Minimal circuit motifs for second-order conditioning in the insect mushroom body

Abstract

In well-established first-order conditioning experiments, the concurrence of a sensory cue with reinforcement forms an association, allowing the cue to predict future reinforcement. Once a sensory cue is established as a predictor, it can also serve as indirect reinforcement, a phenomenon referred to as second-order conditioning. In the insect mushroom body, such associations are encoded in the plasticity of the synapses between the intrinsic and output neurons of the mushroom body, a process mediated by the activity of dopaminergic neurons that encode reinforcement signals. In second-order conditioning, a new sensory cue is paired with an already established one that presumably activates dopaminergic neurons due to its predictive power of the reinforcement. We explore minimal circuit motifs in the mushroom body for their ability to support second-order conditioning. We found that dopaminergic neurons can either be activated directly by the mushroom bodys intrinsic neurons or via feedback from the output neurons via several pathways. We demonstrate that the circuit motifs differ in their computational efficiency and robustness and suggest a particular motif that relies on feedforward input of the mushroom body intrinsic neurons to dopaminergic neurons as a promising additional candidate for experimental evaluation. It differentiates well between trained and novel stimuli, demonstrating robust performance across a range of model parameters.