Rapid learning dynamics in individual honeybees during classical conditioning

Abstract

Associative learning in insects has been studied extensively by a multitude of classical conditioning protocols. However, so far little emphasis has been put on the dynamics of learning in individuals. The honeybee is a well-established animal model for learning and memory. We here studied associative learning as expressed in individual behavior based on a large collection of data on olfactory classical conditioning (25 datasets, 3298 animals). We show that the group-averaged learning curve and memory retention score confound three attributes of individual learning: the ability or inability to learn a given task, the generally fast acquisition of a conditioned response (CR) in learners, and the high stability of the CR during consecutive training and memory retention trials. We reassessed the prevailing view that more training results in better memory performance and found that 24 h memory retention can be indistinguishable after single-trial and multiple-trial conditioning in individuals. We explain how inter-individual differences in learning can be accommodated within the Rescorla–Wagner theory of associative learning. In both data-analysis and modeling we demonstrate how the conflict between population-level and single-animal perspectives on learning and memory can be disentangled.

Automated tracking and analysis of behavior in restrained insects

“…This stable behavioral performance in individual bees is typical: once bees start responding during training they continue to respond (Pamir et al, 2011(Pamir et al, , 2014. However, it is currently unclear whether this abrupt behavioral performance change reflects abrupt learning or whether learning is a more gradual process (Gallistel et al, 2004;Pamir et al, 2011Pamir et al, , 2014. In fact, this abrupt behavioral performance change might be due to the binary monitor of the proboscis extension response which does not allow monitoring gradual changes in behavior.…”

“…To give another example: The observation that once having responded for the first time, honey bees continue to respond with a high probability during training and memory test could suggest that learning results in abrupt performance changes (Pamir et al, 2011(Pamir et al, , 2014. However, learning related gradual changes might exist, and might have been masked by the binary behavioral read out.…”

“…During the test it responded to the trained but not to the novel odor, indicating that it formed an odor specific associative odor-sugar memory. This stable behavioral performance in individual bees is typical: once bees start responding during training they continue to respond (Pamir et al, 2011(Pamir et al, , 2014. However, it is currently unclear whether this abrupt behavioral performance change reflects abrupt learning or whether learning is a more gradual process (Gallistel et al, 2004;Pamir et al, 2011Pamir et al, , 2014.…”

“…For example, the common experimental procedure of pooling binary performance measures of groups of identically treated animals often confounds the interpretation of behavioral data, as the group average is not representative for all individuals (Gallistel et al, 2004;Pamir et al, 2011Pamir et al, , 2014. Our approach helps to overcome this problem, as it allows the analysis of graded behavior in individuals.…”

“…Up to now learning and memory have been mainly assessed by a crude all-or-nothing measure (whether a bee reacts to a learned stimulus, or not). This binary measurement is not suited to reveal individual differences in learning and memory performance, for this purpose a graded performance measurement is required (Pamir et al, 2014).…”