Learning in honeybees (Apis mellifera) as a function of sucrose concentration.

Foraging honeybees (Apis mellifera) were trained with 2 successively presented targets differing in color or odor, one of which always contained a 5-microliters drop of 50% sucrose solution and the other, a 5-microliters drop of 20% sucrose solution. Latency of response to each target was measured during the training, and at the conclusion, preference was measured in an unrewarded choice test. Analysis of the latencies showed both a prospective effect (faster response to the 50% target than to the 20% target) and a nonassociative retrospective effect (faster response after leaving the 20% target than after leaving the 50% target) reminiscent of the frustration effect in rats. The results both for prospective latency and for choice can be understood on the simple theory that the attractiveness of a target depends on the strength of its association with sucrose and that the effect of concentration is on asymptotic strength.     

Delayed alternation in honeybees (Apis mellifera)

Previous experiments with honeybees (Apis mellifera) failed to show learned control of performance by short-ten memory. In this study, honeybees were trained with an improved technique to choose 1 of 2 colors that was either the same as a recently rewarded sample (perseveration) or different (alteration). Because any increase in associative strength stemming from the sample experience would tend to promote perseveration and contravene alternation, the equal difficulty of the 2 tasks suggests that the role played by the sample was primarily discriminative. The animals remembered on each trial the immediately preceding experience with reward and learned to use that information appropriately. These new results extend the list of what may well be fundamental similarities in the learning of vertebrates and honeybees.     

Delayed symbolic matching in honeybees (Apis mellifera)

In a recent experiment on short-term memory (P. A. Couvillon, T. P. Ferreira, & M. E. Bitterman, 2003), honeybees (Apis mellifera) learned to choose between 2 colors on the basis of immediately preceding experience with 1 of them. Some learned to choose the same color as the sample (perseveration or matching), others to choose the alternative color (alternation or nonmatching). Performance in the 2 problems was very much the same. In the present experiment, honeybees learned no less readily to choose between the 2 colors on the basis of sample stimuli that were different from the colors (symbolic matching). A simple associative interpretation of the results is proposed.     

Simultaneous conditioning in honeybees (Apis mellifera).

Honeybees (Apis mellifera) were classically conditioned with odor as conditioned stimulus (CS), sucrose as unconditioned stimulus (US), and proboscis extension as response. The purpose of Experiment 1 (Ns = 26 and 27) was to look for facilitation of forward conditioning by CS-US overlap, but rapid conditioning without overlap left little room for improvement. In 2 further experiments, CS and US were simultaneous, and response to odor alone was measured in subsequent tests. In Experiment 2, a Simultaneous group (N = 25) responded more to the training odor than did an Unpaired control group (N = 25). In Experiment 3, a differentially conditioned Simultaneous group (N = 29) responded more to an odor paired with sucrose in training (S+) than to an odor presented alone (S-). The implications of the results for the problem of the role of amount of reward in honeybee learning are considered.     

Contrasting effects of imidacloprid on habituation in 7- and 8-day-old honeybees (Apis mellifera)

We examined the effects of sublethal doses (0.1, 1, and 10 ng per animal) of a new neonicotinoid insecticide, Imidacloprid, on habituation of the proboscis extension reflex (PER) in honeybees (Apis mellifera) reared under laboratory conditions. In untreated honeybees, the habituation of the proboscis extension reflex is age-dependent and there is a significant increase in the number of trials required for habituation in older bees (8-10 days old) as compared to very young bees (4-7 days old). Imidacloprid alters the number of trials needed to habituate the honeybee response to multiple sucrose stimulation. In 7-day-old bees, treatment with Imidacloprid leads to an increase in the number of trials necessary to abolish the response, whereas in 8-day-old bees, it leads to a reduction in the number of trials for habituation (15 min and 1 h after treatment), and to an increase 4 h after treatment. The temporal effects of Imidacloprid in both 7- and 8-day-old bees suggest that 4h after treatment the observed effects are due to a metabolite of Imidacloprid, rather than to Imidacloprid itself. Our results suggest the existence of two distinct subtypes of nicotinic receptors in the honeybee that have different affinities to Imidacloprid and are differentially expressed in 7- and 8-day-old individuals.     

Conditional withholding of proboscis extension in honeybees (Apis mellifera) during discriminative punishment.

Proboscis extension conditioning of honeybee workers was used to test the ability of bees to respond to appetitive and aversive stimuli while restrained in a harness that allows subjects to move their antennae and mouthparts (Kuwabara, 1957; Menzel, Erber, & Masuhr, 1974). Subjects were conditioned to discriminate between two odors, one associated with sucrose feeding and the other associated with a 10 V AC shock if they responded to the sucrose unconditioned stimulus (US) in the context of that odor. Most Ss readily learned to respond to the odor followed by sucrose feeding and not to the odor associated with sucrose stimulation plus shock. Furthermore, in the context of the odor associated with shock, significantly more subjects withheld or delayed proboscis extension on stimulation with the sucrose US than they did in the context of the odor associated with feeding. Thus, restrained honeybees can readily learn to avoid shock according to an odor context by withholding proboscis extension to a normally powerful releaser. Analysis of individual learning curves revealed that subjects differed markedly in performance on this task. Some learn the discrimination quickly, whereas others show different kinds of response patterns.     

Heritable variation for latent inhibition and its correlation with reversal learning in honeybees (Apis mellifera)

Latent inhibition (LI) in honeybees (Apis mellifera) was studied by using a proboscis extension response conditioning procedure. Individual queens, drones, and workers differed in the degree to which they revealed LI. The authors hypothesized that individual differences would have a substantial genetic basis. Two sets of progeny were established by crossing virgin queens and individual drones, both of which had been selected for differential expression of inhibition. LI was stronger in the progeny from the queens and drones that had shown greater inhibition. The expression of LI was also dependent on environmental factors that are most likely associated with age, foraging experience outside of the colony, or both. Furthermore, there was a correlated response in the speed at which progeny reversed a learned discrimination of 2 odors. These genetic analyses may reveal underlying mechanisms that these 2 learning paradigms have in common.     

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.     

Quantitative analysis of risk sensitivity in honeybees (Apis mellifera) with variability in concentration and amount of reward

Free-flying honeybees (Apis mellifera) were trained in a series of experiments designed to look for evidence of risk sensitivity in foraging for sucrose solution. The suitability of the choice method used was established in 3 preliminary experiments with differences in concentration, amount, and probability of reward. Of 5 subsequent experiments in which 2 alternatives provided the same mean concentration of sucrose solution with different variance, 3 showed risk indifference, and 2 showed risk aversion (preference for consistent reward). Of 2 final experiments in which the alternatives provided the same mean amount of sucrose solution with different variance, both showed risk aversion. Performance could be simulated quantitatively with a simple choice model developed by P. A. Couvillon and M. E. Bitterman (1991) to account for the results of a wide range of previous experiments on discriminative learning in honeybees.     

Evidence for associative learning in newly emerged honey bees (Apis mellifera)

The honey bee is a model organism for studies on the neural substrates of learning and memory. Associative olfactory learning using sucrose rewards is fast and reliable in foragers and older hive bees. However, researchers have so far failed to show any significant learning in newly emerged bees. It is generally argued that in these bees only part of the brain structures important for learning are fully developed. Here we show for the first time that newly emerged honey bees are capable of associative learning, if they are sufficiently responsive to sucrose. Responsiveness to sucrose, which can be measured using the proboscis extension response (PER), increases with age. Newly emerged bees are on average very unresponsive to sucrose. We show that if newly emerged bees displaying a PER to 10% sucrose or lower sucrose concentrations are conditioned to an odour, they show significant associative learning and early long-term memory. Nevertheless, the level of acquisition is still lower than in foragers. The general assumption that newly emerged honey bees are incapable of associative learning must therefore be reconsidered. Further, our study suggests that an age-dependent increase in responsiveness to rewarding stimuli is directly related to the development of early learning abilities. The decisive influence of responsiveness to rewarding stimuli in associative learning of newly emerged bees has far reaching consequences for studies on the development of associative learning capabilities in insects and vertebrates.     

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.     

Involvement of alpha-bungarotoxin-sensitive nicotinic receptors in long-term memory formation in the honeybee (Apis mellifera)

In the honeybee Apis mellifera, multiple-trial olfactory conditioning of the proboscis extension response specifically leads to long-term memory (LTM) which can be retrieved more than 24 h after learning. We studied the involvement of nicotinic acetylcholine receptors in the establishment of LTM by injecting the nicotinic antagonists mecamylamine (1 mM), alpha-bungarotoxin (alpha-BGT, 0.1 mM) or methyllycaconitine (MLA, 0.1 mM) into the brain through the median ocellus 20 min before or 20 min after multiple-trial learning. The retention tests were performed 1, 3, and 24 h after learning. Pre-training injections of mecamylamine induced a lower performance during conditioning but had no effect on LTM formation. Post-training injections of mecamylamine did not affect honeybees' performances. Pre-training injections of MLA or post-training injection of alpha-BGT specifically induced LTM impairment whereas acquisition as well as memory retrieval tested 1 or 3 h after learning was normal. This indicates that brain injections of alpha-BGT and MLA did not interfere with learning or medium-term memory. Rather, these blockers affect the LTM. To explain these results, we advance the hypothesis that honeybee alpha-BGT-sensitive acetylcholine receptors are also sensitive to MLA. These receptors could be essential for triggering intracellular mechanisms involved in LTM. By contrast, medium-term memory is not dependent upon these receptors but is affected by mecamylamine.     

Pattern vision of the honeybee (Apis mellifera): blue and green receptors in the discrimination of translocation

The visual discrimination of horizontal gratings by the honeybee (Apis mellifera) was studied in a Y-choice apparatus with fixed patterns presented vertically at a set range. Translocation in this context is the exchange of the positions of two different colored or black areas. This paper investigates what cues the bees have learned in this task. The patterns, made from combinations of calibrated colored papers, are designed to explore the parts played by the blue and green receptors when the boundary between the two colors provides contrast to only one receptor type. Horizontal translocation is not discriminated without contrast to the green receptors, but up/down translocation can be discriminated whatever the contrast at the boundary. The trained bees were tested on the same patterns made with different papers that included extreme changes in contrast. The results show that discrimination of up/down translocation involves green receptors and also blue receptors. When bees discriminate a translocation that shows contrast to only one type of receptor, they do not use the apparent brightness or the direction of the contrast to that receptor type acting alone. Instead, they discriminate the locations of colored areas irrespective of intensity differences or directions of contrasts. They use some measure of the photon flux at both receptor types and remember the difference between the colors and their locations.     

The Attraction of Africanized Honey Bees (Apis mellifera L.) to Soft Drinks and Perfumes

The attraction of Africanized bees to soft drinks and perfumes was investigated. In the first experiment, the ability of bees to discriminate between two perfumes (Realm for Men and Realm for Women) was assessed. The results indicated that the scents could be used as conditioned stimuli. In the second experiment, bees were divided into individual groups and confined to small metal tubes. Groups were fed either Diet Pepsi, spring water (control), Diet Guaraná, Diet Coca-Cola, Coca-Cola, Sprite, Pepsi, Guaraná, Sukita Orange, Fanta Orange, Fanta Grape, or sucrose (control). The dependent variable was the amount of time the bee's proboscis was in contact with a strip of filter paper saturated with the substance. The results indicated little or no contact with the diet soft drinks and spring water, 45–65 s of contact with Coca-Cola, Sprite, Pepsi, Guaraná, and Sukita Orange, and 75–140 s of contact with Fanta Orange, Fanta Grape, and sucrose (sucrose elicited the most contact of the substances tested). In a third experiment, the ability of bees to associate an odor with a soft drink was assessed in a discrimination task. With Citral and Geraniol as conditioned stimuli, conditioning was best to sucrose, Guaraná, and Fanta Orange. Little conditioning was observed with Pepsi, and no conditioning was observed with Diet Pepsi.     

Apparent height of a stereokinetic cone is decreased by departure from circularity

Subjects made judgements of the comparative height of the stereokinetic cones seen for pairs of rotating figures with varying eccentricity and ellipticity. For any given eccentricity, ellipticity of the figure reduced the apparent height, with narrow ellipses seeming to be shallower. The effect is attributed to an interaction in constancy scaling.     

Perseverative search at a visibly empty place by young infants

Two experiments are presented which indicate that when an object moves to a new place, year-old infants approach both its new location and its prior location. These object locations are not treated as mutually exclusive by the infant even when the object is visible at the new location and visibly absent from the old location. Perseverative error cannot therefore simply be a memory problem. Possible explantions are discussed.     

The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.)

We analyzed sucrose responsiveness and associative tactile learning in two genetic strains of honey bees under laboratory conditions. These strains differ in their foraging behavior. Bees of the "high" strain preferentially collect pollen. "Low"-strain bees mainly forage for nectar. Responsiveness to different sucrose concentrations and tactile learning were examined using the proboscis extension reflex. Acquisition, extinction of conditioned responses, and responses to an alternative tactile stimulus were tested. High-strain bees are more responsive to sucrose than low-strain bees. Regardless of genotype, pollen foragers are more responsive to sucrose than nectar foragers. In bees of both strains we find the same relationship between responsiveness to sucrose and acquisition. Bees responding to low sucrose concentrations show more often the conditioned response during acquisition than those responding only to higher sucrose concentrations. Extinction of conditioned responses depends on the response probability during acquisition. Discrimination between the two tactile stimuli is affected by genotype but not by responsiveness to sucrose. High-strain bees discriminate better than low-strain bees. Our experiments thus establish links between division of labor, responsiveness to sucrose, and associative learning in honey bees.     

Early Development of Mushroom Bodies in the Brain of the Honeybee Apis mellifera as Revealed by BrdU Incorporation and Ablation Experiments

In the honeybee the mushroom bodies are prominent neuropil structures arranged as pairs in the dorsal protocerebrum of the brain. Each mushroom body is composed of a medial and a lateral subunit. To understand their development, the proliferation pattern of mushroom body intrinsic cells, the Kenyon cells, were examined during larval and pupal stages using the bromodeoxyuridine (BrdU) technique and chemical ablation with hydroxyurea.     

Learning and teaching (briefly)

This paper was given as the Annual Ellen Noonan Counselling Lecture on July 2012 and retains some of the spoken style of the lecture. It uses examples of Ellen Noonan’s work to examine aspects of the process of teaching and learning psychodynamic practice. The difficulties of how to embed theoretical knowledge with its clinical application are discussed and the question of what are the key skills of the self-reflective practitioner is raised with reference to whether, and how, they can be taught or learnt. It is suggested that part of this process consists in helping students, and their teachers, to be more comfortable with not knowing, a concept that is both counter intuitive and counter cultural. From this aspects of contemporary therapeutic practice, with specific reference to psychodynamic short-term therapy, are addressed. The paper looks at the ambivalence felt by many psychodynamic clinicians towards working within a short-term paradigm in current workplace settings and how this might be addressed. The paper discusses the intrinsic qualities of a psychodynamic short-term approach and its relation to contemporary therapeutic modalities. It is suggested that the increasing managerial culture, leading to the ascendance of protocol driven, manualised and structured therapies, represents an attack on the relational and must be challenged.     

Differential Development of Learning Strategies on a Pictorial Verbal Learning Test (PVLT) in Primary-School Children

The aim of this study was to test the hypothesis that developmental differences exist in the use of learning strategies in primary school children. Serial and subjective clustering in a multitrial Pictorial Verbal Learning Test (PVLT) were compared in 79 children aged 6–12. Correlation analyses indicated that serial clustering yielded better performance when information was presented on the initial trials of the test. Subjective clustering was superior when information was presented repeatedly, i.e., after three or more trials. Analyses of variance indicated that subjective clustering was used more often in older children with repeated presentations. On the other hand, there was no increase in the use of serial clustering with age and with repeated presentations. The findings imply that training in the use of proper strategies could have benefit for children who use an inefficient learning strategy and/or have a learning problem. In addition, they point to the importance of the factor “age” in relation to the way information is presented to children.