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Full text release has been delayed at the author's request until July 14, 2028

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Distinct Modulatory Actions Enable Network Neuron Recruitment and Regulation

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2023, Doctor of Philosophy, Miami University, Biology.
Neuronal networks that produce oscillations underlie rhythmic motor behaviors (e.g., walking, chewing, and breathing), and complex behaviors (e.g., memory formation, decision making, and sensory processing). Oscillatory networks are subject to neuromodulation, promoting network flexibility, and ultimately enabling individuals to adapt to changes in their environment. Network flexibility includes reconfiguration, such as neuronal switching, in which neurons can change participation from one network into another, or into two distinct networks simultaneously, in response to neuromodulation. While modulation of synapses is an identified mechanism for both recruitment and coordination of a switching neuron in a second network, it is unknown whether alternative mechanisms can be used. In this dissertation, I asked whether modulation of intrinsic membrane properties can serve as a mechanism for recruitment, while modulation of synapses enables coordination of switching neuron activity in a second network. To test this, I used the small, well-characterized feeding-related networks (pyloric [food filtering], ~1 Hz; gastric mill [food chewing], ~0.1 Hz) and identified modulatory inputs of the isolated stomatogastric nervous system of the crab, Cancer borealis. The modulatory projection neuron MCN5 releases the neuropeptide Gly1-SIFamide, which increases pyloric frequency, activates the gastric mill rhythm, and switches the pyloric-only LPG neuron into dual pyloric plus gastric mill-timed bursting. Using bath application of the Gly1-SIFamide peptide, plus photoinactivation to eliminate activity of select neurons, I mimicked MCN5-elicited pyloric and gastric mill network activity. Then, using current clamp electrophysiology techniques, I examined whether the LPG neuron switch into the gastric mill network occurs due to Gly1-SIFamide modulation of LPG intrinsic membrane properties, and whether LPG gastric mill-timed bursting is regulated by pyloric and gastric mill network neurons. Furthermore, I examined whether LPG is involved in regulating and coordinating the gastric mill rhythm. Finally, I used dual two-electrode voltage clamp recordings to determine whether synapses between LPG and gastric mill network neurons are modulated by Gly1-SIFamide for coordination among these neurons. Here, I identified a novel mechanism of neuronal switching, where intrinsic membrane properties are necessary for neuronal switching into a second network, while modulation of synapses is important for enabling regulation and coordination among switching and second network neurons. These findings indicate that separate mechanisms for recruitment and coordination offer an additional dimension of network flexibility, such that switching neuron activity is not constrained by second network synapses, and that coordination among network neurons is adaptable and can vary independent of switching neuron endogenous bursting.
Dawn Blitz (Advisor)
Kathleen Killian (Committee Member)
Anna Radke (Committee Member)
Joseph Ransdell (Committee Member)
Paul James (Committee Member)
259 p.

Recommended Citations

Citations

  • Fahoum, S.-R. H. (2023). Distinct Modulatory Actions Enable Network Neuron Recruitment and Regulation [Doctoral dissertation, Miami University]. OhioLINK Electronic Theses and Dissertations Center. http://rave.ohiolink.edu/etdc/view?acc_num=miami1689163371215407

    APA Style (7th edition)

  • Fahoum, Savanna-Rae. Distinct Modulatory Actions Enable Network Neuron Recruitment and Regulation. 2023. Miami University, Doctoral dissertation. OhioLINK Electronic Theses and Dissertations Center, http://rave.ohiolink.edu/etdc/view?acc_num=miami1689163371215407.

    MLA Style (8th edition)

  • Fahoum, Savanna-Rae. "Distinct Modulatory Actions Enable Network Neuron Recruitment and Regulation." Doctoral dissertation, Miami University, 2023. http://rave.ohiolink.edu/etdc/view?acc_num=miami1689163371215407

    Chicago Manual of Style (17th edition)