Abstract

Many cost-benefit decisions reduce to simple choices between approach or avoidance (or active disregard) to salient stimuli. Physiologically, critical factors in such decisions are modulators of the homeostatic neural networks that bias decision processes from moment to moment. For the predatory sea-slug Pleurobranchaea, serotonin (5-HT) is an intrinsic modulatory promoter of general arousal and feeding. We correlated 5-HT actions on appetitive state with its effects on the approach-avoidance decision in Pleurobranchaea. 5-HT and its precursor 5-hydroxytryptophan (5-HTP) augmented general arousal state and reduced feeding thresholds in intact animals. Moreover, 5-HT switched the turn response to chemosensory stimulation from avoidance to orienting in many animals. In isolated CNSs, bath application of 5-HT both stimulated activity in the feeding motor network and switched the fictive turn response to unilateral sensory nerve stimulation from avoidance to orienting. Previously, it was shown that increasing excitation state of the feeding network reversibly switched the turn motor network response from avoidance to orienting, and that 5-HT levels vary inversely with nutritional state. A simple model posits a critical role for 5-HT in control of the turn network response by corollary output of the feeding network. In it, 5-HT acts as an intrinsic neuromodulatory factor coupled to nutritional status and regulates approach-avoidance via the excitation state of the feeding network. Thus, the neuromodulator is a key organizing element in behavioral choice of approach or avoidance through its actions in promoting appetitive state, in large part via the homeostatic feeding network.

Highlights

  • Major decisions in foraging behavior concern the approach or avoidance of salient stimuli in the environment

  • We addressed how 5-hydroxytryptamine creatine sulfate (5-HT) might influence the choice of approach-avoidance in behavioral choice of intact animals and in the fictive turn responses of their isolated CNSs

  • Readiness-to-feed here is quantified in terms of feeding thresholds measured as the minimal concentrations of appetitive stimuli to elicit proboscis extension and active biting

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Summary

Introduction

Major decisions in foraging behavior concern the approach or avoidance of salient stimuli in the environment. Such decisions are generally made on a cost-benefit basis where decision is informed by the moment-to-moment integration of sensation, internal state and memory. The opisthobranch and pulmonate gastropod molluscs offer model organisms in which the neuromodulatory players in arousal and appetitive state can be addressed directly For these molluscs serotonin (5-HT) is the most prominent neuromodulator yet found to affect arousal and appetitive state through its stimulatory effects on behavior and neural activity when applied to intact animals or to the isolated CNS [1,2,3,4]. Palovcik et al [5] showed that injected 5-HT promoted arousal and appetitive state in terms of general activity and reduced sensory thresholds and latencies for eliciting feeding behaviors in the predatory sea-slug Pleurobranchaea. 5-HT is a central, and possibly the main, neuromodulatory factor regulating arousal and appetitive state through its likely roles in mediating circadian activity rhythms [6,7] and satiation [8]

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