Dopamine as a Multifunctional Neurotransmitter in Gastropod Molluscs: An Evolutionary Hypothesis

AbstractThe catecholamine 3,4-dihydroxyphenethylamine, or dopamine, acts as a neurotransmitter across a broad phylogenetic spectrum. Functions attributed to dopamine in the mammalian brain include regulation of motor circuits, valuation of sensory stimuli, and mediation of reward or reinforcement signals. Considerable evidence also supports a neurotransmitter role for dopamine in gastropod molluscs, and there is growing appreciation for its potential common functions across phylogeny. This article reviews evidence for dopamine's transmitter role in the nervous systems of gastropods. The functional properties of identified dopaminergic neurons in well-characterized neural circuits suggest a hypothetical incremental sequence by which dopamine accumulated its diverse roles. The successive acquisition of dopamine functions is proposed in the context of gastropod feeding behavior: (1) sensation of potential nutrients, (2) activation of motor circuits, (3) selection of motor patterns from multifunctional circuits, (4) valuation of sensory stimuli with reference to internal state, (5) association of motor programs with their outcomes, and (6) coincidence detection between sensory stimuli and their consequences. At each stage of this sequence, it is proposed that existing functions of dopaminergic neurons favored their recruitment to fulfill additional information processing demands. Common functions of dopamine in other intensively studied groups, ranging from mammals and insects to nematodes, suggest an ancient origin for this progression.