Characterization of the neuronal circuits and peptides underlying behavior in nudipleuran sea slugs and Octopus rubescens

Lee, Colin

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https://hdl.handle.net/2142/115311 Copy

Description

Title

Characterization of the neuronal circuits and peptides underlying behavior in nudipleuran sea slugs and Octopus rubescens

Author(s)

Lee, Colin

Issue Date

2021-12-16

Director of Research (if dissertation) or Advisor (if thesis)

Gillette, Rhanor

Doctoral Committee Chair(s)

• Gillette, Rhanor
• Ssweedler, Jonathan V

Committee Member(s)

• Gillette, Martha U
• Southey, Bruce R

Department of Study

Neuroscience Program

Discipline

Neuroscience

Degree Granting Institution

University of Illinois at Urbana-Champaign

Degree Name

Ph.D.

Degree Level

Dissertation

Keyword(s)

Neuroethology, Mollusk

Abstract

Across the metazoa, several molluscan groups stand out as ideal models for the study of the brain. Heterobranch gastropods, with simple behaviors, a small number of neurons (~10,000), and large, spiking neuronal cell bodies, allow for detailed examination of the neuronal basis of behavior. The neuronal circuits of key behaviors have been defined at not only the level of single neurons, but the level of ion channels and neurotransmitters. These studies have provided critical insights into the fundamental principles of learning, central pattern generators, neurotransmission, and many other areas. In contrast, cephalopods, particularly octopuses, are prized for the complexity of their nervous systems. The cephalopod nervous system contains hundreds of millions of neurons, and cephalopods display advanced learning and cognitive abilities that are otherwise absent in invertebrates. The independent evolution of these traits has sparked considerable interest. How did cephalopods evolve a large, advanced nervous system, and what does this say about the fundamental nature of a “smart” animal? However, the cephalopod nervous system shares certain features with that of gastropods, and the basal mollusk likely resembled a gastropod. To what extent do cephalopods reflect this heritage? In this thesis, I explored these topics. In the first chapter, I used the sea slug Pleurobranchaea californica I examined the neuronal basis of crawling and its position in the behavioral hierarchy. Pleurobranchaea is a generalist predator that faces greater decision-making demands than most gastropods, and thus is an excellent model organism for the neuronal basis of decision-making. The neuronal basis of other behaviors and their interplay have been examined, so my work adds crawling to this model. I found that several neurons previously shown to drive turning and swimming also drive crawling, which suggests that they are general arousal elements for locomotion, and moreover that they are hierarchically assimilated into locomotor circuits. Additionally, I found that feeding inhibits these cells, providing a mechanism for the general inhibition of locomotion during feeding. The second chapter annotated the peptide prohormones and characterized the peptide profiles of homologous feeding interneurons in Pleurobranchaea and the nudibranch sea slugs Hermissenda crassicornis and Melibe leonina. Comparative research, particularly peptidomic research, is strongest when many species are included in the comparison, and this study expands the number of gastropods in which there is broad peptidomic information. Additionally, few homologous neurons have been chemically compared, in part due to the difficulty of reproducibly identifying single neurons in many species. By doing so here I help fill in this gap. I found that that each species’ version of the neuron contained peptides from the FMRFamide and SCP prohormone families, but also expressed other peptides not seen in the others. For the third and final experimental chapter I turned my focus to the octopus, and characterized the motor output of the buccal ganglion and stained for SCP in Octopus rubescens. My final main chapter reviewed satiation in gastropods. The first paper on this topic was published 47 years ago, and in the subsequent decades hundreds of papers have been published on this topic, covering all aspects of the phenomenon: behavioral changes that occur with satiation, the factors that reduce the motivation to feed, the neuronal basis of satiation, and the possible neurotransmitters involved in the effect. Despite this wealth of research, this topic has never been systematically reviewed. I did so here. In gastropods, satiation does not occur as feeding network inhibition, but rather feeding network reconfiguration. Stomach distention leads to inhibition of the network elements that drive ingestion and radular protraction, and excitation of the elements that drive egestion and radular retraction, effectively preventing feeding behavior. Feeding inhibition in gastropods is probabilistic, and I argued that this mechanism of inhibition, which preserves excitation in the feeding network, facilitates this probabilistic effect. Additionally, I examined the hypothesis that stomach distention is the only factor that regulates hunger in gastropods. I also performed several smaller studies that were not seen to completion, and contributed to the efforts of other students in the Sweedler and Martha Gillette labs. These studies are described in three supplementary chapters at the end of the thesis.

Graduation Semester

2022-05

Type of Resource

Thesis

Copyright and License Information

Copyright 2022 Colin Lee

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