Backward inhibitory learning in honeybees: A behavioral analysis of reinforcement processing

One class of theoretical accounts of associative learning suggests that reinforcers are processed according to learning rules that minimize the predictive error between the expected strength of future reinforcement and its actual strength. The omission of reinforcement in a situation where it is expected leads to inhibitory learning of stimuli indicative for such a violation of the prediction. There are, however, results indicating that inhibitory learning can also be induced by other mechanisms. Here, we present data from olfactory reward conditioning in honeybees that show that (1) one- and multiple-trial backward conditioning results in conditioned inhibition (CI); (2) the inhibition is maximal for a 15-sec interval between US and CS; (3) there is a nonmonotonic dependency on the degree of CI from the US-CS interval during backward pairing; and (4) the prior association of context stimuli with reinforcement is not necessary for the development of CI. These results cannot be explained by models that only minimize a prediction error. Rather, they are consistent with models of associative learning that, in addition, assume that learning depends on the temporal overlap of a CS with two processes, a fast excitatory and a slow inhibitory one, both evoked by a reinforcer. The findings from this behavioral analysis of reinforcement processing are compared with the known properties of an individual, identified neuron involved in reinforcement processing in the bee brain, to further understand the mechanisms underlying predictive reward learning.