Evidence for a second hippocampal efferent pathway to hypothalamus and basal forebrain comparable to fornix system: a unit study in the awake monkey.

Abstract

Extracellular microelectrode techniques were used to investigate the influence of anterior and posterior hippocampal volleys on hypothalamic, basal forebrain and preoptic unit activity in the awake primate with complete bilateral lesions of the fornix system. Anterior hippocampal formation volleys affected 13% (80/603) of all units tested: 19% in basal forebrain (32/168), 12% in the hypothalamus (44/372) and 6% in preoptic areas (4/63). The 3 structures with the highest percentage of responses were nucleus accumbens (23%), bed nucleus stria terminalis (20%) and ventromedial nucleus hypothalamus (19%). Of 80 units responding, 76% were initially excited and 24% initially inhibited. Minimum unit latency was 20 ms. The most characteristic response was to low-intensity single-shock stimulation and consisted of several spikes with an initial latency of more than 20 ms and small-latency variability. Complex responses consisting of combined excitatory and inhibitory influences were infrequent. Posterior hippocampal volleys affected only 1 of 603 units. During hippocampal afterdischarges, 55 of 56 units affected in the 3 regions were excited. Following the afterdischarge, the excited units showed suppressed activity typically lasting 70 s. Comparison was made with the intact primate. A major part of hippocampal formation influence on hypothalamus and basal forebrain apprently is mediated via a nonfornix pathway(s). The anterior hippocampal formation has a dual influence on hypothalamus and basal forebrain: the major influence of the anterior hippocampus on hypothalamus and basal forebrain appears mediated via a nonformix pathway(s). A lesser influence is exerted via the fornix system. In the ventromedial nucleus of the hypothalamus, the anterior hippocampus exerts a significant excitatory nonfornix influence and possibly an inhibitory influence via the fornix system. The posterior hippocampal formation appears to influence the basal diencephalon almost entirely via the fornix system. Three possible anatomical pathways for this major nonfornix hippocampal influence are proposed. This dual hippocampal influence on hypothalamus and basal forebain is discussed considering the distinct and often contrasting behavioral, autonomic and endocrine functions of the posterior vs. anterior hippocampal formation.