Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems

Abstract

The expression of innate reproductive, defensive, and ingestive behaviors appears to be controlled by three sets of medial hypothalamic nuclei, which are modulated by cognitive influences from the cerebral hemispheres, including especially the amygdala and hippocampal formation. PHAL analysis of the rat amygdala indicates that a majority of its cell groups project topographically (a) to hypothalamic behavior systems via direct inputs, and (b) to partly overlapping sets of hypothalamic behavior control systems through inputs to ventral hippocampal functional domains that in turn project to the medial hypothalamus directly, and by way of the lateral septal nucleus. Amygdalar cell groups are in a position to help bias or prioritize the temporal order of instinctive behavior expression controlled by the medial hypothalamus, and the memory of associated events that include an emotional or affective component.

Introduction

The influential work of Klüver and Bucy [65] established an important role for the medial temporal lobes and adjacent regions of the cerebral hemispheres in modulating sexual, defensive, and ingestive behaviors — which are innate or hard-wired genetically, and are modified by life experiences encoded in the hemispheres. One part of the medial temporal lobe, the hippocampal formation (HPF), participates in the consolidation of episodic memory (e.g., [34], [116], [129], [130], [148]), whereas certain parts of the adjacent amygdala are specialized to modulate instinctive behaviors and the visceral/emotional responses coordinated with them (e.g., [11], [21], [30], [36], [47], [61], [76], [79], [81], [128], [155]). Recent high resolution structural analysis of medial hypothalamic circuits with PHAL, combined with earlier functional results, have begun to clarify the organization of distinct systems that appear to control the initiation of coordinated ingestive behaviors, as well as reproductive and defensive behaviors — that is, homeostatic and social behaviors [15], [115], [135]. This information has stimulated a detailed reexamination of how temporal lobe inputs to the hypothalamus are organized with respect to particular functional systems.

One outcome has been the characterization of topographic order in hippocampus to hypothalamus projections, especially those involved in ‘relays’ through the lateral septal complex [112], [114], [115]. Anterograde and retrograde axonal pathway tracing experiments indicate that distinct though partly overlapping domains along the dorsoventral (septotemporal, longitudinal) axis of the hippocampus proper/subiculum project in a topographically ordered way to components of the various hypothalamic behavior control systems, predicting that differential information processing or neural activity localized to particular HPF domains influences the temporal order displayed by particular classes of behavior. In other words, hippocampus to hypothalamus pathways are strategically placed to help prioritize the expression of alternative behavioral options over the course of time.

In this paper we present a detailed reexamination of topographic order in two other aspects of temporal lobe circuitry related either directly or indirectly to the hypothalamus. One involves the organization of direct projections from various cell groups of the amygdala to the hypothalamus, whereas the other involves the areal and laminar distribution of amygdalar projections to the HPF — which in turn projects to the hypothalamus. In an accompanying paper we consider how another aspect of this circuitry — projections from the amygdala to the bed nuclei of the stria terminalis — is organized [33]. Taken as a whole, this information provides a new model of amygdalar influences on hypothalamic systems. The functional dynamics of this circuitry remain to be characterized.