Associative in honey bees R Menzel

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R Menzel. Associative learning in honey bees. Apidologie, Springer Verlag, 1993, 24 (3), pp.157-168. ￿hal-00891068￿

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Associative learning in honey bees

R Menzel

Freie Universität Berlin, Fachbereich Biologie, Institut für Neurobiologie, Königin-Luise-Straße 28-30, 1000 Berlin 33, Germany

(Received 20 October 1992; accepted 9 February 1993)

Summary — The learning of honey bees has been reviewed. In the context of foraging be havior, bees perform 2 forms of learning, latent (or observatory) and associative learning. Latent learning plays an important role in spatial orientation and learning during dance communication, but the mechanisms of this kind of learning are little understood. In associative learning, stimuli experi- enced immediately before the reward (usually sucrose solution) are memorized for the guidance of future behavior. Well-established paradigms have been used to characterize operant and . The classical conditioning of olfactory stimuli is a very effective form of learning in bees and has helped to describe the behavioral and physiological basis of memory formation. It is con- cluded that memory needs time to be established and is processed in sequential phases. The neuro- nal compartments of the brain involved in the chemosensory pathway appear to participate different- ly in the sequential memory phases. A model is developed which assigns the strong non-associative components in olfactory conditioning to the antennal lobes, and the associative components to the mushroom bodies and the lateral output region of the protocerebrum. It is speculated that the amne- sia-sensitive memory resides in the mushroom bodies and the amnesia-resistant memory in certain structures (eg the lateral protocerebrum) perhaps together with the mushroom bodies. learning / olfactory conditioning / memory / protocerebrum / mushroom bodies / Apis melli- fera

INTRODUCTION Bees foraging for food (nectar and pol- len for the colony storehouse), water and The social life of the honey bee (Apis mel- resin (for colony care purposes) com- lifera L) colony forms the evolutionary mence their foraging trips at the colony framework for the behavior of the individu- and return to it within minutes or hours. As al insect and is crucial for the survival of young bees, they learn the landmarks sur- each bee, as it cannot exist independent- rounding the nest location on self-training ly. The lifespan of the individual bee is rel- flights. They also learn to orientate them- atively short (4-6 wk in summer, several selves to the sun compass in relation to months in autumn, winter and spring), but the landmarks surrounding the nest. When the colony itself is potentially everlasting. the colony reproduces, a large number of the well-experienced bees leave the colo- The study of learning in bees has fo- ny, together with the old queen, in search cused on appetitive learning in the context of a new nesting place. During this pro- of food collection, because experimenta- cess, each bee has to replace the old tion is most convenient under these condi- memory of its terrestrial and celestial or- tions: stimuli are easily selected and stimu- ientation cues with a new memory (Lin- lus-response conditions can be accurately dauer, 1955, 1959, 1967; von Frisch, controlled. Since an average colony con- 1967). Food is collected from flowers tains > 40 000 foraging bees, a virtually un- when and wherever available and is stored limited number of test animals are availa- for periods of starvation. Consequently, ble and can be motivated to search for the innate search image for food sources food by means of the recruitment behavior has to be very general, and individual as- of experienced bees. for both sociative learning processes are most im- recruitment and seach behavior can be portant for the effective accomplishment of manipulated by the concentration of the foraging activities. Celestial and terrestial sucrose reward. Because bees learn very cues, position in relation to landmarks and fast (often by a single trial), experimenta- features (color, shape, odor, etc) of the tion is facilitated. The experimental insect new feeding place are learned afresh for returns to the artificial feeding station relia- each new location. An individual bee may bly and shuttles back and forth between collect food from only one location and the colony and the feeding station at inter- one kind of flower during its lifetime, but in vals of minutes. Choice behavior can be most cases, each bee will visit many differ- easily tested because extinction proce- ent place and learn many different flower dures have little effect and search motiva- cues throughout its lifespan. tion is high. The training procedure of indi- marked bees is also used Within the colony, the foragers commu- vidually nicate using ritualized body movements effectively to study other forms of learning (waggle dance), which encode the dis- (eg latent learning during orientation to ce- tance, direction and relative profitability of lestial and terrestrial cues) and cooperative behavior in the communica- the food source. The odor of the food colony (dance allocation of social source can be smelled by the attending tion, duties) (von bees from the hairy body of the dancing Frisch, 1967; Lindauer, 1967; Menzel, bee and, in the case of nectar collection, 1985; Seeley, 1985b; Gould, 1986b). the collected food may be sampled, as the Genetic predispositions to learning may dancer offers minute amounts for tasting. be of particular importance in insects. It is The relative profitability of the food source often assumed, though with limited experi- is estimated by the foraging bee on the ba- mental verification, that the small brain of sis of how quickly its sample is taken up an insect (in the bee: 1 mm3, 900 000 neu- by the young receiving bees at the colony rons) might be more effective if it had a entrance. Since the young receiving bees particularly large proportion of stereotyped register the needs of the colony (brood , genetically controlled connec- condition, storage space, size and density tions and a preprogrammed switchboard of of the colony) and the quality of the incom- potential neural contacts. In other words, ing food, the feedback to the individual for- sensory cues may be preordained, motor ager provides the necessary information for programs adjusted only within strict limits, quick adjustments to the colony’s needs reinforcing conditions preprogrammed so and a relative rating of its foraging behavior that associations can be formed quickly (von Frisch, 1967; Seeley, 1985a, b). but selectively, and internal memory pro- cesses may run under the tight control of However, it is not known whether this be- automatic storage routines (Gould and havior indicates a backward conditioning, Marler, 1984; Menzel, 1984). In view of because the unconditioned stimulus has this, it is astounding how adaptable the be- not yet been identified for this kind of learn- havior of bees actually is, how important ing. how learning phenomena are, persistent During departure from a newly-discover- the memories and how are, many signals ed natural food source, the bees perform and motor are learned. The programs ge- circular flights at an increasing distance netic frame for learning has, therefore, to from the feeding place. Most learning dur- in be quite broad order to allow the estab- ing this phase is directed towards more lishment of new neural connections under distant signals such as landmarks, celes- the conditions of learning rules (Menzel, tial cues and the direction of and distance Menzel 1990; et al, 1993). between the food source and the colony. It is not known what kind of learning guides the bee during the circular observatory APPETITIVE LEARNING flights. Associative learning is unlikely, be- IN THE NATURAL CONTEXT cause bees transported to an unknown place perform the same circling flights and When a searching bee discovers a source learn to fly back to the hive along the short- of sweet solution, eg an artificial feeder est possible route without being fed at the with sucrose solution, it quickly learns to release site (Menzel, 1989). What bees re- associate the surrounding visual and olfac- port through their dance behavior within tory signals with the reward. Acquisition the colony also relates to their experience functions indicate that olfactory stimuli (eg during the return flight to the colony. It ap- floral odorants) are learned within 1-2 pears from these results that both forward learning trials, colors within 1-5 learning and observatory learning are effective in trials, and black and white patterns from learning of freely-flying bees. the 5th learning trial onward. Most of this Long-distance orientation (usually up to learning is forward conditioning, because several kilometers) requires the learning of signals perceived before the reward are signal sequences and the retrieval of con- most strongly associated, whereas those text-specific memories. It is indeed possi- perceived during the reward or during the ble to train bees to different visual cues in departure flight are associated less effec- a sequence within one foraging bout (Col- tively or not at all. lett and Kelber, 1988). They also learn to More recently, it has been demonstrat- associate a particular time of day with a set of stimuli ed that bees perform a specific behavior particular (eg flight direction, color or on departure, which leads to learning of distance, odor) (von Frisch, 1967). new and unexpected cues (Lehrer, 1991). Reversal learning, overlearning and If visual cues are different from those ex- multireversal learning are effective learning perienced before, the bee does not fly phenomena. The speed of reversal learn- away immediately after completion of feed- ing in a dual forced-choice situation is at ing, but rather turns around in flight and first retarded in proportion to the increasing looks back at the feeding place. The occur- number of initial learning trials on 1 of 2 al- rence of this behavior correlates with the ternatives, and strongest resistance to re- choice behavior at the next visit. It is there- versal learning is reached after 5-10 initial fore concluded that bees learn the new trials. If the number of initial learning trials conditions during their look-back behavior. exceeds 10 trials, reversal to the other al- ternative is increasingly favored (over- experimental psychology and have been learning reversal effect) (Menzel, 1969). reported by Bitterman (1988). Such an overlearning reversal effect is The study of operant and latent learning also known to exist in other animals and is in bees in a natural behavioral context has either as a loss of US interpreted strength provided many examples of impressive of expected (already learned) signals or a and complex actions (von Frisch, 1967). loss of attention to the conditioned stimuli How complex is the mind of the honey (CS) as a result of a general decrease in bee? Are there indications of mental oper- motivation (Rescorla and Wagner, 1972). ations that, in the absence of behavioral In the motivation does not bees, general acts, may be interpreted as internal opera- change throughout the series of learning tions of learned representations? When a trials, which might indicate a decrease in bee is transported in a dark box from the the associative strength in predicted US hive to any site within its foraging area (= 2 presentations as a mechanism. Multirever- km radius), it will recognize the landmarks sal schedules with fixed performance surrounding the hive very well and return schedules reveal a learning strategy that, to it reliably and quickly. Do bees under after many reversals, leads to a decrease these conditions consult a mental map of in the number of reversed learning trials the landmarks which would allow them to necessary to reach a constant level of calculate the shortest flight path, although choice preference. This would seem to in- they have never experienced this flight dicate an acquired strategy to assimilate path before? reversal Bitter- learning (Meineke, 1978; Gould (1986a) reported experiments man, 1988). However, the effect is quite which appear to favor such an interpreta- small and depends greatly on the design tion. Recent experiments, however, sup- of the experiment and the conditioned port the conclusion that bees use a differ- stimuli used (Menzel, 1990). ent strategy (Wehner and Menzel, 1990). The experimental procedures which test They appear to apply a hierarchy of best- the ability of an insect to adapt its perfor- matching rules to different kinds of orienta- mance to reward schedules are Skinner’s tion marks. The celestial cues (sun, polar- (1938) continuous, fixed ratio and fixed in- ized light pattern) rank highest. Bees al- terval schedules (CR, FR ways start to fly according to the sun and FI respectively). Bees develop a high- compass. If that flight path produces a mis- er resistance to extinction in a FR than ina match with the long distance landmarks CR schedule. In an FI reinforcement (landmarks without motion parallax, eg schedule, bees show lower response rates profile of horizon) they gradually switch to than those in an FR schedule. FR sched- these landmarks and fly according to the ules of up to 1 reinforcement out of 30 best match between the memorized and trials and FI schedules with up to 90 s be- the actually experienced pattern. When tween are reached after this flight path brings them close to local several days of training (Grossmann, landmarks (landmarks with motion paral- 1973). This behavior appears to be an ad- lax) in the hive surroundings (or the feed- aptation to ecological conditions, since ing place if they are motivated for forag- only a fraction of the flowers on which ing), then they home in by a successive bees alight provide nectar and/or pollen, search for the best match with the local and these rewards are usually minute. Ad- landmarks (Cartwright and Collett, 1983). ditional operant learning phenomena in The rank order of the orientation marks honey bees were studied in the tradition of (celestial, distant and local cues) and the precision with which the matching is ap- forced context. Partial reinforcement plied depends on the level of experience schedules have little effect on the acquisi- regarding each of these orientation marks. tion function, because extinction trials do It thus appears that mental operations on a not alter the CR probability but increase representational level have not to be as- the resistance to extinction and other sumed to explain the impressive capability measures of learning (Menzel, 1990). of bees during long-distance flights. Blocking and overshadowing experi- ments are used to characterize the infor- mational content of the CS (Rescorla, REFLEX CONDITIONING 1988). In PER conditioning, olfactory stim- uli overshadow mechanical stimuli, and Classical conditioning of reflexes is a most blocking effects are not found. This indi- convenient way to study the behavioral cates that attentiveness is not a limiting and neural mechanisms of associative factor, and that the salience or associabili- learning. In the honey bee, proboscis ex- ty of a stimulus (olfactory over mechanical) tension reflex (PER) to a sucrose stimulus is an important factor. Second-order condi- at the antennae is a reliable reflex in the tioning is a procedure which tests whether context of feeding. The bee will extend its a CS can acquire the potential of an US. proboscis (tongue) reflexively when the an- This has also been demonstrated for olfac- tennae are touched with a drop of sucrose tory PER conditioning (Bitterman et al, solution. It can be conditioned to olfactory 1983; Menzel, 1990). The strength of the or mechanical stimuli (conditioned stimuli, effect is highly dependent on the CS used. CS), even under conditions where the in- Citral, a particularly salient CS and chemi- sect is harnessed in a tube (Kuwabara, cal component of an attraction pheromone 1957) or prepared for physiological studies produced by bees to mark food sources, (Menzel et al, 1974, 1991, 1993; Menzel, has the strong potential of an acquired US; 1990). The PER and its conditioning to a more neutral odors (eg octanal) have a CS is highly dependent on hunger-induced weak potential for second-order condition- motivation. ing. The associative nature of PER condi- tioning has been established by demon- SEQUENTIAL MEMORY PROCESSING strating that only forward pairing of CS-US sequences are effective in various control groups (unpaired CS and US, CS or US A stable lifelong memory is formed even only presentations), and via differential after only a few learning trials. Harnessed conditioning of the 2 olfactory stimuli. The bees prepared for olfactory PER condition- predictive value of the CS depends on the ing do not survive long enough to allow reliability with which it is causally related to testing of their memory over periods of > the US. For example, repeated exposure 2-3 d, but retention remains high during to the CS in unpaired trials reduces its ac- this period, even after only 1-3 condition- quisition in subsequent conditioning. In dif- ing trials. After a single learning trial, the ferential conditioning, the reversal to the in- retention curve follows an early biphasic itially unpaired stimulus is slower after time course and a slowly decreasing slope more frequent initial unreinforced pre- in the long-term range (fig 1). The early exposure than after a lesser number of memory phase in the minute range is par- pre-exposures. The same applies for US- ticularly susceptible to both extinction and only pre-exposures in an otherwise rein- reversal learning, whereas the consolidat- ed memory is much more resistant. The cess (Menzel et al, 1991). Genetic lines of sensitizing effect of the appetitive stimulus bees with poor learning performance lack (sucrose solution) overlaps with the early the typical biphasic retention function, and high response level, indicating that, at are poor in both the early nonassociative least in PER conditioning, the nonassocia- component and the associative consolida- tive memory initiated by the US contrib- tion (Brandes et al, 1988; Brandes and utes substantially to the response probabil- Menzel, 1990). ity immediately after the single learning Amnestic treatments (cooling, narcosis, trial (fig 1). The specific associative memo- weak electroconvulsive brain stimulation ry increases slowly over 5-7 min; thus (EBS)) erase the memory trace if applied consolidation is a purely associative pro- within minutes of the single-trial learning. Several trials within a minute or longer time intervals after a single trial render the memory trace immune to amnestic treat- ment. The time course of retrograde am- nestic sensitivity is independent of the kind of learning (operant color learning, olfacto- ry PER-conditioning), but depends on the structure of the brain to which the treat- ment is applied. Local cooling of the pe- ripheral olfactory neuropile (antennal lobes) within 1 min after the learning trial causes retrograde amnesia in the treated input side only (fig 2). In contrast, cooling of the central processing neuropile (mush- room bodies) initiates retrograde amnesia with a longer time course which is similar to that caused by cooling the whole insect, and the effect is not limited to the treated side of the brain (Menzel et al, 1974; Erber et al, 1980). The model arising from these results lo- calizes the specific associative compo- nents of the olfactory memory trace in a prominent structure of the insect brain, the mushroom bodies, and the nonassociative memory in the antennal lobes (sensory components) with its direct connections to the suboesophageal ganglion (SOG), where the motor components are localized (fig 3). Such a model is supported by find- ings on structural brain mutants of Dro- sophila: mutants with distorted or miniature mushroom bodies are able to orient nor- mally to olfactory stimuli, but lack the ca- pacity for olfactory learning (Heisenberg et al, 1985). Because the reflex pathway of the PER in bees is based on a direct con- nection between sucrose receptors on the antenna and motoneurons which run via the antennal lobes and the SOG, the neu- rons connecting the mushroom bodies run parallel to the reflex pathway. Consequent- ly, associative memory does not appear to be a property of the reflex pathway, but rather of a parallel pathway. Therefore, nonassociative (sensitization) and associa- tive memory components may be separat- room bodies to the ganglia in the ventral cord, SOG neurons, intrinsic premotor and motorneurons. Correlates of associative memory are found in neurons downstream from the neurons of the central brain. Mushroom body extrinsic neurons have some properties which are compatible with the neural plasticity underlying associative learning. They are multimodal, have long- lasting stimulus after-effects which outlive a stimulus by many seconds and change their response properties in an associative learning situation (Erber et al, 1987). Re- cently, a single mushroom body extrinsic neuron, the PE1 neuron, has been charac- terized in great detail. It changes its re- ponse behavior to a forward-paired odor but not to a backward-paired odor during differential conditioning (Mauelshagen, 1990, 1993). Thus, specific properties of associative learning are represented at the level of a single identified neuron, the PE1 neuron. These results can be used to sup- port the notion that the mushroom bodies are specificially involved in associative learning. However, it was found that the re- sponse changes induced in the PE1 by for- ward pairing of an odor with sucrose stimu- lation does not last longer than a few minutes. Since memory lasts for days, it is tempting to conclude that the neural sub- strate of memory is restructured in such a way that brain regions other than the mushroom bodies (eg the lateral protocer- ed into 2 parallel structures (Menzel et al, ebrum) are involved in storing the long- 1991). term memory trace. Another possibility may be that the neural circuity intrinsic to the mushroom bodies may be restructured LOCALIZATION OF MEMORY in such a way that other extrinsic neurons become responsible for the retrieval of the The concept of functionally and anatomi- memory. cally separated memory traces is support- ed cell Sucrose by single recordings. (US) CONCLUSIONS induces sensitization effects in neurons at all levels, eg intrinsic antennal lobe neu- rons, relay neurons to the mushroom The effective learning behavior of honey lobes, projection neurons from the mush- bees in the context of feeding and the clear separation between memory pro- pense. En particulier, aucune dépendance cesses have helped us to approach basic quantitative des caractéristiques d’un questions in memory research. The results éventuel stimulus externe de récompense on the location of the olfactory memory n’a pu encore être mise en évidence pour engram in the bee brain provides a work- cette forme d’apprentissage. Une série de ing hypothesis, which localizes different paradigmes bien établis a été utilisée pour forms of behavioral plasticities and the se- étudier le conditionnement opérant quential memory phases in different re- d’abeilles volant librement et le condition- gions of the brain. In essence, the hypoth- nement classique d’abeilles immobilisées. esis states that transient and non- Le conditionnement olfactif d’abeilles im- associatively modifiable pathways run par- mobilisées est une méthode particulière- allel to pathways modified by associative ment utile pour suivre la formation de la learning processes. Pathways, including mémoire à long terme. Elle montre que la the mushroom bodies, are considered to mémoire passe par des phases séquentiel- change their properties, specifically during les qui se différencient par leur sensibilité associative memory formation, whereas di- à la perturbation et la contribution de diffé- rect connections between the sensory- rentes régions du cerveau. Nos connais- motor centers or the sensory neuropile of sances actuelles sont résumées dans un the antennal lobes alone do not contain all modèle (fig 3), qui suppose que les com- the necessary components for an associa- posantes fortement non associatives, qui tive memory trace. émanent du stimulus inconditionnel (solu- Over many decades research on honey tion sucrée), déterminent la première bees has contributed substantially to the phase de mémorisation et sont principale- solution of basic problems of , ment localisées dans le lobe antennaire. sensory physiology and neurophysiology, Les phases de mémorisation associative quite apart from the important contributions se distinguent par leur sensibilité à l’amné- it has made to , ecology and sie et par le rôle que jouent les actes répé- genetics. It is hoped that the methodologi- tés d’apprentissage. La phase sensible à cal advances in neurophysiology and bio- la perturbation est principalement attribuée chemistry will even further increase the im- aux corps pédonculés. On suppose que le portance of this fascinating species for protocérébron latéral participe également à neurobiological research. la mémoire stable, à long terme. L’organi- sation et la localisation de la mémoire de longue durée sont particulièrement incer- Résumé — L’apprentissage associatif taines. Les résultats présentés montrent chez l’abeille, Apis mellifera L. Une vue que l’abeille convient à merveille aux étu- d’ensemble du comportement d’apprentis- des qui visent à expliquer les bases neuro- sage des abeilles est présentée dans le nales de l’apprentissage et de la mémoire. cadre du comportement de butinage. Deux types d’apprentissage sont distingués : Apis mellifera L / apprentissage / condi- l’apprentissage latent (ou par observation) tionnement olfactif / mémoire / protocé- et l’apprentissage associatif. L’apprentissa- rébron / corps pédonculés ge latent, dont les mécanismes sont enco- re très mal connus, joue un rôle important dans l’orientation spatiale et la communica- Zusammenfassung — Assoziatives tion par les danses. Il n’y a pas de rapport Lernen bei Honigbienen. Das Lernverhal- spatio-temporel avec des stimuli de récom- ten von Bienen im Kontext ihres Futter- Sammelverhaltens wird übersichtsartig Gedächtnisses. Die dargestellten Ergeb- dargestellt. Zwei generelle Formen von nisse zeigen, daß die Honigbiene sich aus- Lernen werden unterschieden : Das laten- gezeichnet für Studien eignet, die auf die te (oder beobachtende) Lernen und das Aufklärung der neuronalen Grundlagen assoziative Lernen. Für das beobachtende von Lernen und Gedächtnis zielen. Lernen sind die Mechanismen noch recht wenig bekannt. Es spielt bei der Raumo- Lernen / olfaktorische Konditionierung / rientierung und bei der Tanzkommunika- Gedächtnis / Protocerebrum / Pilzkörper tion eine wichtige Rolle. Ein strenger zeit- lich-räumlicher Bezug zu belohnenden Sti- muli besteht nicht. Insbesondere wurde für REFERENCES diese Form des Lernens noch keine quan- titative Abhängigkeit von den Eigenschaf- Bicker G, Menzel R (1989) Chemical codes for ten eines möglichen externen belohnen- the control of behaviour in arthropods. Nature den Stimulus nachgewiesen. Das assozia- 337, 33-39 tive Lernen wurde dagegen sehr genau Bitterman ME (1988) Vertebrate-invertebrate untersucht. Eine Reihe von Standardpro- comparisons. NATO ASI Series-Intell. Evol zeduren wurden verwendet, um das ope- Biol 17, 251-275 rante Lernen von frei fliegenden Tieren Bitterman ME, Menzel R, Fietz A, Schäfer S und die klassische Konditionierung von fi- (1983) Classical conditioning of proboscis ex- in xierten Tieren zu studieren. Vor allem die tension honeybees (Apis mellifera). 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In: Experimen- Lindauer M (1955) Schwarmbienen auf Woh- tal Analysis of Insect Behaviour (Barton- nungssuche. Z Vgl Physiol 37, 263-324 Browne, L, ed) Springer, Berlin, 195-217 Lindauer M (1959) Angeborene und erlernte Menzel R, Michelsen B, Rüffer P, Sugawa M Komponenten in der Sonnenorientierung der (1988) Neuropharmacology of learning and Bienen. Z 43-62 Vgl Physiol 42, memory in honey bees. In: Synaptic Trans- Lindauer M (1967) Recent advances in bee mission and Plasticity in Nervous Systems communication and orientation. Annu Rev (Herting H, Spatz HC, eds) Springer, Berlin, Entomol 12, 439-470 335-350. Menzel R, Hammer M, Mauelshagen J (1990a) Lewis AC, eds) Chapman and Hall, New Memory stages in the honey bee. In: Brain — York, 79-125 Perception — Cognition. Proc 18th Göttingen Rescorla RA (1988) Behavioral studies of Ppav- Neurobiol Conf Thieme Roth (Eisner, G, eds) lovian conditioning. 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Princeton Univ Press, Princeton Menzel R, Greggers U, Hammer M (1993) Functional organization of appetitive learning Skinner BF (1938) The Behavior of Organisms. New York and memory in a generalist pollinator, the Appleton-Century-Crofts, honey bee. In: Insect Learning: Ecological Wehner R, Menzel R (1990) Do insects have cog- and Evolutionary Perspectives (Papaj D, nitive maps? Annu Rev Neurosci 13, 403-414