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

Neural Organization of A3 Mushroom Body Extrinsic Neurons in the Honeybee Brain

In the insect brain, the mushroom body is a higher order brain area that is key to memory formation and sensory processing. Mushroom body (MB) extrinsic neurons leaving the output region of the MB, the lobes and the peduncle, are thought to be especially important in these processes. In the honeybee brain, a distinct class of MB extrinsic neurons, A3 neurons, are implicated in playing a role in learning. Their MB arborisations are either restricted to the lobes and the peduncle, here called A3 lobe connecting neurons, or they provide feedback information from the lobes to the input region of the MB, the calyces, here called A3 feedback neurons. In this study, we analyzed the morphology of individual A3 lobe connecting and feedback neurons using confocal imaging. A3 feedback neurons were previously assumed to innervate each lip compartment homogenously. We demonstrate here that A3 feedback neurons do not innervate whole subcompartments, but rather innervate zones of varying sizes in the MB lip, collar, and basal ring. We describe for the first time the anatomical details of A3 lobe connecting neurons and show that their connection pattern in the lobes resemble those of A3 feedback cells. Previous studies showed that A3 feedback neurons mostly connect zones of the vertical lobe that receive input from Kenyon cells of distinct calycal subcompartments with the corresponding subcompartments of the calyces. We can show that this also applies to the neck of the peduncle and the medial lobe, where both types of A3 neurons arborize only in corresponding zones in the calycal subcompartments. Some A3 lobe connecting neurons however connect multiple vertical lobe areas. Contrarily, in the medial lobe, the A3 neurons only innervate one division. We found evidence for both input and output areas in the vertical lobe. Thus, A3 neurons are more diverse than previously thought. The understanding of their detailed anatomy might enable us to derive circuit models for learning and memory and test physiological data

Neural Correlates of Social Behavior in Mushroom Body Extrinsic Neurons of the Honeybee Apis mellifera

The social behavior of honeybees (Apis mellifera) has been extensively investigated, but little is known about its neuronal correlates. We developed a method that allowed us to record extracellularly from mushroom body extrinsic neurons (MB ENs) in a freely moving bee within a small but functioning mini colony of approximately 1,000 bees. This study aimed to correlate the neuronal activity of multimodal high-order MB ENs with social behavior in a close to natural setting. The behavior of all bees in the colony was video recorded. The behavior of the recorded animal was compared with other hive mates and no significant differences were found. Changes in the spike rate appeared before, during or after social interactions. The time window of the strongest effect on spike rate changes ranged from 1 s to 2 s before and after the interaction, depending on the individual animal and recorded neuron. The highest spike rates occurred when the experimental animal was situated close to a hive mate. The variance of the spike rates was analyzed as a proxy for high order multi-unit processing. Comparing randomly selected time windows with those in which the recorded animal performed social interactions showed a significantly increased spike rate variance during social interactions. The experimental set-up employed for this study offers a powerful opportunity to correlate neuronal activity with intrinsically motivated behavior of socially interacting animals. We conclude that the recorded MB ENs are potentially involved in initiating and controlling social interactions in honeybees

Sensory memory for odors is encoded in spontaneous correlated activity between olfactory glomeruli

Sensory memory is a short-lived persistence of a sensory stimulus in the nervous system, such as iconic memory in the visual system. However, little is known about the mechanisms underlying olfactory sensory memory. We have therefore analyzed the effect of odor stimuli on the first odor-processing network in the honeybee brain, the antennal lobe, which corresponds to the vertebrate olfactory bulb. We stained output neurons with a calcium-sensitive dye and measured across-glomerular patterns of spontaneous activity before and after a stimulus. Such a single-odor presentation changed the relative timing of spontaneous activity across glomeruli in accordance with Hebb's theory of learning. Moreover, during the first few minutes after odor presentation, correlations between the spontaneous activity fluctuations suffice to reconstruct the stimulus. As spontaneous activity is ubiquitous in the brain, modifiable fluctuations could provide an ideal substrate for Hebbian reverberations and sensory memory in other neural systems

The Circuitry of Olfactory Projection Neurons in the Brain of the Honeybee, Apis mellifera

In the honeybee brain, two prominent tracts – the medial and the lateral antennal lobe tract – project from the primary olfactory center, the antennal lobes (ALs), to the central brain, the mushroom bodies (MBs), and the protocerebral lobe (PL). Intracellularly stained uniglomerular projection neurons were reconstructed, registered to the 3D honeybee standard brain atlas, and then used to derive the spatial properties and quantitative morphology of the neurons of both tracts. We evaluated putative synaptic contacts of projection neurons (PNs) using confocal microscopy. Analysis of the patterns of axon terminals revealed a domain-like innervation within the MB lip neuropil. PNs of the lateral tract arborized more sparsely within the lips and exhibited fewer synaptic boutons, while medial tract neurons occupied broader regions in the MB calyces and the PL. Our data show that uPNs from the medial and lateral tract innervate both the core and the cortex of the ipsilateral MB lip but differ in their innervation patterns in these regions. In the mushroombody neuropil collar we found evidence for ALT boutons suggesting the collar as a multi modal input site including olfactory input similar to lip and basal ring. In addition, our data support the conclusion drawn in previous studies that reciprocal synapses exist between PNs, octopaminergic-, and GABAergic cells in the MB calyces. For the first time, we found evidence for connections between both tracts within the AL

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