Abstract
Learning of stimulus sequences is considered as a characteristic feature of episodic memory since it contains not only a particular item but also the experience of preceding and following events. In sensorimotor tasks resembling navigational performance, the serial order of objects is intimately connected with spatial order. Mammals and birds develop episodic(-like) memory in serial spatio-temporal tasks, and the honeybee learns spatio-temporal order when navigating between the nest and a food source. Here I examine the structure of the bees’ memory for a combined spatio-temporal task. I ask whether discrimination and generalization are based solely on simple forms of stimulus-reward learning or whether they require sequential configurations. Animals were trained to fly either left or right in a continuous T-maze. The correct choice was signaled by the sequence of colors (blue, yellow) at four positions in the access arm. If only one of the possible 4 signals is shown (either blue or yellow), the rank order of position salience is 1, 2 and 3 (numbered from T-junction). No learning is found if the signal appears at position 4. If two signals are shown, differences at positions 1 and 2 are learned best, those at position 3 at a low level, and those at position 4 not at all. If three or more signals are shown these results are corroborated. This salience rank order again appeared in transfer tests, but additional configural phenomena emerged. Most of the results can be explained with a simple model based on the assumption that the four positions are equipped with different salience scores and that these add up independently. However, deviations from the model are interpreted by assuming stimulus configuration of sequential patterns. It is concluded that, under the conditions chosen, bees rely most strongly on memories developed during simple forms of associative reward learning, but memories of configural serial patterns contribute, too.
Highlights
Learning of stimulus sequences requires memory of the temporal order of occurrences
The aim was to simulate a navigational task during a foraging episode, with the parameters involved in sequential landmark experience during approach flights more precisely controlled than it would be possible in a natural foraging range
Bees are known to interpret the length of their flights through a narrow tunnel as up to five times longer than their flights in the open due to their distance estimation via visual flow field [25], [26], [27], and they are known to learn the sequence of landmarks on their foraging trips [9], [28], [8]
Summary
Learning of stimulus sequences requires memory of the temporal order of occurrences. Under natural conditions temporal sequence is often combined with spatial sequence, e.g. in navigational tasks. It is not too far fetched to ask whether an insect like the honeybee is able to create episodic-like memory because bees are known to navigate with reference to a map-like spatial memory [4], perform configural forms of compound learning (such as positive and negative patterning in olfactory conditioning, [5]), master serial conditional discrimination like matching-to-sample and non matching-to-sample tasks [6], extract rules from multiple training sets (e.g. symmetrical vs asymmetrical patterns, [7] sequences of turn is mazes with multiple choice points, [8]), and organize their foraging activities according to multiple circadian time windows according to occasion setting conditions (review: [9], [10]) None of these experiments allowed rejecting more simple explanations, e.g the familiarity of signals, the recency of experience, differences of the strengths of memory traces and other characteristics of associative learning. In such a scenario one would expect the learning of the temporal-spatial sequences to be defined predominantly with respect to the evaluating conditions for the choice, the reward following the correct choice, and the fact that positions closer to the evaluating signal may have a greater impact on memory
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