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.     

Learning in honey bees with brain lesions: how partial mushroom-body ablations affect sucrose responsiveness and tactile antennal learning

Honey bees are ideal organisms for studying associative learning, because they can rapidly learn different sensory cues, even under laboratory conditions. Classical olfactory learning experiments have shown that the mushroom bodies (MBs), a prominent neuropil of the central nervous system of the bee, are involved in olfactory learning and memory formation. We tested whether the MBs are also involved in tactile antennal learning. As in olfactory learning, bees use the antennae during tactile learning to sense tactile cues. We produced specific MB ablations by applying the mitotic blocker hydroxyurea (HU). In Drosophila, HU-induced brain lesions of the MBs strongly impaired olfactory memory formation. As treatment with HU might also interfere with the processing of the reward stimulus, sucrose, we measured the responsiveness to sucrose stimuli in these bees. Treatment with HU led to partial ablations of the median MB sub-units on one or both sides of the brain. We analysed side-specific effects in double-blind tests, testing sucrose responsiveness separately for each antenna, and conditioning first one antenna and then the other in a reversal learning assay. HU-treated bees without detectable ablations were less responsive to sucrose and had a poorer learning performance than untreated controls. Partial MB ablation did not additionally affect responsiveness to sucrose or tactile antennal learning. Interestingly, bees with bilateral MB ablations did not differ from untreated controls in their learning performance during the first learning phase. During reversal learning, acquisition in these bees was significantly lower than that in untreated controls. It is concluded that HU treatment affects sucrose responsiveness and tactile learning even without detectable ablation of neuropils. The effects of MB ablations on tactile learning are not side-specific and not correlated with the volume of the ablated neuropil. Accepted after revision: 15 January 2001 ❚ Electronic Publication     

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.     

Development of an ethanol model using social insects: II. Effect of Antabuse on consumatory responses and learned behavior of the honey bee (Apis mellifera L.)

The ability of Antabuse (disulfiram) to influence ethanol consumption and learning in harnessed honey bees was investigated. In the first series of experiments a factorial design was used with 5 levels of ethanol concentration (0%, 1%, 5%, 10%, 20%), 4 doses of Antabuse (0, 37 microg/g, 3.7 microg/g, .37 microg/g), and 2 testing intervals (1 min., 10 min.). Animals were fed a single 1 microl dose of Antabuse and contact time with an ethanol solution measured. A second series of experiments investigated the influence of Antabuse on the formation of Pavlovian conditioning of the proboscis extension reflex. A factorial design was used with two levels of training (paired, unpaired), three levels of ethanol (0%, 1%, 5%), and 2 levels of pretreatment (distilled water, 3.7 microg/g). Analysis of the consumption experiments indicate that pretreatment with Antabuse reduces ethanol intake, although there was substantial variability. The findings of the Pavlovian experiments suggest that pretreatment with Antabuse significantly reduced responding to a CS signaling the availability of ethanol.     

Sensory responsiveness and the effects of equal subjective rewards on tactile learning and memory of honeybees

In tactile learning, sucrose is the unconditioned stimulus and reward, which is usually applied to the antenna to elicit proboscis extension and which the bee can drink when it is subsequently applied to the extended proboscis. The conditioned stimulus is a tactile object that the bee can scan with its antennae. In this paper we describe the quantitative relationships between gustatory antennal stimulation, gustatory proboscis stimulation, and tactile learning and memory. Bees are 10-fold more responsive to sucrose solutions when they are applied to the antenna compared to proboscis stimulation. During tactile conditioning, the sucrose solution applied to the proboscis determines the level of acquisition, whereas antennal input is of minor importance. Bees differing in their gustatory responsiveness measured at the antenna differ strongly in their tactile acquisition and memory. We demonstrate how these differences in tactile acquisition and memory can be greatly reduced by calculating equal subjective rewards, based on individual gustatory responsiveness.     

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.     

Work engagement,performance, and active learning: The role of conscientiousness

The present study examines whether the relationship between work engagement and job performance is moderated by the extent to which individuals are inclined to work hard, careful, and goal-oriented. On the basis of the literature, it was hypothesized that conscientiousness strengthens the relationship between work engagement and supervisor ratings of task and contextual performance as well as active learning. The hypotheses were tested on a sample of 144 employees from several occupations. Results of moderated structural equation modeling supported the hypotheses. Work engagement was positively related to task performance, contextual performance, and active learning, particularly for employees high in conscientiousness.     

Learning and foraging efficiency in German cockroaches, Blattella germanica (L.) (Insecta: Dictyoptera)

We analysed, under laboratory test conditions, how German cockroach larvae oriented their outgoing foraging trip from their shelter. Our results stressed the importance of external factors, like availability and spatial distribution of food sources, in the choice of a foraging strategy within their home range. When food sources were randomly distributed, larvae adopted a random food search strategy. When food distribution was spatially predictable and reliable, cockroaches were able to relate the presence of food with a landmark during a 3-day training period and to develop an oriented search strategy. Cockroaches were able to associate learned spatial information about their home range to the presence of food resources and then to improve their foraging efficiency. However, conflict experiments revealed that detection of food odour overrode learned landmark cues. Received: 16 October 1999 / Accepted after revision: 18 July 2000     

Differential effects of stress-inducing instructions on anxiety, learning and performance

Marton, F. I., Fransson, A., Jonsson, B., Klenell, A.-Ch. & Roos, B. Differential effects of stress-inducing instructions on anxiety, learning and performance. Scand. J. Psychol., 1973, 14, 213–219.-In an attempt to investigate the effects of induced stress on anxiety, learning and performance, the separate effects on the learning and performance phases were obtained by varying the timing of the introduction and the removal of stressinducing instructions. Stess-inducing instructions had a positive effect on learning but were not significantly related to the level of anxiety in the learning phase. In the performance phase the results were reversed, i.e. the stress-inducing instructions had a significantly positive effect on the level of anxiety but none on performance. The apparent paradox stemming from the significant negative relationship between anxiety and achievement within conditions could be resolved by considering the common confusion concerning statistical vs. causal relationship.     

The role of working memory in motor learning and performance

Three experiments explore the role of working memory in motor skill acquisition and performance. Traditional theories postulate that skill acquisition proceeds through stages of knowing, which are initially declarative but later procedural. The reported experiments challenge that view and support an independent, parallel processing model, which predicts that procedural and declarative knowledge can be acquired separately and that the former does not depend on the availability of working memory, whereas, the latter does. The behaviour of these two processes was manipulated by providing or withholding visual (and auditory) appraisal of outcome feedback. Withholding feedback was predicted to inhibit the use of working memory to appraise success and, thus, prevent the formation of declarative knowledge without affecting the accumulation of procedural knowledge. While the first experiment failed to support these predictions, the second and third experiments demonstrated that procedural and declarative knowledge can be acquired independently. It is suggested that the availability of working memory is crucial to motor performance only when the learner has come to rely on its use.     

Differences in performance on a reversal learning test and division of labor in honey bee colonies

We studied the association between honey bee (Apis mellifera) division of labor and performance on an olfactory reversal-learning test. Manipulations of colony age structure and flight experience were used to test whether differences in performance are associated with age, current behavioral state, or flight experience. Nurse bees showed significantly faster rates of extinction to a learned odor than did foragers. This difference was associated primarily with differences in behavioral state, rather than age; it was seen when comparing nurses and foragers from typical colonies and normal-age nurses and precocious foragers from single-cohort colonies. Differences in extinction rate were not related to differences in flight experience; there was no difference between foragers and foraging-age bees denied flight experience. These results suggest that changes in learning and memory occur in association with division of labor. We speculate on the possible functional significance of the difference in extinction rate between nurses and foragers. Received: 15 January 2000 / Accepted: 22 August 2000     

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 role of participation and control in the effects of computer monitoring on fairness perceptions, task satisfaction, and performance

Procedural justice and social facilitation theories were used to investigate effects of 2 kinds of process control on fairness perceptions, task satisfaction and performance of complex, computer-monitored tasks. A laboratory study manipulated participation (high or low voice) and monitoring approach (monitoring, control over monitoring, or no monitoring). High-voice participants perceived higher justice. Monitored participants reported higher satisfaction with high voice and lower satisfaction with low voice. Task performance was poorer for monitored participants unless they had control over monitoring. Among those with control, performance was not impaired for higher baseline performers. The 2 kinds of process control had different effects on the outcome variables. Results suggest the value of considering variations in the kinds of control provided and the justice principles that may apply in predicting effects of monitoring procedures.     

The role of verbal behavior in human learning: infant performance on fixed-interval schedules

The performances of two infants less than one year old were investigated on fixed-interval schedules. When the infants touched a cylinder either music or food was presented according to fixed-interval schedules ranging in value from 10 to 50 seconds. With respect to two principal criteria, namely, pattern of responding and sensitivity to the schedule parameter, the subjects' behavior closely resembled that of animals but differed markedly from that of older children and adults. Negatively accelerated responding in the course of the fixed interval in the early sessions gave way to a scalloped pattern, consisting of a pause after reinforcement followed by an accelerated response rate. This scalloped pattern was the final form of responding on all schedule values. Analysis of data after performance had stabilized showed that postreinforcement pause was a negatively accelerated increasing function, and running rate (calculated after excluding the postreinforcement pause) was a declining function, of schedule value. On each schedule, the durations of mean successive interresponse times declined in the course of the fixed interval and were directly related to schedule value. The results supported Lowe's (1979) suggestion that verbal behavior may be responsible for major differences in the schedule performance of older humans and animals.     

The role of anticipation and intention in the learning of effects of self-performed actions

The anticipative learning model for acquiring action-effect relations states that the acquisition of action-effect relations depends on processes that are part of action planning, in particular the anticipation of possible effects. Experiment 1 shows that response planning is indeed crucial for the learning of response effects. In this experiment distractors (tones) were presented either during response preparation or in the time interval between response execution and the presentation of a response effect. Response-effect learning was impaired when the distractors were presented during response preparation. The finding is consistent with the assumption that the distractors impaired the anticipation of potential effects and therefore reduced effect learning. In Experiment 2 all responses had two effects. Participants were instructed to produce one of the effects. Under this condition, response-effect learning was only found for the instructed effect, not for the non-instructed effect. The two experiments thus support the view that response-effect learning is selective and depends on the anticipation of potential effects during response planning. The results are discussed in terms of a model that explains both the learning of response-effect relations and the use of these effects for action control within the same theoretical framework.     

Motivating learning, performance, and persistence: the synergistic effects of intrinsic goal contents and autonomy-supportive contexts

Three field experiments with high school and college students tested the self-determination theory hypotheses that intrinsic (vs. extrinsic) goals and autonomy-supportive (vs. controlling) learning climates would improve students' learning, performance, and persistence. The learning of text material or physical exercises was framed in terms of intrinsic (community, personal growth, health) versus extrinsic (money, image) goals, which were presented in an autonomy-supportive versus controlling manner. Analyses of variance confirmed that both experimentally manipulated variables yielded main effects on depth of processing, test performance, and persistence (all ps <.001), and an interaction resulted in synergistically high deep processing and test performance (but not persistence) when both intrinsic goals and autonomy support were present. Effects were significantly mediated by autonomous motivation.     

The effects of hippocampal lesions on learning, memory, and reward expectancies

The hippocampus appears to be critical for the formation of certain types of memories. Hippocampal-lesioned animals fail to exhibit some spatial, contextual, and relational associations. After aspiration lesions of the hippocampus and/or cortex, male rats were allowed to recover for three weeks before being trained on a matching-to-position task. The matching-to-position task was altered to influence the type of cognitive strategies a subject would use to solve the task. The main behavioral manipulation was the reinforcement contingency assignment: Use of a differential outcomes procedure (DOP) or a nondifferential outcomes procedure (NOP). The DOP involves correlating each to-be-remembered event with a distinct reward condition via Pavlovian trace conditioning, whereas the NOP results in random reward contingency. We found that hippocampal lesions did retard learning the matching rule, regardless of the reinforcement contingency assignment. However, when delay intervals were added to the task memory performance of subjects with hippocampal lesions was dramatically impaired--if subjects were not trained with the DOP. When subjects were trained with the DOP, the hippocampal lesion had a marginal effect on delayed memory performance. These findings demonstrate two important points regarding lesions of the hippocampus: (1) hippocampal lesions have a minimal effect on the on the ability of rats to use reward information to solve a delayed discrimination task; (2) rats with hippocampal lesions have the ability to learn about reward information using Pavlovian trace conditioning procedures.     

The mediating role of maternal responsiveness in some longer term effects of postnatal depression on infant development

We hypothesized a mediating role for low maternal responsiveness in certain child developmental deficits found previously to be associated with postnatal depression. Forty depressed inpatients and 48 control (non-depressed) mothers and their infants were followed until 42 months postpartum. Mother–infant interactions were impaired at 6 months postpartum in the depressed group. Subsequent cognitive deficits were found in children's Full Scale IQ on the Wechsler Preschool Primary Scale of Intelligence (Revised) at 42 months of age. Statistical modeling of the mediation hypothesis confirmed that these effects were overwhelmingly explained by lowered maternal responsiveness at 6 months. Similarly, increased temperamental difficulties were apparent in children of depressed mothers but were not correlated with maternal responsiveness. Male infants of depressed mothers were disproportionately vulnerable (compared to females) to impaired cognitive abilities associated with maternal depression. The data concur with previous work and provide empirical support for the theoretical prediction that early disturbances of the mother–infant interaction will mediate some developmental deficits in the children of depressed mothers.