Operant Conditioning in Honey Bees (Apis mellifera L.): The Cap Pushing Response

Abstract

The honey bee has been an important model organism for studying learning and memory. More recently, the honey bee has become a valuable model to understand perception and cognition. However, the techniques used to explore psychological phenomena in honey bees have been limited to only a few primary methodologies such as the proboscis extension reflex, sting extension reflex, and free flying target discrimination-tasks. Methods to explore operant conditioning in bees and other invertebrates are not as varied as with vertebrates. This may be due to the availability of a suitable response requirement. In this manuscript we offer a new method to explore operant conditioning in honey bees: the cap pushing response (CPR). We used the CPR to test for difference in learning curves between novel auto-shaping and more traditional explicit-shaping. The CPR protocol requires bees to exhibit a novel behavior by pushing a cap to uncover a food source. Using the CPR protocol we tested the effects of both explicit-shaping and auto-shaping techniques on operant conditioning. The goodness of fit and lack of fit of these data to the Rescorla-Wagner learning-curve model, widely used in classical conditioning studies, was tested. The model fit well to both control and explicit-shaping results, but only for a limited number of trials. Learning ceased rather than continuing to asymptotically approach the physiological most accurate possible. Rate of learning differed between shaped and control bee treatments. Learning rate was about 3 times faster for shaped bees, but for all measures of proficiency control and shaped bees reached the same level. Auto-shaped bees showed one-trial learning rather than the asymptotic approach to a maximal efficiency. However, in terms of return-time, the auto-shaped bees’ learning did not carry over to the covered-well test treatments.

Cognitive Aspects of Comb-Building in the Honeybee?

“…This behavioral complexity has often been dismissed as ‘just instinct.’ Yet, recent discoveries in insect learning, memory and cognition have generated a profound change in the perception of the behavioral flexibility of several species. For example, bees learn from past experiences to improve motor skills ( Mirwan et al, 2015 ; Abramson et al, 2016 ). Such operant learning is distinguished from cognitive operations, where, for example, bees are also able to combine multiple experiences (acquired in separate learning trials) to form simple rules and concepts ( Giurfa et al, 2001 ; Avargues-Weber et al, 2012 ) and display counting-like abilities ( Howard et al, 2018 ; Skorupski et al, 2018 ), and ants and bumblebees show simple forms of tool use ( Loukola et al, 2017 ; Maák et al, 2017 ).…”

Bumblebees show cognitive flexibility by improving on an observed complex behavior

“…Insects have been trained on complex behaviors such as pushing a cap (14), rotating a lever (15), and pulling a string (16) to gain a reward. Although these works have added to our understanding of operant conditioning, such behaviors required shaping with simple associations, in which subjects are trained on a series of tasks that increase in difficulty (17).…”

“…Previous works also trained bees on tasks that relied on local and stimulus enhancement to solve the task (14)(15)(16). In our current work, on most successful trials, bees used the closest ball instead of the furthest ball (which they had seen the demonstrator moving) and in the generalization test used a differently colored ball than previously encountered, suggesting that bees did Fig.…”

Conspecific and interspecific stimuli reduce initial performance in an aversive learning task in honey bees (Apis mellifera)

“…In appetitive experiments, bees either learn to associate neutral stimuli with desirable events, or learn to alter their behavior to produce a pleasant outcome. The proboscis extension response conditioning procedure has long been used to study appetitive conditioning in controlled laboratory conditions [18][19][20][21], while other methods use free-flying, foraging bees when ecological validity is of greater importance [22,23]. Research using these methods has produced a number of findings related to topics such as visual and olfactory sensation [24][25][26], perception of time [27], conditioned taste aversion [28], learning of abstract concepts [29,30], quantity discrimination [31,32], and the neurophysiology of memory [33][34][35].…”