One retrieval trial induces reconsolidation in an appetitive learning paradigm in honeybees (Apis mellifera)

Combining memory retrieval with the application of a protein synthesis-inhibitor leads to an amnestic effect that is referred to as the reconsolidation phenomenon. Several behavioural studies demonstrate that only a few or weak retrieval trials (that do not result in significant extinction) lead to this phenomenon. In contrast, many trials (that result in significant extinction) combined with a protein synthesis inhibitor result in an inhibition of the extinction memory. Based on these findings it was suggested that extinction is the boundary condition for reconsolidation: when extinction is induced the consolidation of the extinction memory is the dominant process. Recently we were not able to confirm this hypothesis in the honeybee (Apis mellifera): We did not find the reconsolidation phenomenon after one retrieval trial, but demonstrated reconsolidation after five retrieval trials that led to extinction. To exclude that this observation resembles a special case in insects we here wanted to know if one retrieval trial induces reconsolidation as it has been demonstrated before in many other species. To do so we used experimental parameters that had been used before to demonstrate consolidation in the honeybee with the exception that this time the protein synthesis-inhibitor was applied 1 h after one memory retrieval instead after acquisition. We thereby demonstrate the reconsolidation phenomenon after one retrieval trial but only when using the doubled dose of protein synthesis-inhibitor that has been used to inhibit consolidation.     

The cognitive implications of asymmetric color generalization in honeybees

Generalization occurs when a conditioned response formed to one stimulus is also elicited by other stimuli which have not been used in the course of conditioning. Here, we studied color generalization in honeybees Apis mellifera trained to two rewarded colors, S₁+ and S₂+. After training, bees were tested with non-rewarded novel stimuli, which lay between the trained stimuli in a honeybee color space (Int) or outside the range defined by the trained stimuli (E ₁ and E ₂). We analyzed whether bees interpolated their choice to Int and/or extrapolated it to E ₁ and E ₂. We compared the performances of the group trained with S₁+ and S₂+ to those of control groups trained only with S₁+ or S₂+. Bees trained with S₁+ and S₂+ responded similarly and highly to all test stimuli. These results do not allow discerning between generalization models based on the presence of interpolation and/or extrapolation. Nevertheless, bee’s performance was consistent with a linear summation of the two generalization gradients generated by S₁+ and S₂+, respectively. These gradients were asymmetric because control bees responded to the test stimuli as if these belonged to different similarity classes in spite of the fact that they had similar perceptual distances separating them. Stimuli treated as similar were located in the same half of the color spaces, whereas stimuli treated as different were located in opposite halves. Our results suggest that color categories could exist in honeybees and may underlie the performance of the control groups. Under this assumption, color categories would be also present in simpler nervous systems, and would not require factors such as language to be expressed.     

Honeybees (Apis mellifera) holding on to memories: response competition causes retroactive interference effects

Five experiments on honeybees examined how the learning of a second task interferes with what was previously learned. Free flying bees were tested for landmark-based memory in variations on a paradigm of retroactive interference. Bees first learned Task 1, were tested on Task 1 (Test 1), then learned Task 2, and were tested again on Task 1 (Test 2). A 60-min delay (waiting in a box) before Test 2 caused no performance decrements. If the two tasks had conflicting response requirements, (e.g., target right of a green landmark in Task 1 and left of a blue landmark in Task 2), then a strong decrement on Test 2 was found (retroactive interference effect). When response competition was minimised during training or testing, however, the decrement on Test 2 was small or nonexistent. The results implicate response competition as a major contributor to the retroactive interference effect. The honeybee seems to hold on to memories; new memories do not wipe out old ones.     

Error is proportional to distance measured by honeybees: Weber’s law in the odometer

Honeybees were trained to fly a specific distance, the same over trials, down a tunnel for a reward. After training, they were tested occasionally with the reward absent. On tests, bees fly to or just past the expected place of reward, then turn around and fly back. After some distance, they turn back again, and may continue turning back and forth a number of times. Past research has shown that distance estimation in this task is based on the retinal flow of visual texture on the walls of the tunnel. Here we measured the errors in distance estimation as a function of training distance. Errors were measured as the standard deviation across trials of the positions of the first two turns (Turn1 and Turn2), and of the Middle (average of Turn1 and Turn2) and Spread (difference between Turn1 and Turn2). All errors were proportional to the training distance, thus obeying Weber’s law. Models of possible mechanisms underlying this phenomenon are discussed. The mean Spread matches the errors in Turn1 and Middle, suggesting that the bee chooses the spread of its search to match the expected odometric error. Received: 28 April 1998 / Accepted after revision: 19 November 1998     

Evidence for counting in insects

Here we investigate the counting ability in honeybees by training them to receive a food reward after they have passed a specific number of landmarks. The distance to the food reward is varied frequently and randomly, whilst keeping the number of intervening landmarks constant. Thus, the bees cannot identify the food reward in terms of its distance from the hive. We find that bees can count up to four objects, when they are encountered sequentially during flight. Furthermore, bees trained in this way are able count novel objects, which they have never previously encountered, thus demonstrating that they are capable of object-independent counting. A further experiment reveals that the counting ability that the bees display in our experiments is primarily sequential in nature. It appears that bees can navigate to food sources by maintaining a running count of prominent landmarks that are passed en route, provided this number does not exceed four.     

Categorization of visual stimuli in the honeybee Apis mellifera

Categorization refers to the classification of perceptual input into defined functional groups. We present and discuss evidence suggesting that stimulus categorization can also be found in an invertebrate, the honeybee Apis mellifera, thus underlining the generality across species of this cognitive process. Honeybees show positive transfer of appropriate responding from a trained to a novel set of visual stimuli. Such a transfer was demonstrated for specific isolated features such as symmetry or orientation, but also for assemblies (layouts) of features. Although transfer from training to novel stimuli can be achieved by stimulus generalization of the training stimuli, most of these transfer tests involved clearly distinguishable stimuli for which generalization would be reduced. Though in most cases specific experimental controls such as stimulus balance and discriminability are still required, it seems appropriate to characterize the performance of honeybees as reflecting categorization. Further experiments should address the issue of which categorization theory accounts better for the visual performances of honeybees.This contribution is part of the special issue “Animal Logics” (Watanabe and Huber 2006).