Color modulates olfactory learning in honeybees by an occasion-setting mechanism

A sophisticated form of nonelemental learning is provided by occasion setting. In this paradigm, animals learn to disambiguate an uncertain conditioned stimulus using alternative stimuli that do not enter into direct association with the unconditioned stimulus. For instance, animals may learn to discriminate odor rewarded from odor nonrewarded trials if these two situations are indicated by different colors that do not themselves become associated with the reward. Despite a growing interest in nonelemental learning in insects, no study has so far attempted to study occasion setting in restrained honeybees, although this would allow direct access to the neural basis of nonelemental learning. Here we asked whether colors can modulate olfactory conditioning of the proboscis extension reflex (PER) via an occasion-setting mechanism. We show that intact, harnessed bees are not capable of learning a direct association between color and sucrose. Despite this incapacity, bees solved an occasion-setting discrimination in which colors set the occasion for appropriate responding to an odor that was rewarded or nonrewarded depending on the color. We therefore provide the first controlled demonstration of bimodal (color-odor) occasion setting in harnessed honeybees, which opens the door for studying the neural basis of such bimodal, nonelemental discriminations in insects.     

Food approach conditioning and discrimination learning using sound cues in benthic sharks

The marine environment is filled with biotic and abiotic sounds. Some of these sounds predict important events that influence fitness while others are unimportant. Individuals can learn specific sound cues and ‘soundscapes’ and use them for vital activities such as foraging, predator avoidance, communication and orientation. Most research with sounds in elasmobranchs has focused on hearing thresholds and attractiveness to sound sources, but very little is known about their abilities to learn about sounds, especially in benthic species. Here we investigated if juvenile Port Jackson sharks could learn to associate a musical stimulus with a food reward, discriminate between two distinct musical stimuli, and whether individual personality traits were linked to cognitive performance. Five out of eight sharks were successfully conditioned to associate a jazz song with a food reward delivered in a specific corner of the tank. We observed repeatable individual differences in activity and boldness in all eight sharks, but these personality traits were not linked to the learning performance assays we examined. These sharks were later trained in a discrimination task, where they had to distinguish between the same jazz and a novel classical music song, and swim to opposite corners of the tank according to the stimulus played. The sharks’ performance to the jazz stimulus declined to chance levels in the discrimination task. Interestingly, some sharks developed a strong side bias to the right, which in some cases was not the correct side for the jazz stimulus.     

Size-distance paradox with accommodative micropsia

Two experiments tested the hypothesis that the paradoxical relative distance judgment associated with the size-distance paradox is due to the visual system’s assuming equal linear size and perceiving a smaller angular size for the closer stimulus equal in visual angle. In Experiment I, two different sized coins were presented successively, and 16 Ss were asked to give ordinal judgments of apparent distance and apparent size. When the two coins depicted the same figures, the closer stimulus was judged to be farther and smaller, more frequently, than when two coins depicted different figures. In Experiment II, 48 Ss were asked to give ratio judgments of apparent distance, apparent linear size, and apparent angular size for two stimuli which were presented successively. When the stimuli were of equal shape, the mean ratios of the far stimulus to the near stimulus were smaller for the apparent distance but larger for the apparent linear size and angular size than when the stimuli were of different shape. The obtained distance judgments were consistent with the hypothesis but the obtained judgments of linear size and angular size were not.     

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.     

Brain composition and olfactory learning in honey bees

Correlations between brain or brain component size and behavioral measures are frequently studied by comparing different animal species, which sometimes introduces variables that complicate interpretation in terms of brain function. Here, we have analyzed the brain composition of honey bees (Apis mellifera) that have been individually tested in an olfactory learning paradigm. We found that the total brain size correlated with the bees’ learning performance. Among different brain components, only the mushroom body, a structure known to be involved in learning and memory, showed a positive correlation with learning performance. In contrast, visual neuropils were relatively smaller in bees that performed better in the olfactory learning task, suggesting modality-specific behavioral specialization of individual bees. This idea is also supported by inter-individual differences in brain composition. Some slight yet statistically significant differences in the brain composition of European and Africanized honey bees are reported. Larger bees had larger brains, and by comparing brains of different sizes, we report isometric correlations for all brain components except for a small structure, the central body.     

Concept learning set‐size functions for Clark's nutcrackers

Same/Different abstract‐concept learning by Clark's nutcrackers (Nucifraga columbiana) was tested with novel stimuli following learning of training set expansion (8, 16, 32, 64, 128, 256, 512, and 1024 picture items). The resulting set‐size function was compared to those from rhesus monkeys (Macaca mulatta), capuchin monkeys (Cebus apella), and pigeons (Columba livia). Nutcrackers showed partial concept learning following initial eight‐item set learning, unlike the other species (Magnotti, Katz, Wright, & Kelly, 2015). The mean function for the nutcrackers' novel‐stimulus transfer increased linearly as a function of the logarithm of training set size, which intersected its baseline function at the 128‐item set size. Thus, nutcrackers on average achieved full concept learning (i.e., transfer statistically equivalent to baseline performance) somewhere between set sizes of 64 to 128 items, similar to full concept learning by monkeys. Pigeons required a somewhat larger training set (256 items) for full concept learning, but results from other experiments (initial training and transfer with 32‐ and 64‐item set sizes) suggested carryover effects with smaller set sizes may have artificially prolonged the pigeon's full concept learning. We find it remarkable that these diverse species with very different neural architectures can fully learn this same/different abstract concept, and (at least under some conditions) do so with roughly similar sets sizes (64‐128 items) and numbers of training exemplars, despite initial concept learning advantages (nutcrackers), learning disadvantages (pigeons), or increasing baselines (monkeys).     

Intermodal perception at birth: Intersensory redundancy guides newborn infants’ learning of arbitrary auditory−visual pairings

In this study the ability of newborn infants to learn arbitrary auditory–visual associations in the absence versus presence of amodal (redundant) and contingent information was investigated. In the auditory-noncontingent condition 2-day-old infants were familiarized to two alternating visual stimuli (differing in colour and orientation), each accompanied by its ‘own’ sound: when the visual stimulus was presented the sound was continuously presented, independently of whether the infant looked at the visual stimulus. In the auditory-contingent condition the auditory stimulus was presented only when the infant looked at the visual stimulus: thus, presentation of the sound was contingent upon infant looking. On the post-familiarization test trials attention recovered strongly to a novel auditory–visual combination in the auditory-contingent condition, but remained low, and indistinguishable from attention to the familiar combination, in the auditory-noncontingent condition. These findings are a clear demonstration that newborn infants’ learning of arbitrary auditory–visual associations is constrained and guided by the presence of redundant (amodal) contingent information. The findings give strong support to Bahrick’s theory of early intermodal perception.     

Successive olfactory reversal learning in honeybees

Honeybees Apis mellifera can associate an originally neutral odor with a reinforcement of sucrose solution. Forward pairings of odor and reinforcement enable the odor to release the proboscis extension reflex in consecutive tests. Bees can also be conditioned differentially: They learn to respond to a reinforced odor and not to a nonreinforced one. They can also learn to reverse their choice. Here we ask whether honeybees can learn successive olfactory differential conditioning tasks involving different overlapping pairs of odors. The conditioning schedules were established in order to train the animals with 3, 2, 1, or 0 reversals previous to a last differential conditioning phase in which two additional reversals were present. We studied whether or not successive reversal learning is possible and whether or not learning olfactory discrimination reversals affects the solving of subsequent discrimination reversals. Therefore we compared the responses of bees that had experienced reversals with those of bees that had not experienced such reversals when both are confronted with a new reversal situation. In experiment 1 we showed that bees that had experienced three previous reversals were better in solving the final reversal task than bees with no previous reversal experience. In experiment 2, we showed that one reversal learning is enough for bees to perform better in the final reversal task. The successive different reversals trained in our experiments resemble the natural foraging situation in which a honeybee forager has to switch successively from an initial floral species to different ones. The fact that experiencing such changes seems to improve a bee's performance in dealing with further new exploited food sources has therefore an adaptive impact for the individual and for the colony as a whole.     

Instructional control of generalized relational matching to sample in children.

Three experiments examined the performance of 4-year-old children in matching geometric stimuli. Performance was developed as a simulation in which all components of the behavior were overt and directly measured. A correct match depended on the state of an instructional stimulus: the background color of the display. In the first two experiments, on nonidentity trials (signified by a green background) the next longer length, larger size, or greater distance was correct. With a blue background, a comparison identical to the sample was correct. In Experiment 3, red was added for which shorter, smaller, or nearer was correct. Also here, on nonidentity trials, if a comparison of the correct length was not presented, the children adjusted their search target to the comparison of the next succeeding size (larger or smaller) so as to maintain a constant matching relation. Subsequently, when exposure to the instructional stimulus was reduced to presentation only at the beginning of each trial, performance simulated matching based on instructions about abstract relations. In all experiments, accurate matching generalized across novel stimuli and reduced exposure to the instructional stimuli.     

Effects of training condition on the contribution of specific items to relational processing in baboons (Papio papio)

Relational processing involves learning about the relationship between or among stimuli, transcending the individual stimuli, so that abstract knowledge generalizable to novel situations is acquired. Relational processing has been studied in animals as well as in humans, but little attention has been paid to the contribution of specific items to relational thinking or to the factors that may affect that contribution. This study assessed the intertwined effects of item and relational processing in nonhuman primates. Using a procedure that entailed both expanding and contracting sets of pictorial items, we trained 13 baboons on a two-alternative forced-choice task, in which they had to distinguish horizontal from vertical relational patterns. In Experiment 1, monkeys engaged in item-based processing with a small training set size, and they progressively engaged in relation-based processing as training set size was increased. However, in Experiment 2, overtraining with a small stimulus set promoted the processing of item-based information. These findings underscore similarities in how humans and nonhuman primates process higher-order stimulus relations.     

Making Probabilistic Relational Categories Learnable

Theories of relational concept acquisition (e.g., schema induction) based on structured intersection discovery predict that relational concepts with a probabilistic (i.e., family resemblance) structure ought to be extremely difficult to learn. We report four experiments testing this prediction by investigating conditions hypothesized to facilitate the learning of such categories. Experiment 1 showed that changing the task from a category‐learning task to choosing the “winning” object in each stimulus greatly facilitated participants' ability to learn probabilistic relational categories. Experiments 2 and 3 further investigated the mechanisms underlying this “who's winning” effect. Experiment 4 replicated and generalized the “who's winning” effect with more natural stimuli. Together, our findings suggest that people learn relational concepts by a process of intersection discovery akin to schema induction, and that any task that encourages people to discover a higher order relation that remains invariant over members of a category will facilitate the learning of putatively probabilistic relational concepts.     

Configural olfactory learning in honeybees: negative and positive patterning discrimination

In an appetitive context, honeybees (Apis mellifera) learn to associate odors with a reward of sucrose solution. If an odor is presented immediately before the sucrose, an elemental association is formed that enables the odor to release the proboscis extension response (PER). Olfactory conditioning of PER was used to study whether, beyond elemental associations, honeybees are able to process configural associations. Bees were trained in a positive and anegative patterning discrimination problem. In the first problem, single odorants were nonreinforced whereas the compound was reinforced. In the second problem, single odorants were reinforced whereas the compound was nonreinforced. We studied whether bees can solve these problems and whether the ratio between the number of presentations of the reinforced stimuli and the number of presentations of the nonreinforced stimuli affects discrimination. Honeybees differentiated reinforced and nonreinforced stimuli in positive and negative patterning discriminations. They thus can process configural associations. The variation of the ratio of reinforced to nonreinforced stimuli modulated the amount of differentiation. The assignment of singular codes to complex odor blends could be implemented at the neural level: When bees are stimulated with odor mixtures, the activation patterns evoked at the primary olfactory neuropile, the antennal lobe, may be combinations of the single odorant responses that are not necessarily fully additive.     

The impact of arbitrarily applicable relational responding on evaluative learning about hypothetical money and shock outcomes

Evaluative learning comprises changes in preferences after co-occurrences between conditioned stimuli (CSs) and an unconditioned stimulus (US) of affective value. Co-occurrences may involve relational responding. Two experiments examined the impact of arbitrary relational responding on evaluative preferences for hypothetical money and shock outcomes. In Experiment 1, participants were trained to make arbitrary relational responses by placing CSs of the same size but different colours into boxes and were then instructed that these CSs represented different intensities of hypothetical USs (money or shock). Liking ratings of the CSs were altered in accordance with the underlying bigger/smaller than relations. A reversal of preference was also observed: the CS associated with the smallest hypothetical shock was rated more positively than the CS associated with the smallest amount of hypothetical money. In Experiment 2, procedures from Relational Frame Theory (RFT) established a relational network of more than/less than relations consisting of five CSs (A-B-C-D-E). Overall, evaluative preferences were altered, but not reversed, depending on (a) how stimuli had been related to one another during the learning phase and (b) whether those stimuli referred to money or shocks. The contribution of RFT to evaluative learning research is discussed.     

Transformation of the discriminative and eliciting functions of generalized relational stimuli

In three experiments, match-to-sample procedures were used with undergraduates to establish arbitrary relational functions for three abstract visual stimuli. In the presence of samples A, B, and C, participants were trained to select the smallest, middle, and largest member, respectively, of a series of three-comparison arrays. In Experiment 1, the B (choose middle) stimulus was then used to train a steady rate of keyboard pressing before the A (choose smallest) and the C (choose largest) stimuli were presented. Participants pressed slower to A and faster to C than to B. Then B was paired with mild shock in a Pavlovian procedure with skin conductance change as the dependent variable. When presented with A and C, 6 of 8 experimental participants showed smaller skin conductance changes to A and larger skin conductance changes to C than to B. In Experiment 2, A was then used as a sample in a match-to-sample procedure to establish an arbitrary size ranking among four same-sized colored circle comparisons. One of the middle circles was then used to establish a steady rate of pressing before the other circles were presented. Five of 6 participants responded slower to the "smaller" circle and faster to the "larger" circle than they did to the "middle" circle. In Experiment 3, A, B, and C were then presented on a series of test trials requiring participants to pick the comparison that was less than, greater than, or equal to the sample. Novel stimuli were included on some trials. Results indicated that the relational training procedures produced derived relations among the stimuli used in training and that these allowed correct inferences of relative size ranking among novel stimuli.     

A comparison of stimulus set size on tact training for children with autism spectrum disorder

Previous studies on skill acquisition have taught targets in stimulus sets composed of different numbers of stimuli. Although the rationale for selection of a stimulus set size is not clear, the number of target stimuli trained within a set is a treatment decision for which there is limited empirical support. The current investigation compared the efficiency of tact training in 4 stimulus set sizes, each of which included 12 stimuli grouped into (a) 4 sets of 3 stimuli, (b) 3 sets of 4 stimuli, (c) 2 sets of 6 stimuli, and (d) 1 set of 12 stimuli. Results of all 4 participants with autism spectrum disorder show tact training with larger (i.e., 6 and 12) stimulus set sizes was more efficient than training with smaller (i.e., 3 and 4) stimulus set sizes.     

Induction of combination rules in two-dimensional function learning

Previous studies have typically found that when people learn to combine two dimensions of a stimulus to select a response, they learn additive combination rules more easily than nonadditive (e.g., multiplicative) ones. The present experiments demonstrate that in some situations people can learn multiplicative rules more easily than other (e.g., additive) rules. Subjects learned to produce specified response durations when presented with stimulus lines varying in length and angle of orientation. When stimuliand correct responses were related by a multiplicative combination of power functions, learning was relatively easy (Experiment 1). In contrast, systematic response biases occurred during the early phases of learning an additive combination of linear functions (Experiment 2) and a more complex (nonadditive and nonmultiplicative) combination of linear functions (Experiment3), suggesting that people have a tendency to induce a multiplicative combination of power functions. However, the initial biases decreased with practice. These results are explained in terms of a revised adaptive regression model of function learning originally proposed by Koh and Meyer (1991). Differences between the present results and previous results in the literature are discussed.     

Maze Learning by Honeybees

This study examines whether honeybees can learn to fly through complex mazes, in the presence or the absence of specific visual cues. The results are summarized as follows: 1. Bees can learn to fly through a complex maze by following a trail of colored marks. 2. Bees, initially trained to follow color marks through an initial part of the maze, are immediately able to use the same sign-tracking cue to find their way through the rest of the maze, which is unfamiliar to them. 3. Bees trained to follow color marks through a particular maze can use the same cue to negotiate a novel maze. 4. Bees trained to use a particular color to negotiate a maze can immediately use a novel color to negotiate the same maze or even a novel maze. 5. After learning to negotiate a maze by following colored marks, bees can find their way through the maze even when the marks are removed, albeit at reduced levels of accuracy. Thus, the trained bees do not rely solely on sign-tracking to find their way through the maze: they also acquire a spatial memory of the maze or at least a sequence of motor commands describing the correct path through it. 6. Bees can learn to use color as a signal even when it indicates the path through the maze in a symbolic way, for example, blue indicating a turn to the right and green a turn to the left. 7. Bees can learn an unmarked maze. Performance under these conditions is poorer than when marks are provided, but is still significantly better than chance level. 8. Control experiments rule out the use of external landmarks in all of these situations.     

Aversive learning overcomes appetitive innate responding in honeybees

Despite their miniature brain, honeybees have emerged as a powerful model for the study of learning and memory. Yet, they also exhibit innate responses to biologically relevant social signals such as pheromones. Here, we asked whether the bees’ developed learning capabilities allow them to overcome hardwired appetitive responses. Can they learn that attractant pheromones, that are not normally associated with a noxious stimulation in nature, predict the punishment of an electric shock? Immobilized honeybees were trained to discriminate two odorants, one that was paired with a shock and another that had no consequences. We measured whether they learned to produce aversive sting extension responses to the punished but not the non-punished odorant. One odorant was a neutral odor without innate value while the other was either an attractive pheromone (geraniol or citral) or an attractive floral odorant (phenylacetaldehyde). In all cases, bees developed a conditioned aversive response to the punished odorant, be it pheromone or not, and efficiently retrieved this information 1 h later. No learning asymmetries between odors were found. Thus, associative aversive learning in bees is strong enough to override preprogrammed responding, thus reflecting an impressive behavioral flexibility.     

Acquisition of a relative class concept by an African gray parrot (Psittacus erithacus): discriminations based on relative size

We report that an African gray parrot (Psittacus erithacus), Alex, responds to stimuli on a relative basis. Previous laboratory studies with artificial stimuli (such as pure tones) suggest that birds make relational responses as a secondary strategy, only after they have acquired information about the absolute values of the stimuli. Alex, however, after learning to respond to a small set of exemplars on the basis of relative size, transferred this behavior to novel situations that did not provide specific information about the absolute values of the stimuli. He responded to vocal questions about which was the larger or smaller exemplar by vocally labeling its color or material, and he responded "none" if the exemplars did not differ in size. His overall accuracy was 78.7%.     

Honeybee Memory: Navigation by Associative Grouping and Recall of Visual Stimuli

Studies of navigation in bees and ants are beginning to reveal that foraging insects traveling repeatedly to a food source navigate by using a series of visual images of the environment acquired en route (Collett, 1996; Collett et al., 1993; Judd & Collett, 1998; Wehner et al., 1990, 1996). By comparing the currently viewed scene with the appropriate stored image, the insect is able to ascertain whether or not it is on the correct path and make any necessary corrections. If a bee happens to forage at more than one site, then she needs not only to memorize a separate set of images for each route that she has learned but also to retrieve the set of images that is appropriate to each route. Here we examine the bee's capacity to learn and later retrieve from memory two different sets of visual stimuli. Bees were trained to fly through a compound Y-maze where they were presented alternately with two different sequences of visual stimuli on their route to a food reward. We find that bees can indeed store two different sequences of images simultaneously. Furthermore, the trained bees are able to classify the memorized images into two groups, one pertaining to each three-stimulus set. Exposure to any of the images pertaining to one set triggers recall of all of the other images associated with that set. Associative grouping and recall of visual stimuli, demonstrated here for the first time in honeybees, provide an effective means of retrieving the appropriate navigational information from memory.