Reinforcement Expectation in the Honey Bee (Apis mellifera): Can Downshifts in Reinforcement Show Conditioned Inhibition?

Abstract

When animals learn the association of a Conditioned Stimulus with an Unconditioned Stimulus, later presentation of the CS invokes a representation of the US. When the expected US fails to occur, theoretical accounts predict that conditioned inhibition can accrue to any other stimuli that are associated with this change in the US. Empirical work with mammals has confirmed the existence of conditioned inhibition. But the way it is manifested, the conditions that produce it, and determining whether it is the opposite of excitatory conditioning, are important considerations. Invertebrates can make valuable contributions to this literature because of the well-established conditioning protocols and access to the central nervous system for studying neural underpinnings of behavior. Nevertheless, conditioned inhibition has yet to be conclusively demonstrated in invertebrates. Here we evaluate the role of the unconditioned stimulus (US) in producing conditioned inhibition by using Proboscis Extension Response conditioning of the honey bee (Apis mellifera). Specifically, using variations of a feature-negative experimental design, we employ downshifts in US intensity relative to US intensity used during initial excitatory conditioning, to show that an odorant in an odor-odor mixture can become a conditioned inhibitor. We argue that alternative interpretations to conditioned inhibition are unlikely. However, we show variation across individuals in how strongly they show Conditioned Inhibition, with some individuals possibly revealing a different means of learning about changes in reinforcement. We discuss how more work can reveal more details of conditioned inhibition, how it can be extended to investigate how it is encoded in the CNS, and how the work can generalize to other insect models. On particular, work like this will be important as more is revealed of the complexity of the insect brain from connectome projects.

Cognitive limits of larvalDrosophila: testing for conditioned inhibition, sensory preconditioning, and second-order conditioning

“…We provide evidence for conditioned inhibition in larval Drosophila, corresponding to what has been reported in adult flies (Barth et al 2014;Jacob and Waddell 2020) and honeybees (Takeda 1961;Bitterman et al 1983;Hellstern et al 1998;Chandra et al 2010;Matsumoto et al 2012;Mahoney et al 2024). However, our data do not provide evidence for sensory preconditioning or second-order conditioning in larval Drosophila.…”