Evolution and function in serotonergic systems

Abstract

Serotonergic systems of invertebrate and vertebrate central nervous systems (CNS) are functionally similar in multiple characters. Serotonin (5-HT) neurons dispersed throughout the CNS of lophotrochozoan invertebrates (molluscs and leeches) are analogous to vertebrate 5-HT neurons concentrated in the raphe nuclei of mid- and hindbrain: they innervate specific central pattern generators and other circuits of the CNS, receive feedback from them, and support general behavioral arousal. In both groups 5-HT regulates excitatory gain of CNS circuitry and uses similarly diverse 5-HT receptors. Marked contrast, however, exists for roles of 5-HT in regulation of appetite. Where invertebrate 5-HT neurons promote an appetitive state, this role is supplanted in the vertebrates by a peptidergic network centered around orexins/hypocretins, to which the role of 5-HT in arousal is subordinate. In the vertebrates, 5-HT has appetite-suppressant properties. This is paralleled by differing complexities of mechanisms that bring about satiety. Lophotrozoans appear to rely on simple stretching of the gut, with no obvious feedback from true nutrient stores. In contrast, vertebrate appetite is regulated by hypothalamic sensitivity to hormonal signals reporting separately on the status of fat cells and digestive activity, and to blood glucose, in addition to gut stretch. The simple satiety mechanism of a mollusc can be used in value-based foraging decisions that integrate hunger state, taste, and experience (Gillette and others 2000). For vertebrates, where appetite and arousal are regulated by signals from long-lived nutrient stores, decisions can be based on resource need going far beyond simple gut content, enabling value estimation and risk assessment in the longer-term. Thus, connection of nutrient storage depots to CNS circuitry mediating appetite may supply critical substrate for evolving complexity in brain and behavior. This hypothesis may be tested in expanded comparative studies of 5-HT and peptidergic functions in appetite and arousal. © The Author 2006. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved.