Abstract
In natural environments, stimuli and events learned by animals usually occur in a combination of more than one sensory modality. An important problem in experimental psychology has been thus to understand how organisms learn about multimodal compounds and how they discriminate this compounds from their unimodal constituents. Here we tested the ability of honey bees to learn bimodal patterning discriminations in which a visual-olfactory compound (AB) should be differentiated from its visual (A) and olfactory (B) elements. We found that harnessed bees trained in classical conditioning of the proboscis extension reflex (PER) are able to solve bimodal positive and negative patterning (NP) tasks. In positive patterning (PP), bees learned to respond significantly more to a bimodal reinforced compound (AB+) than to non-reinforced presentations of single visual (A-) or olfactory (B-) elements. In NP, bees learned to suppress their responses to a non-reinforced compound (AB-) and increase their responses to reinforced presentations of visual (A+) or olfactory (B+) elements alone. We compared the effect of two different inter-trial intervals (ITI) in our conditioning approaches. Whereas an ITI of 8 min allowed solving both PP and NP, only PP could be solved with a shorter ITI of 3 min. In all successful cases of bimodal PP and NP, bees were still able to discriminate between reinforced and non-reinforced stimuli in memory tests performed one hour after conditioning. The analysis of individual performances in PP and NP revealed that different learning strategies emerged in distinct individuals. Both in PP and NP, high levels of generalization were found between elements and compound at the individual level, suggesting a similar difficulty for bees to solve these bimodal patterning tasks. We discuss our results in light of elemental and configural learning theories that may support the strategies adopted by honey bees to solve bimodal PP or NP discriminations.
Highlights
Living in a complex world demands learning and memory of relationships between diverse stimuli in the environment
Honeybees trained to discriminate a visual element (A−) and an olfactory element (B−) from its bimodal compound (AB+) in a positive patterning (PP) protocol with an inter-trial intervals (ITI) of 3 min were successful in learning the task
Global performances significantly differed between all stimuli (Tukey test; stimulus effect; A− vs. B− and A− vs. AB+: p < 0.001; B− vs. AB+: p < 0.05), no differences were found in responses to A− and B− at the last trial of conditioning (Tukey test; stimulus × trial 10 effect; A− vs. B−: NS)
Summary
Living in a complex world demands learning and memory of relationships between diverse stimuli in the environment. Natural environments are composed by multimodal stimuli and animals usually associate these compounds with an US, rather than single unimodal elements (Lorenz, 1951). Several studies indicated a synergistic effect between color and odor within a bimodal compound, so that combined colorodor cues led to better learning and memory compared with unimodal cues (Kunze and Gumbert, 2001; Reinhard et al, 2004, 2006; Kulahci et al, 2008). It is difficult to interpret bees’ performance, given that sequential rather than simultaneous stimulus processing may occur during the approach to the target (Mota et al, 2011) These two scenarios, sequential versus simultaneous stimulus processing, may determine dramatic differences in performance, such as those supporting synergistic versus inhibitory withincompound processing
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