The evolution of honey bee dance communication: a mechanistic perspective.

Honey bee dance has been intensively studied as a communication system, and yet we still know very little about the neurobiological mechanisms supporting how dances are produced and interpreted. Here, we discuss how new information on the functions of the central complex (CX) of the insect brain might shed some light on possible neural mechanisms of dance behaviour. We summarise the features of dance communication across the species of the genus Apis We then propose that neural mechanisms of orientation and spatial processing found to be supported by the CX may function in dance communication also, and that this mechanistic link could explain some specific features of the dance form. This is purely a hypothesis, but in proposing this hypothesis, and how it might be investigated, we hope to stimulate new mechanistic analyses of dance communication.

Differences in long-term memory stability and AmCREB level between forward and backward conditioned honeybees (Apis mellifera).

In classical conditioning a predictive relationship between a neutral stimulus (conditioned stimulus; CS) and a meaningful stimulus (unconditioned stimulus; US) is learned when the CS precedes the US. In backward conditioning the sequence of the stimuli is reversed. In this situation animals might learn that the CS signals the end or the absence of the US. In honeybees 30 min and 24 h following backward conditioning a memory for the excitatory and inhibitory properties of the CS could be retrieved, but it remains unclear whether a late long-term memory is formed that can be retrieved 72 h following backward conditioning. Here we examine this question by studying late long-term memory formation in forward and backward conditioning of the proboscis extension response (PER). We report a difference in the stability of memory formed upon forward and backward conditioning with the same number of conditioning trials. We demonstrate a transcription-dependent memory 72 h after forward conditioning but do not observe a 72 h memory after backward conditioning. Moreover we find that protein degradation is differentially involved in memory formation following these two conditioning protocols. We report differences in the level of a transcription factor, the cAMP response element binding protein (CREB) known to induce transcription underlying long-term memory formation, following forward and backward conditioning. Our results suggest that these alterations in CREB levels might be regulated by the proteasome. We propose that the differences observed are due to the sequence of stimulus presentation between forward and backward conditioning and not to differences in the strength of the association of both stimuli.

Short- and long-term memories formed upon backward conditioning in honeybees (Apis mellifera).

In classical conditioning, the temporal sequence of stimulus presentations is critical for the association between the conditioned stimulus (CS) and the unconditioned stimulus (US). In forward conditioning, the CS precedes the US and is learned as a predictor for the US. Thus it acquires properties to elicit a behavioral response, defined as excitatory properties. In backward conditioning, the US precedes the CS. The CS might be learned as a predictor for the cessation of the US acquiring inhibitory properties that inhibit a behavioral response. Interestingly, behavior after backward conditioning is controlled by both excitatory and inhibitory properties of the CS, but the underlying mechanisms determining which of these opposing properties control behavior upon retrieval is poorly understood. We performed conditioning experiments in the honeybee (Apis mellifera) to investigate the CS properties that control behavior at different time points after backward conditioning. The CS properties, as characterized by the retardation or enhancement of subsequent acquisition, were examined 30 min and 24 h after backward conditioning. We found that 30 min after backward conditioning, the CS acquired an inhibitory property during backward conditioning depending on the intertrial interval, the number of trials, and the odor used as the CS. One day after backward conditioning, we observed significant retardation of acquisition. In addition, we demonstrated an enhanced, generalized odor response in the backward conditioned group compared to untreated animals. These results indicate that two long-lasting opposing memories have been formed in parallel: one about the excitatory properties of the CS and one about the inhibitory properties of the CS.

Reinstatement in honeybees is context-dependent.

During extinction animals experience that the previously learned association between a conditioned stimulus (CS) and an unconditioned stimulus (US) no longer holds true. Accordingly, the conditioned response (CR) to the CS decreases. This decrease of the CR can be reversed by presentation of the US alone following extinction, a phenomenon termed reinstatement. Reinstatement and two additional phenomena, spontaneous recovery and renewal, indicate that the original CS-US association is not lost through extinction but can be reactivated through different processes. In honeybees (Apis mellifera), spontaneous recovery, i.e., the time-dependent return of the CR, has been demonstrated, suggesting that also in these insects the original CS-US association is not lost during extinction. To support this notion, we ask whether honeybees show reinstatement after extinction. In vertebrates reinstatement is context-dependent, so we examined whether the same holds true for honeybees. We demonstrate reinstatement in restrained honeybees and show that reinstatement is context-dependent. Furthermore, we show that an alteration of the color of light illuminating the experimental setup suffices to indicate a contextual change. We conclude that in honeybees the initially formed CS-US memory is not lost after extinction. Rather, honeybees might learn about the context during extinction. This enables them to adequately retrieve one of the two opposing memories about the CS that have been formed after extinction.