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

Abstract

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.

Involvement of phosphorylated Apis mellifera CREB in gating a honeybee's behavioral response to an external stimulus

“…Similar results were obtained in rats, where the CS acquires excitatory and inhibitory properties during unpaired training (Droungas and LoLordo 1994). A CS with "mixed" properties has also been reported during backward conditioning in honeybee and vertebrates (Williams and Overmier 1988;Felsenberg et al 2013) indicating that two opposing properties of a CS are learned whenever the CS' meaning is ambiguous during training.…”

Reinforcement signaling of punishment versus relief in fruit flies

“…S1 for a meta-analysis of fly data). Likewise, cues that are learned as predictors for a reward versus its termination are, respectively, acted upon appetitively versus aversively (Hellstern et al 1998;Felsenberg et al 2013).…”

Pain-relief learning in flies, rats, and man: basic research and applied perspectives

“…1) (we use "relief" to refer specifically to the acute effects of punishment offset; an equally legitimate yet broader use of the word in, e.g., "fear relief," encompasses any process that eases fear [Riebe et al 2012]). Indeed, in experimental settings, it turns out that stimuli experienced before and during a punishing episode are later avoided as they signal upcoming punishment, whereas stimuli experienced after a painful episode can subsequently prompt approach behavior, arguably (Box 1) because of their association with the relieving cessation of pain (Konorski 1948;Smith and Buchanan 1954;Wolpe and Lazarus 1966;Zanna et al 1970;Solomon and Corbit 1974;Schull 1979;Solomon 1980;Wagner 1981;Walasek et al 1995;Tanimoto et al 2004;Yarali et al 2008Yarali et al , 2009bAndreatta et al 2010Andreatta et al , 2012Yarali and Gerber 2010;Ilango et al 2012;Navratilova et al 2012;Diegelmann et al 2013b); for a corresponding finding in the appetitive domain, see Hellstern et al (1998) and Felsenberg et al (2013). Such relief can both support the learning of the cues associated with the disappearance of the threat and reinforce those behaviors that helped to escape it.…”