Implication of dopaminergic modulation in operant reward learning and the induction of compulsive-like feeding behavior inAplysia

Abstract

Feeding in Aplysia provides an amenable model system for analyzing the neuronal substrates of motivated behavior and its adaptability by associative reward learning and neuromodulation. Among such learning processes, appetitive operant conditioning that leads to a compulsive-like expression of feeding actions is known to be associated with changes in the membrane properties and electrical coupling of essential action-initiating B63 neurons in the buccal central pattern generator (CPG). Moreover, the food-reward signal for this learning is conveyed in the esophageal nerve (En), an input nerve rich in dopamine-containing fibers. Here, to investigate whether dopamine (DA) is involved in this learning-induced plasticity, we used an in vitro analog of operant conditioning in which electrical stimulation of En substituted the contingent reinforcement of biting movements in vivo. Our data indicate that contingent En stimulation does, indeed, replicate the operant learning-induced changes in CPG output and the underlying membrane and synaptic properties of B63. Significantly, moreover, this network and cellular plasticity was blocked when the input nerve was stimulated in the presence of the DA receptor antagonist cis-flupenthixol. These results therefore suggest that En-derived dopaminergic modulation of CPG circuitry contributes to the operant reward-dependent emergence of a compulsive-like expression of Aplysia's feeding behavior.

Frank Beach Award Winner: Steroids as neuromodulators of brain circuits and behavior

“…This role for dopamine is not exclusively a vertebrate phenomenon. Many invertebrate organisms like Aplysia exhibit environmentally-contingent dopamine release that is involved in learning-induced plasticity via specific actions on a motor CPG (Bedecarrats et al, 2013). Therefore, one key feature of neuromodulators is that they can change the information content of a network, providing instructive signals and/or feedback inputs to influence ongoing circuit computations.…”

Localization of tyrosine hydroxylase‐like immunoreactivity in the nervous systems of Biomphalaria glabrata and Biomphalaria alexandrina, intermediate hosts for schistosomiasis

“…While the modality of peripheral dopaminergic neurons remains uncertain, they are generally associated with cephalic sensory organs (CSOs) that mediate contact chemoreception and mechanoreception (Salimova et al, 1987;Croll et al, 2003;Wyeth and Croll, 2011). Peripheral dopaminergic neurons project to the CNS where their synaptic actions can influence the expression of behavior (Nargeot et al, 1999;Mart ınez-Rubio et al, 2009;Wyeth and Croll, 2011;B ed ecarrats et al, 2013).…”

Commentary: New Insights in Anorexia Nervosa

“…To meet the challenge of starvation, animals have developed efficient foraging strategies that are mediated by dopamine (Stephens and Krebs, 1986; Faure et al, 2008; O'Connell and Hofmann, 2011; Richard and Berridge, 2011; McCue, 2012; Bédécarrats et al, 2013; Moe et al, 2014; Søvik et al, 2014; Masek et al, 2015). Moreover, hunger hormones influence how animals relate to environmental food cues by acting on dopamine neurons (Cone et al, 2015).…”