screen" organized to receive and bring to awareness primitive emotional impulses originating in the diencephalon. An analogous relationship holds between a film projector and its receiving screen. Just as the image produced by the projector requires a screen to capture and focus its contents, the limbic cortex receives, transforms, and brings to awareness the emotional impulses generated by the hypothalamus. Prior to reaching the limbic cortical areas, emotional input lacks a hedonic quality and an experienced subjective content.

Besides its apparent role in the experience of emotion, the cingulate area appears to play a role in the regulation of motor activity. Stimulation of the anterior cingulate area excites motor activity, whereas stimulation of the posterior cingulate area inhibits it. The cingulate gyrus also appears to play an important role in the exhibition of sexual behavior. in males, cingulate lesions result in a reduction of sexual drive, whereas similar lesions in females have no effect on sexual drive but will disrupt maternal behavior, including patterns of nursing and audiovocal communication maintaining mother-progeny contact. Additionally, the cingulate appears to serve an important function in the facilitation of play (MacLean, 1986). The development of maternal behavior, distress vocalization, and play are limbic hallmarks differentiating the mammalian brain from that of the reptile. The reptile brain lacks a structure equivalent to the cingulate gyrus. An important implication of MacLean's work for dogs is the putative localization of separation-distress vocalization within the anterior cingulate gyrus.

Another limbic structure of interest is the septal area—a putative reward center. in humans, electrical stimulation of the septum results in the pleasurable sensation of building to, but never realizing, orgasm. Whereas the amygdala is largely involved with the expression and experience of emotions associated with self-preservation (e.g., escape-avoidance of aversive stimuli), the septal area mediates the experience of affects associated with sexual behavior (MacLean, 1986). Electrical stimulation of the septal area results in strong erotic feelings and increased libido. An im portant regulatory function performed by the septum is the inhibition of negatively motivated behaviors such as aggression. Self-stimulative electrodes implanted in the septum of human patients have been used to control impulsive aggression. in general, lesions of the septal area result in disinhibition of aggressive impulses together with exaggerated reactivity to startle—septal rage syndrome. Supporting this inhibitory function, the septum receives serotonergic projections from the raphe bodies in the brain stem. Apparently, the septal area performs an excitatory role over hedonically pleasurable affects (e.g., erotic sensations) while inhibiting aversive ones. Not surprisingly, it follows that septal damage adversely affects the animal's ability to play (Panksepp, 1998). Although cingulate lesions appear to negatively influence active avoidance learning (negative reinforcement), passive avoidance learning (positive and negative punishment) may be enhanced by such lesioning. in contrast, septal lesions interfere with passive avoidance learning (i.e., learning that requires strong inhibition) but do not appreciably interfere with active avoidance learning and, in some cases, may even improve it (Gray, 1971). Also, extinction and reversal learning in which a previously learned response must be abandoned or inhibited in order to learn a new one is disrupted by lesioning of the septal area.

Most investigations of subcortical and cortical limbic areas have been carried out with the aid of ablation techniques or electrical stimulation of target brain areas. This emphasis has naturally led some researchers to explore invasive procedures in the treatment of behavior disorders. Delgado (1969) has been particularly influential in this regard. in his famous demonstrations, a charging bull is halted in its tracks at the push of a button, showing in a very dramatic way that aggressive behavior can be controlled by remote electrical stimulation of the brain. His work offered hope that alternative treatment modalities for the control of intractable and otherwise untreatable behavior disorders might be on the horizon. Another area that has received some attention, including some rather horrifying applications in human patients, is neurosurgery. Although very little experimental work utilizing neurosurgery as a means to control abnormal behavior has been carried out in dogs, it would appear from basic research that neurosurgery could provide relief in some cases involving severe or intractable anxiety, phobia, and aggression (Beaumont, 1983), especially where euthanasia is the only alternative. Prefrontal lobotomies have been performed on dog-aggressive sled dogs (malamutes) and on family dogs with various aggression problems (Allen et al., 1974). The surgeries appeared to be most effective in the management of intraspecific aggression in the sled dogs but yielded only limited benefits for pet dogs exhibiting aggression toward people. Other targets for such surgery that have been mentioned in the literature include thalamocingulate projections (cingulectomy), the thalamocortical pathways, or various sites in the amygdala and hypothalamus. Since a considerable amount of surgical risk and cost is associated with such interventions, the procedure is rarely used. A major problem associated with neurosurgery is the brain's tendency to compensate for its losses, often resulting in shortlived benefits (for weeks to months) from limbic lesioning (Thompson, 1967).

In addition to neurosurgery, electrocon-vulsive therapy (ECT) has also been used to treat aggression problems in dogs (Redding and Walker, 1976). The authors reported a significant reduction in aggression exhibited by the treated dogs toward the owner, children, dogs, or other adults (both men and women) as the result of ECT. Redding (1978) also suggests that ECT may prove to be a useful therapeutic tool in the treatment of other behavior problems, including fear biting, neurodermatitis, destructive tendencies, flank sucking, tail biting, and excessive fear of loud noises. The effect of ECT in the treatment of these behavior problems has not been evaluated. Redding (1978) recommends a treatment program involving daily multiple convulsive exposures (under general anesthesia) carried out over a week. After day 3 or 4, marked changes are usually observed in aggressive dogs in the direction of increasing docility. He notes that repeated treatments and retreatments may be necessary to maintain the improved behavior. As is the case in human patients, ECT has a pronounced effect on memory:

After ECT treatment an "aura" of confusion and apparent loss of memory is observed in all patients. Owners report that their dogs are confused at times for 2 to 4 weeks after the treatment, after which there is a gradual return of memory. Following treatment and release from the hospital, the dog may show no more interest in the owner than in any other person. The ability to recognize the owner returns relatively rapidly, however. (1978:695-696)

According to Redding, memory loss is associated with the therapeutic benefit of ECT. To my knowledge, little additional research has been carried out to evaluate the effectiveness and side effects of ECT. Like psychosurgery, ECT has an ethical stigma attached to its use, making it a last-resort option for the treatment of refractory aggression—if used at all.

How To Buy A Shock Collar

How To Buy A Shock Collar

Bark collars are a specific type of training tool that is ideal for dogs with a natural tendency to bark excessively, or more than usual for any reason. Bark collars are designed to provide negative reinforcement in reaction to the unwanted barking behavior. Over time, the dog will learn to avoid the behavior in order to avoid the negative reinforcement.

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    What is hyperphagia in dogs?
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    How does the limbic system control a dog?
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