The hippocampus and behavioral maturation

Abstract

The morphology and connections of the hippocampus are briefly described in light of recent anatomical investigations. There is a lack of direct connections with primary sensory and motor structures, instead the hippocampus is the focal point of two loops: the direct septohippocampal loop mediated by cells of the dentate gyrus and regio inferior; and an indirect corticohippocampal loop involving the entorhinal cortex, regio superior, the mammillary body, anterior thalamic nuclei, and cingulate cortex. The literature on the effects of hippocampal lesions on behavior is briefly reviewed. It is suggested that the hippocampus facilitates response braking in the aroused animal. Accordingly, hippocampectomy leads in ambiguous appetitive learning situations to bouts of response emission even when these do not lead to or even interfere with reinforcement; in aversive conflict situations to hyperreactivity rather than defensive immobility; and, while engaged in a prepotent behavioral act, to reduced attentiveness. Septal lesions produced changes similar to those produced by hippocampectomy, while in some tests the opposite effects were obtained after cingulectomy. The different electrical patterns of the hippocampus accompanying different behavioral states are reinterpreted in light of the assumption that the hippocampus is involved in the braking of response emission in the aroused animal by facilitating the septum and inhibiting the cingulate cortex. Desynchronized high amplitude activity is assumed to represent hippocampal inactivation when voluntary activity is not in progress; synchronous slow activity (theta wave) represents the alerting of the braking system without engagement, which is set in readiness concurrently with the onset of voluntary activity; and desynchronized low amplitude is the correlate of the actual engagement of the braking system, as when responding is stopped in the passive avoidance situation. Finally, the syndromes of hippocampectomy in adults are identified as juvenile traits and the hypothesis is put forward that the function of the late-maturing hippocampus is to transform “exuberant,” “reckless,” and “inattentive” juveniles into “placid,” “cautious,” and “observant” adults. This hypothesis predicts that hippocampectomized adults will display additional juvenile traits to those already recognized, and that treatments that retard, accelerate, or prolong postnatal hippocampal development will affect behavioral maturation.