Figure 6.

Sequential acquisition of dopamine functions in nervous systems. The proposed sequence is shown on the left (shaded boxes), using the feeding system of Aplysia as a prototype. Mechanisms or levels of nervous complexity that enabled DA to assimilate each function are shown at right. According to this hypothesis: (A) Initially, DA mediated sensory-motor synaptic signals could influence food searching networks. (B) With the advent of central pattern generator circuits, the role of DA as a sensory neurotransmitter favored its utilization as an activator of motor programs (E: egestive motor program). (C) With the elaboration of more complex multifunctional CPG circuits, the ability of DA to activate motor programs facilitated its implementation in the specification of one pattern versus another. Here, DA is shown selecting an egestive program (E, dark shading) from a network that can also produce ingestive (I, light shading) programs. (D) The ability of DA neurons to select a specific program from a multifunctional CPG led to their utility for factoring the value of a stimulus into such decisions. Here, state sensitivity causes dopaminergic signaling to be down-regulated (potentiometer, lighter blue shading) as the hunger level of the organism is increased, decreasing activation of egestive motor programs (lighter shading) and increasing the tendency toward ingestive programs (dark shading). (E) The ability of DA to activate motor networks via modulatory second messenger cascades facilitated its deployment as a phasic reinforcing signal. Here, a DA pulse originating from pharyngeal sensory neurons is shown following a spontaneous ingestive motor pattern (I). Through activity-dependent modulation of rhythm and burst-generating currents in key interneurons, the dopaminergic reinforcing signal causes the feeding CPG to produce repetitive ingestive programs. (F) The ability of dopaminergic sensory neurons to inform the feeding CPG about the consequences of its activity also led to their participation in stimulus coincidence detection. Here, modulatory DA signals enable a conditioned stimulus (CS) to evoke a specific behavior (ingestive motor pattern shown) following pairing with an unconditioned stimulus (US). Strengthening of synaptic input from the CS pathway to the feeding CPG is proposed to reflect enhancement of an intrinsic plasticity, such as long-term potentiation, In this paradigm, the actions of DA constitute a form of modulatory metaplasticity.