The Sea Slug, Pleurobranchaea californica: A Signpost Species in the Evolution of Complex Nervous Systems and Behavior

How and why did complex brain and behavior evolve? Clues emerge from comparative studies of animals with simpler morphology, nervous system, and behavioral economics. The brains of vertebrates, arthropods, and some annelids have highly derived executive structures and function that control downstream, central pattern generators (CPGs) for locomotion, behavioral choice, and reproduction. For the vertebrates, these structures-cortex, basal ganglia, and hypothalamus-integrate topographically mapped sensory inputs with motivation and memory to transmit complex motor commands to relay stations controlling CPG outputs. Similar computations occur in the central complex and mushroom bodies of the arthropods, and in mammals these interactions structure subjective thought and socially based valuations. The simplest model systems available for comparison are opisthobranch molluscs, which have avoided selective pressure for complex bodies, brain, and behavior through potent chemical defenses. In particular, in the sea-slug Pleurobranchaea californica the functions of vertebrates' olfactory bulb and pallium are performed in the peripheral nervous system (PNS) of the chemotactile oral veil. Functions of hypothalamus and basal ganglia are combined in Pleurobranchaea's feeding motor network. The actions of basal ganglia on downstream locomotor regions and spinal CPGs are analogous to Pleurobranchaea's feeding network actions on CPGs for agonist and antagonist behaviors. The nervous systems of opisthobranch and pulmonate gastropods may conserve or reflect relations of the ancestral urbilaterian. Parallels and contrasts in neuronal circuits for action selection in Pleurobranchaea and vertebrates suggest how a basic set of decision circuitry was built upon in evolving segmentation, articulated skeletons, sociality, and highly invested reproductive strategies. They suggest (1) an origin of olfactory bulb and pallium from head-region PNS; (2) modularization of an ancestral feeding network into discrete but interacting executive modules for incentive comparison and decision (basal ganglia), and homeostatic functions (hypothalamus); (3) modification of a multifunctional premotor network for turns and locomotion, and its downstream targets for mid-brain and hind-brain motor areas and spinal CPGs; (4) condensation of a distributed serotonergic network for arousal into the raphe nuclei, with superimposed control by a peptidergic hypothalamic network mediating appetite and arousal; (5) centralization and condensation of the dopaminergic sensory afferents of the PNS, and/or the disperse dopaminergic elements of central CPGs, into the brain nuclei mediating valuation, reward, and motor arousal; and (6) the urbilaterian possessed the basic circuit relations integrating sensation, internal state, and learning for cost-benefit approach-avoidance decisions.