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The effects of forebrain lesions on defense and submission may be explained if one assumes that the parallel pathways of defense and submission in the forebrain have reciprocal inhibitory interactions. Two such inhibitory connections have been illustrated in Figure 3, one from the amygdala to the ventromedial hypothalamus, and a second from the ventromedial hypothalamus to the defense mechanism in the midbrain central gray. According to this model, lesions that disrupt the forebrain pathways of submission should release the defense from inhibition, making the animal more likely to show a lunge-and-bite or striking attack. This is the reason, it is suggested, why lesions of the following structures increase defense behavior: ventromedial hypothalamus in the rat (Anand & Brobeck 1951) and cat (Wheatley 1944); septum in the rat (Brady & Nauta 1953) and cat (Spiegel et al. 1940): anterior hypothalamus in the rat (Maire & Patton 1954) and cat (Fulton & Ingraham 1929), and secondary olfactory structures in the rat (Cain 1974) Most of these effects have been confirmed by many authors, although it should be noted that the effects of septal lesions are transitory and not always observed (Slotnick et al 1973; Sodetz et al 1967). Many authors have concluded that denervation supersensitivity must be involved, because the resulting defense behavior is quite strong. This may be true, but on the other hand it may reflect a subjective judgment on the part of observers who have not seen the defense behavior of wild animals. Although the lesion-induced defense is excessive in comparison to that of laboratory rats and house cats, it may appear normal if compared to that of wild-trapped rats and feral cats.
Lesions that destroy the amygdala would be expected to have the opposite effect, decreasing defense behaviors. The effect should be complicated, however, according to the model. Lesions would: 1) destroy inhibitory projections to the ventromedial hypothalamus, thus releasing its inhibition of defense; 2) destroy afferents of the forebrain pathways that provide motivating inputs for both defense and submission; and 3) destroy a part of the afferent system to the ventromedial nucleus that responds to consociate stimuli. Of these three effects, the first might be expected to dominate, since both the second and third destroy only part of the relevant inputs to their target nuclei. Destruction of the remaining afferents to those nuclei might reverse the effect, however. For this reason, it may be possible to explain why lesions of the amygdala have a pronounced taming effect in the rat (Woods 1956) and cat (Schreiner & Kling 1953), but the taming effect is reversed following additional lesions of the septum in the rat (King & Meyer 1958). According to the present analysis, the taming effect should depend upon the ventromedial nucleus, which may explain why lesions of the ventromedial nucleus reverse the taming effect produced by amygdaloid lesions (Kling & Hutt 1958). If the inhibitory projections to the ventromedial nucleus are M-cholinergic, this may explain why M-cholinergic blockade in the ventromedial nucleus suppresses affective defense produced by chemical stimulation in the midbrain central gray of the cat (Romaniuk & Golebiewski 1977).
Stimulation of structures that project to the ventromedial hypothalamus should facilitate submission and suppress defense according to the model. Considerable published data support this prediction. In rats, electrical stimulation of the septum suppresses defense (lunge-and-bite attack) previously enhanced by ventromedial hypothalamic lesions (Brayley & Albert 1977) and inhibits affective attack in cats (Siegel & Skog 1970). Similar stimulation facilitates submission (fleeing) in response to footshock or electrical stimulation of the central gray and adjacent tegmentum in rats (Gardner & Malmo 1969) and facilitates hissing and escape from hypothalamic stimulation in cats (Siegel & Skog 1970). In cats, chemical stimulation of the amygdala suppresses defense behavior previously enhanced by chemical stimulation of the hypothalamus (Decsi & Nagy 1974); chemical stimulation of the hippocampus, which provides the main input to the septum, can also suppress defense that has been enhanced by chemical stimulation of the hypothalamus (Nagy & Decsi 1974), while the opposite effect, as one would predict, is produced by lesions of the hippocampus, especially if combined with neocortical damage (Rothfield & Harman 1954). There is a parallel between the latter finding and that of Yutzey et al (1964) that neocortical damage prolongs the hyper-defensiveness of rats produced by septal damage.
There are two thalamocortical circuits that appear to modulate the balance between submission and defense. In one circuit, involving projections from the medial dorsal thalamus to the fronto-orbital cortex, there is apparently an inhibitory projection, since the former appears to inhibit defense and facilitate submission, while the latter has the opposite effects. Thus, stimulation of the medial dorsal thalamus produces submission ("fear") in cats (Roberts 1962), and lesions of the medial dorsal thalamus increase affective defense in cats (Schreiner et al 1952), while lesions of the fronto-orbital cortex increase boxing but not biting during shock-elicited fighting in rats (Kolb & Nonneman 1974); the latter would appear to represent increased submissive behavior. In another circuit, involving projections from the anterior thalamus to the cingulate cortex (and thence to the hippocampus), there is again a reciprocal relationship. since the former appears to inhibit submission and facilitate defense, while the latter appears to facilitate submission and inhibit defense. Thus, lesions of the anterior thalamus increase submission and suppress defense in the cat (Schreiner et al 1952), while stimulation of the cingulate cortex and its fiber tract, the cingulum, produces submission (called "fear" by the authors), and lesioning them increases defense behavior in the cat (Koridze & Oniani 1972).
There may be other points in the forebrain where there are inhibitory interactions between the defense and submission systems. These have been indicated by dotted connections in Figure 3. From their work with knife cuts and injections of blocking agents in the rat, Albert & Richmond (1977) came to the conclusion that the septum and olfactory structures inhibit the defense pathways in the lateral hypothalamus. This conclusion is further warranted by the finding by Brayley & Albert (1977) that septal stimulation suppresses defense even after ventromedial hypothalamic lesions. It is also possible that there are inhibitory projections from the ventromedial hypothalamus, not only to the defense motivational mechanism in the midbrain, but also to the defense pathway in the lateral hypothalamus. This could explain why knife cuts between the medial and lateral hypothalamus increase defense behavior in the rat (Paxinos & Bindra 1972; Sclafani 1971).
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