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A neuronal switch for approach/avoidance in cost-benefit decision

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Title: A neuronal switch for approach/avoidance in cost-benefit decision
Author(s): Hirayama, Keiko
Director of Research: Gillette, Rhanor
Doctoral Committee Chair(s): Gillette, Rhanor
Doctoral Committee Member(s): Cox, Charles L.; Nelson, Mark; Sweedler, Jonathan
Department / Program: School of Molecular & Cell Bio
Discipline: Neuroscience
Degree Granting Institution: University of Illinois at Urbana-Champaign
Degree: Ph.D.
Genre: Dissertation
Subject(s): appetitive state decision-making goal-oriented behavior
Abstract: Animals make decisions by integrating their internal state, external sensory stimuli, and previous experiences. The neuronal bases of these decisions are accessible in the predatory sea- slug Pleurobranchaea, which has a very simple nervous system. Orienting and avoidance responses are dependent on the appetitive state, such that very hungry animals may attack noxious stimuli and satiated animals will avoid appetitive stimuli. A multifunctional turn network is active in response to the unilateral application of the stimulus, promoting the appropriate turn response. The goal of my study was to answer the following questions: 1) How does the nervous system encode the appetitive state of animal? 2) How does the animal’s appetitive state affect the turn network to drive approach or avoidance? 3) How does the turn network compute the orientation of the turn? We hypothesize that corollary outputs from the feeding network modulate the configuration of the premotor network that mediates turns, toggling the turn choice from avoidance to orienting. Consequently, electrophysiological recordings from the isolated central nervous system of animals demonstrated the conservation of donor appetitive state. As animal’s appetitive state (readiness to feed) was conserved in the fictive turning decisions of the isolated nervous system, and the decision to orient or avoid was a function of spontaneous rhythmic activity in the feeding motor network. In addition, manipulating the feeding network activity modified the fictive turn motor output in response to the unilateral sensory stimulus. Activation and suppression of the feeding network by driving feeding command neurons or stimulation of feeding nerve promoted approach and avoidance, respectively. Thus these results confirmed that the excitation state of the homeostatic feeding network manifested the animal’s readiness to feed and controlled expression of approach vs. avoidance turn response to the stimuli. A simple possible model suggested that corollary outputs from the feeding to the turn network changed the configuration of the premotor turn network and thereby switching the turn output. Electrophysiological observations were found to fit to this model. Bilaterally paired serotonergic neurons of the turn CPG network critical to turning output were asymmetrically active during turns appropriate to turn direction. These neurons, necessary for avoidance, were inhibited during fictive feeding, consistent with behavioral observations in intact animals. Bath addition of serotonin, an endogenous regulator of arousal and appetitive state, converted animal’s choice of turn response to the stimulus from avoidance to orienting. Serotonin was also found to excite the feeding network. Thus serotonin as a neuromodulator encodes the animal’s hunger state, and toggles animal’s turn decision by changing its internal state. These findings demonstrate the neuronal mechanisms of appetitive state dependence of behavioral choice processes. Results outline the framework for a simple neuronal circuit model for the cost benefit decision in approach/avoidance behavior, which could be applicable to the modeling of decision-making processes in more complex systems.
Issue Date: 2012-09-18
URI: http://hdl.handle.net/2142/34361
Rights Information: Copyright 2012 Keiko Hirayama
Date Available in IDEALS: 2012-09-18
Date Deposited: 2012-08
 

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