The Waggle Dance as an Intended Flight: A Cognitive Perspective

The notion of the waggle dance simulating a flight towards a goal in a walking pattern has been proposed in the context of evolutionary considerations. Behavioral components, like its arousing effect on the social community, the attention of hive mates induced by this behavior, the direction of the waggle run relative to the sun azimuth or to gravity, as well as the number of waggles per run, have been tentatively related to peculiar behavioral patterns in both solitary and social insect species and are thought to reflect phylogenetic pre-adaptations. Here, I ask whether these thoughts can be substantiated from a functional perspective. Communication in the waggle dance is a group phenomenon involving the dancer and the followers that perform partially overlapping movements encoding and decoding the message respectively. It is thus assumed that the dancer and follower perform close cognitive processes. This provides us with access to these cognitive processes during dance communication because the follower can be tested in its flight performance when it becomes a recruit. I argue that the dance message and the landscape experience are processed in the same navigational memory, allowing the bee to fly novel direct routes, a property understood as an indication of a cognitive map

Serial Position Learning in Honeybees

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

Navigation and dance communication in honeybees: a cognitive perspective

Flying insects like the honeybee experience the world as a metric layout embedded in a compass, the time-compensated sun compass. The focus of the review lies on the properties of the landscape memory as accessible by data from radar tracking and analyses of waggle dance following. The memory formed during exploration and foraging is thought to be composed of multiple elements, the aerial pictures that associate the multitude of sensory inputs with compass directions. Arguments are presented that support retrieval and use of landscape memory not only during navigation but also during waggle dance communication. I argue that bees expect landscape features that they have learned and that are retrieved during dance communication. An intuitive model of the bee’s navigation memory is presented that assumes the picture memories form a network of geographically defined locations, nodes. The intrinsic components of the nodes, particularly their generalization process leads to binding structures, the edges. In my view, the cognitive faculties of landscape memory uncovered by these experiments are best captured by the term cognitive map

A short history of studies on intelligence and brain in honeybees

Reflections about the historical roots of our current scientific endeavors are useful from time to time as they help us to acknowledge the ideas, concepts, methodological approaches, and idiosyncrasies of the researchers that paved the ground we stand on right now. The 50-year anniversary of Apidologie offers the opportunity to refresh our knowledge about the history of bee research. I take the liberty of putting the founding year of Apidologie in the middle of the period I cover here. The nascent period of behavioral biology around the late 19th to the early twentieth century was intimately connected with a loss of concepts related to the mental functions of the brain, concepts that were rooted in Darwin’s theory of gradualism in the living world including cognition in animals. This loss was celebrated both in ethology and behaviorism as the gateway to scientific impartiality. Using this apparently strict scientific approach, impressive discoveries were made by observing and strictly quantifying the behavior of bees. The first forays into the brain, however, uncovered a richness of structure and function that reached far beyond stereotypical input/output connections and opened the way to compensating the conceptual restrictions imposed on us by traditional ethology. Honeybee research provides us with a particularly exciting story in this context. The cognitive turn in behavioral biology is intimately connected to the increasing knowledge of how the brain works, also in honeybee research. What has been achieved so far is just the beginning, but it gives us a glimpse of a promising future. Teamwork between neuroscientists and behavioral biologists is needed to elucidate brain functions such as the expectation of future outcomes and intentionality as an entry to animal intelligence reflecting the flexibility and adaptability in behavior also seen in honeybees

Memory Formation in Reversal Learning of the Honeybee

In reversal learning animals are first trained with a differential learning protocol, where they learn to respond to a reinforced odor (CS+) and not to respond to a non-reinforced odor (CS−). Once they respond correctly to this rule, the contingencies of the conditioned stimuli are reversed, and animals learn to adjust their response to the new rule. This study investigated the effect of a protein synthesis inhibitor (emetine) on the memory formed after reversal learning in the honeybee Apis mellifera. Two groups of bees were studied: summer bees and winter bees, each yielded different results. Blocking protein synthesis in summer bees inhibits consolidation of the excitatory learning following reversal learning whereas it blocked the consolidation of the inhibitory learning in winter bees. These findings suggest that excitatory and inhibitory learning may involve different molecular processes in bees, which are seasonally dependent

Sensory Representation and Learning-Related Plasticity in Mushroom Body Extrinsic Feedback Neurons of the Protocerebral Tract

Gamma-aminobutyric acid immunoreactive feedback neurons of the protocerebral tract are a major component of the honeybee mushroom body. They have been shown to be subject to learning-related plasticity and provide putative inhibitory input to Kenyon cells and the pedunculus extrinsic neuron, PE1. We hypothesize, that learning-related modulation in these neurons is mediated by varying the amount of inhibition provided by feedback neurons. We performed Ca2+ imaging recordings of populations of neurons of the protocerebral-calycal tract (PCT) while the bees were conditioned in an appetitive olfactory paradigm and their behavioral responses were quantified using electromyographic recordings from M17, the muscle which controls the proboscis extension response. The results corroborate findings from electrophysiological studies showing that PCT neurons respond to sucrose and odor stimuli. The odor responses are concentration dependent. Odor and sucrose responses are modulated by repeated stimulus presentations. Furthermore, animals that learned to associate an odor with sucrose reward responded to the repeated presentations of the rewarded odor with less depression than they did to an unrewarded and a control odor

Generalization of navigation memory in honeybees

Flying insects like the honeybee learn multiple features of the environment for efficient navigation. Here we introduce a novel paradigm in the natural habitat, and ask whether the memory of such features is generalized to novel test conditions. Foraging bees from colonies located in 5 different home areas were tested in a common area for their search flights. The home areas differed in the arrangements of rising natural objects or their lack, and in the existence or lack of elongated ground structures. The test area resembled partly or not at all the layout of landmarks in the respective home areas. In particular, the test area lacked rising objects. The search flights were tracked with harmonic radar and quantified by multiples procedures, extracting their differences on an individual basis. Random search as the only guide for searching was excluded by two model calculations. The frequencies of directions of flight sectors differed from both model calculations and between the home areas in a graded fashion. Densities of search flight fixes were used to create heat maps and classified by a partial least squares regression analysis. Classification was performed with a support vector machine in order to account for optimal hyperplanes. A rank order of well separated clusters was found that partly resemble the graded differences between the ground structures of the home areas and the test area. The guiding effect of elongated ground structures was quantified with respect to the sequence, angle and distance from these ground structures. We conclude that foragers generalize their specific landscape memory in a graded way to the landscape features in the test area, and argue that both the existence and absences of landmarks are taken into account. The conclusion is discussed in the context of the learning and generalization process in an insect, the honeybee, with an emphasis on exploratory learning in the context of navigation