The Evolution of Neuroanatomical Substrates of Reproductive Behavior: Sex Steroid and LHRH-Specific Pathways Including the Terminal Nerve

Abstract

Fairly recent anatomical methods have made possible the mapping of neurobehavioral systems involving two types of reproductive hormones, gonadal steroids and the peptide luteinizing hormone releasing hormone (LHRH). Brain sites of steroid uptake are detected using autoradiography; LHRH is localized in cells and fibers using immunocytochemical procedures. Both hormone types are known to strongly influence sex behavior and it can reasonably be assumed that these effects are mediated in large part via systems identified using the anatomical procedures. Analysis of the comparative anatomy of these systems should therefore provide information useful in the construction of models concerning the evolution of neurohormonal control of reproductive behavior. The results of such a study are reported. Sex steroid and LHRH systems in cyclostomes, teleosts, amphibians, reptiles, birds and mammals are considered in detail. A synthesis of this information has led to the following ideas. Androgenic control of male reproductive systems has evolved in a number of nonhomologous motor systems controlling male reproductive behavior. Sex steroid and LHRH systems may interact at several different levels of the neuraxis but the most obvious overlap of the systems occurs in the septal and POA areas. The latter especially is a fairly constant and perhaps primitive feature. LHRH secretion into the systemic circulation was most likely the earliest means for LHRH modulation of both pituitary function and neural systems controlling reproductive behavior.Pathways for more direct delivery of LHRH to pituitary cells and brain nuclei probably developed in the early gnathostomes. The terminal nerve appears to be a rather conservative LHRH-containing pathway connecting olfactory systems with septal-preoptic nuclei. A function in pheromonal control of sex behavior is suggested. The general distribution of steroid concentrating cells and LHRH pathways in tetrapods seems to be rather constant. Absence of the systems in neocortical areas and their homologs is conspicuous.