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Title:Reciprocal interactions between feeding and turning motor networks mediate foraging decisions in a predatory sea-slug
Author(s):Brown, Jeffrey
Director of Research:Gillette, Rhanor
Doctoral Committee Chair(s):Gillette, Rhanor
Doctoral Committee Member(s):Anastasio, Thomas J.; Gillette, Martha U.; Nelson, Mark E.
Department / Program:School of Molecular & Cell Bio
Discipline:Biophysics & Computnl Biology
Degree Granting Institution:University of Illinois at Urbana-Champaign
Degree:Ph.D.
Genre:Dissertation
Subject(s):Decision-making
Neuroethology
Pleurobranchaea californica
Sea-slug
Neuronal Networks
Foraging
Dopamine
Cyberslug
Abstract: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 prior observation that avoidance turning suppressed feeding behavior. While the neurons mediating this interaction could not be identified, one of the candidates, A-ci1, was shown to exhibit dynamic interactions with both the feeding and turn motor networks, potentially implicating it as an intermediary between feeding, turning, and swimming behaviors. Swimming had been previously demonstrated to elicit activity in the neuron. These findings were synthesized in an agent-based simulation, in which approach-avoidance foraging decisions were executed on the basis of appetitive state. This computational model faithfully reproduced experimental results and constitutes a core module of foraging-based decision-making onto which more complex behavioral functionalities could be grafted.
Issue Date:2015-01-21
URI:http://hdl.handle.net/2142/72767
Rights Information:Copyright 2014 Jeffrey William Brown
Date Available in IDEALS:2015-01-21
Date Deposited:2014-12


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