Forward and backward second-order Pavlovian conditioning in honeybees

Abstract

Second-order conditioning (SOC) is the association of a neutral stimulus with another stimulus that had previously been combined with an unconditioned stimulus (US). We used classical conditioning of the proboscis extension response (PER) in honeybees (Apis mellifera) with odors (CS) and sugar (US). Previous SOC experiments in bees were inconclusive, and, therefore, we attempted to demonstrate SOC in the following three experiments: (Experiment 1) After differential conditioning (pairing odor A with US and presenting odor B without US), the bees experienced two pairs of partially overlapping odors, either a new odor C followed by a previously reinforced odor A (C-A) or a new odor C followed by a previously nonreinforced odor B (C-B). (Experiment 2) After differential conditioning, bees were presented with C-A or A-C. (Experiment 3) Bees were first presented with C-A or A-C before differential conditioning and were tested with odor C. We observed: (Experiment 1) 40% of the bees showed PER to the C-A presentation, but only 20% showed PER to the C-B presentation. (Experiment 2) 40% of the bees showed PER to the C-A presentation, while only 20% showed PER to the reversed sequence A-C. Experiments 1 and 2 showed that a previously reinforced odor can be a secondary reinforcer for excitatory SOC only with forward-pairing. (Experiment 3) PER toward C was lower (15%) in bees presented with A-C than with C-A (25%). This showed that backward SOC is not as effective as forward SOC. These results help to delineate different conditions that are critical for the phenomenon of SOC.

Differential conditioning and long-term olfactory memory in individual Camponotus fellah ants

“…A similar phenomenon may be occurring in the Y-maze, thus leading the ants to prefer the CS-to the novel odorant. Second-order conditioning has been shown in honeybees both in the olfactory (Bitterman et al, 1983;Menzel, 1990;Hussaini et al, 2007) and visual modality (Grossmann, 1971), thus making this explanation plausible. In any case, the CS-would always be less attractive than the CS+, given the close connection (spatial and temporal) between the sucrose reward and the CS+.…”

Revisiting olfactory classical conditioning of the proboscis extension response in honey bees: A step toward standardized procedures

“…Many PER conditioning variants have been used to study perception, learning and memory in bees: blocking (Smith and Cobey, 1994;Hosler and Smith, 2000;Guerrieri et al, 2005a), overshadowing (Smith, 1998), second-order conditioning (Hussaini et al, 2007), reversal learning (Komischke et al, 2002;Devaud et al, 2007;Mota and Giurfa, 2010), sensory preconditioning (Müller et al, 2000), latent inhibition (Chandra et al, 2000(Chandra et al, , 2010Fernández et al, 2009), and negative and positive patterning (Deisig et al, 2001(Deisig et al, , 2002(Deisig et al, , 2003 are just some examples of a battery of protocols that have been adapted to bees and that implied establishing appropriate conditioning schedules and controls. Despite the apparent complexity of some of these protocols, we are confident that the basic procedures explained in this article will help researchers to perform these protocols and design still other variants of PER conditioning.…”

Acute ethanol ingestion impairs appetitive olfactory learning and odor discrimination in the honey bee

“…Honey bees can perform sophisticated learning tasks previously thought to be the exclusive domain of vertebrates such as delayed match-to-sample learning (Giurfa, Zhang, Jenett, Menzel, & Srinivasan, 2001), second order learning (Hussaini, Komischke, Menzel, & Lachnit, 2007), stimulus classification (Stach, Benard, & Giurfa, 2004; Wright, Kottcamp, & Thomson, 2008), blocking (Hosler & Smith, 2000), and contextual learning (Gerber & Menzel, 2000). Furthermore, an atlas of the honey bee brain has been developed (http://www.neurobiologie.fu-berlin.de/beebrain/), its genome has been sequenced (Honeybee Genome Sequencing Consortium, 2006), and the molecular mechanisms of learning and memory in honey bees have been well-studied (Eisenhardt, 2006; Müller, 2002).…”