Mushroom body extrinsic neurons in the honeybee (Apis mellifera) brain integrate context and cue values upon attentional stimulus selection.

Abstract

Multimodal GABA-immunoreactive feedback neurons in the honeybee brain connecting the output region of the mushroom body with its input are expected to tune the input to the mushroom body in an experience-dependent way. These neurons are known to change their rate responses to learned olfactory stimuli. In this work we ask whether these neurons also transmit learned attentional effects during multisensory integration. We find that a visual context and an olfactory cue change the rate responses of these neurons after learning according to the associated values of both context and cue. The learned visual context promotes attentional response selection by enhancing olfactory stimulus valuation at both the behavioral and the neural level. During a rewarded visual context, bees reacted faster and more reliably to a rewarded odor. We interpreted this as the result of the observed enhanced neural discharge toward the odor. An unrewarded context reduced already low rate responses to the unrewarded odor. In addition to stimulus valuation, these feedback neurons generate a neural error signal after an incorrect behavioral response. This might act as a learning signal in feedback neurons. All of these effects were exclusively found in trials in which the animal prepares for a motor response that happens during attentional stimulus selection. We discuss possible implications of the results for the feedback connections of the mushroom body.