The pathways mediating affective defense and quiet biting attack behavior from the midbrain central gray of the cat: an autoradiographic study

Abstract

The purpose of this study was to describe the pathways which mediate feline affective defense and quiet biting attack behavior elicited from the midbrain central gray. In these experiments, methods of [ 3H]leucine and 2-deoxy-[ 14C]glucose (2-DG) radioautography were utilized in concert with the technique of electrical and chemical brain stimulation. Affective defense behavior elicited from the midbrain central gray is characterized by marked vocalization such as hissing and growling, pupillary dilatation, urination and piloerection. In contrast, quiet biting attack elicited from the midbrain central gray lacks overt autonomic signs observed with affective defense response as well as the stalking component which is typically associated with stimulation of the lateral hypothalamus. Nevertheless, central gray-elicited attack resulted in a directed bite of the neck of an anesthetized rat in a manner similar to that observed from the hypothalamus. Affective defense was elicited from the dorsal half of the midbrain central gray, while quiet biting attack was obtained following stimulation of the ventral half of the midbrain central gray, thus indicating a functional differentiation of the central gray with respect to these two forms of aggression. In a separate series of experiments, affective defense or quiet biting attack response was identified by electrical stimulation through a cannula electrode situated in the midbrain central gray. The affective defense responses were subsequently elicited following microinjections of d,l-homocysteic acid through the same cannula electrode in order to demonstrate that these responses were the result of direct stimulation of cell bodies within the central gray. Then, one of the following autoradiographic tracing procedures was utilized: (1) [ 3H]leucine was injected through a cannula electrode and the animal was sacrificed after a 4- to 14-day survival period; or (2) a 2-DG solution was systemically injected and electrical stimulation was applied through the cannula electrode in order to metabolically activate the pathways associated with each of these responses. In general, the pattern of labelled target regions as indicated by 3H-amino acid radioautography was similar to that obtained from the 2-DG autoradiographic analysis. The principal ascending pathway associated with affective defense was traced to the anteromedial hypothalamus and medial thalamus. Concerning descending projections, label was traced into the central tegmental fields of the midbrain and pons, locus coeruleus and motor and main sensory nuclei of the trigeminal complex. With regard to quiet biting attack, a different projection pattern appears to be present. Label was followed rostrally to the level of the posterior half of the perifornical hypothalamus. Caudally directed fibers associated with quiet attack appeared to be more restricted than those linked to the affective defense response. These axons were traced primarily to the superior colliculus, central tegmental fields and raphe complex of the midbrain and pons. The results suggest that: (1) the midbrain central gray serves as a critical structure for the expression of, at least, the vocalization component of affective defense behavior since axons associated with this response supply nuclei of the trigeminal complex; and (2) the expression of quiet biting attack from the midbrain central gray may involve the activation of both descending fiber bundles from the central gray to the tegmentum as well as those which innervate the perifornical hypothalamus.