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The AIB interneurons are modulated by excitatory and inhibitory signaling pathways to shape aversive behaviors in response to 1-octanol

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2015, Doctor of Philosophy, University of Toledo, Biology (Cell-Molecular Biology).
Dysfunctional integration of sensory information is associated with numerous pathological conditions in the human nervous system, including autism spectrum disorders, attention deficit hyperactivity disorder (ADHD), and schizophrenia. In the model organism Caenorhabditis elegans, the noxious odorant 1-octanol is primarily sensed by the ASH sensory neurons, and presentation of the odorant causes animals to initiate an aversive response that is modulated by the presence of food or serotonin (5- HT). However, in the present study we found that presentation of 1-octanol to animals activates, inhibits, and has no effect on the glutamatergic ASH, AWC, and ASE right (ASER) sensory neurons, respectively. The ASHs, AWCs, and ASER all synapse onto a common postsynaptic pair of interneurons, the AIB interneurons. The AIB interneurons profoundly affect animal behavior. Based on indirect evidence, the leading hypothesis states that some of the upstream glutamatergic sensory neurons signal onto the AIBs through receptors containing the AMPA-type subunit GLR- 1. Using whole-cell patch clamp electrophysiology and calcium imaging, we found that glutamate evokes both an anionic current mediated by the glutamate-gated Cl- (GluCl) channel subunit AVR-14, and a cationic GLR-1-dependent current in the AIBs. Similarly, previous work has shown that tonic glutamate release from the AWCs and ASER onto GLR-1 and AVR-14 on the AIBs, respectively, differentially modulate 1- octanol-evoked aversive behaviors. Additionally, the L-type voltage-gated calcium channel (VGCC) subunit EGL-19 amplifies glutamate-evoked increases in AIB intracellular Ca2+ (iCa2+). In addition to glutamate, acetylcholine also evokes an inhibitory current in the AIBs that is partially mediated by the acetylcholine-gated Cl- (AChCl) channel subunit ACC-1. Interestingly, the AIA interneurons are cholinergic, direct much of their synaptic output onto the AIBs, are thought to inhibit the AIBs, and are also innervated by the ASHs, AWCs, and ASER. In order to correlate neuronal activity with animal behavior, we used calcium imaging to investigate the effects of the noxious odorant 1-octanol the AIAs and AIBs. Presentation of 1-octanol activates and inhibits the AIA and AIB interneurons, respectively, and odorant inhibition of the AIBs is partially dependent on both AVR-14 and cholinergic transmission from the AIAs. Together, these data demonstrate how multiple signaling pathways modulate a pair of interneurons to differentially shape animal behavior.
Bruce Bamber, PhD (Committee Chair)
Richard Komuniecki, PhD (Committee Member)
Robert Steven, PhD (Committee Member)
Guofa Liu, PhD (Committee Member)
Scott Molitor, PhD (Committee Member)
John Bellizzi, PhD (Committee Member)
158 p.

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Citations

  • Layne, R. M. (2015). The AIB interneurons are modulated by excitatory and inhibitory signaling pathways to shape aversive behaviors in response to 1-octanol [Doctoral dissertation, University of Toledo]. OhioLINK Electronic Theses and Dissertations Center. http://rave.ohiolink.edu/etdc/view?acc_num=toledo1445452178

    APA Style (7th edition)

  • Layne, Robert. The AIB interneurons are modulated by excitatory and inhibitory signaling pathways to shape aversive behaviors in response to 1-octanol. 2015. University of Toledo, Doctoral dissertation. OhioLINK Electronic Theses and Dissertations Center, http://rave.ohiolink.edu/etdc/view?acc_num=toledo1445452178.

    MLA Style (8th edition)

  • Layne, Robert. "The AIB interneurons are modulated by excitatory and inhibitory signaling pathways to shape aversive behaviors in response to 1-octanol." Doctoral dissertation, University of Toledo, 2015. http://rave.ohiolink.edu/etdc/view?acc_num=toledo1445452178

    Chicago Manual of Style (17th edition)