Reciprocal interactions between feeding and turning motor networks mediate foraging decisions in a predatory sea-slug

by Jeffrey Brown

Institution: University of Illinois – Urbana-Champaign
Department: 0319
Degree: PhD
Year: 2015
Keywords: Decision-making
Record ID: 2061250
Full text PDF: http://hdl.handle.net/2142/72767


All animals constantly select among an array of competing behaviors in response to environmental stimuli and internal state to maximize their fitness. In simpler invertebrate nervous systems, decision-making arises at the level of antagonistic and cooperative interactions between motor networks mediating different behaviors. These decisions are based on appetitive state, i.e., the moment-to-moment integration of sensation, physiological state, and learning. As a generalist predator, the sea-slug Pleurobranchaea californica confronts a variety of approach-avoidance foraging decisions. Its simple nervous system and behaviors have enabled the neural correlates of these foraging decisions, including those related to sensation, feeding, and locomotion, to be studied in depth at the level of small neuronal circuits and their individual elements. The research described here was aimed at further elucidating the neuronal bases of foraging decisions in Pleurobranchaea, from sensation to motor output, premised on the hypothesis that these decisions involved reciprocal interactions between the feeding and turn motor networks. Behavioral data motivating this hypothesis included observations that extremely hungry slugs would approach nominally aversive stimuli, while highly satiated animals would avoid otherwise appetitive prey. In investigating the integration of sensation in the peripheral nervous system, it was found that dopamine, a pervasive neurotransmitter in both vertebrates and invertebrates, played a role in peripheral sensory processing. Immunohistochemical analyses confirmed putatively homologous dopaminergic densities reported in other gastropods. Sulpiride, a dopamine antagonist, significantly reduced the animal???s performance in a food-seeking task and attenuated responses to stimuli in the major afferent nerves innervating the cephalic sensory organs. These observations suggest that dopaminergic synaptic transmission in the peripheral nervous system is a contributor to sensory integration. It had been previously shown in the isolated central nervous system that sensory input normally eliciting fictive avoidance turns could induce fictive orienting turns through input from the feeding to the turn motor network. It was shown here that this feeding-driven conversion of turn polarity was mediated via a population of neurons exhibiting corollary activation during feeding-network excitation. This input from the feeding network effectively rerouted sensory input from one side of the turn motor network to the other by shifting excitation from one set of serotonergic turn interneurons to their bilateral homologs. Additionally, avoidance-turn command interneurons were inhibited during orienting turns, suggesting that a distinct set of unidentified neuronal elements receive input from the feeding network to effect orienting. At sufficiently high levels of feeding network activation, all turning activity was suppressed. Reciprocal connections from the turn to the feeding motor network were suspected to account for the…