Indicators of Early and Late Processing Reveal the Importance of Within-Trial-Time for Theories of Associative Learning

In four human learning experiments (Pavlovian skin conductance, causal learning, speeded classification task), we evaluated several associative learning theories that assume either an elemental (modified unique cue model and Harris’ model) or a configural (Pearce’s configural theory and an extension of it) form of stimulus processing. The experiments used two modified patterning problems (A/B/C+, AB/BC/AC+ vs. ABC-; A+, BC+ vs. ABC-). Pearce’s configural theory successfully predicted all of our data reflecting early stimulus processing, while the predictions of the elemental theories were in accord with all of our data reflecting later stages of stimulus processing. Our results suggest that the form of stimulus representation depends on the amount of time available for stimulus processing. Our findings highlight the necessity to investigate stimulus processing during conditioning on a finer time scale than usually done in contemporary research.     

Acquisition of discriminations involving ambiguous or non-ambiguous features: an evaluation of two configural learning models

The present rat experiment evaluated the validity of two formal accounts of configural learning in the framework of discrimination tasks involving the serial presentation of feature and target stimuli: Rescorla's (1973) modification of the Rescorla-Wagner model (1972) and the Pearce model (1987). The first, ambiguous feature task was of the form X-->A+, Y-->A-, X-->B-, Y-->B+, in which X and Y represent visual features, '-->' signifies a serial arrangement, A and B are auditory target stimuli, and '+' and '-' symbolise food-reinforcement and non-reinforcement, respectively. The second, non-ambiguous feature task was of the form: X-->A+, Y-->A-, X-->B+, Y-->B-. The former task was much more difficult to solve than was the latter task. The Rescorla model is able to account for the observed differences between the two tasks in learning rates and in the associative strength of feature X with more plausible parameter values than is the Pearce model. It is suggested that models acknowledging a role for both elemental and configural learning can better account for discrimination learning in discrimination tasks of the sort presented in this study than do models that exclusively allow for configural learning.     

Eye-specific learning of routes and “signposts” by walking honeybees

This study investigates the honeybee's ability to learn routes based on visual stimuli presented to a single eye, and to then navigate these routes using the other (naive) eye. Bees were trained to walk through a narrow tunnel carrying visual stimuli on the two walls. At the end of the tunnel the bees had to choose between two arms, one of which led to a feeder. In a first experiment, bees had to learn to choose the left arm to get a reward when the right wall carried a yellow grating, but the right arm when the left wall carried a blue grating. The bees learned this task well, indicating that stimuli encountered by different eyes could be associated with different routes. In a second experiment, bees had to turn left when the right eye saw a blue grating, but to the right when the same eye saw a yellow grating. They also learned this task well. In subsequent tests, they chose the correct arm even when these gratings were presented to the untrained eye. These results suggest that there is interocular transfer of route-specific learning with respect to visual stimuli that function as navigational “signposts”. Accepted: 18 December 1997     

Fruit flies can learn non-elemental olfactory discriminations

Associative learning allows animals to establish links between stimuli based on their concomitance. In the case of Pavlovian conditioning, a single stimulus A (the conditional stimulus, CS) is reinforced unambiguously with an unconditional stimulus (US) eliciting an innate response. This conditioning constitutes an ‘elemental’ association to elicit a learnt response from A⁺ without US presentation after learning. However, associative learning may involve a ‘complex’ CS composed of several components. In that case, the compound may predict a different outcome than the components taken separately, leading to ambiguity and requiring the animal to perform so-called non-elemental discrimination. Here, we focus on such a non-elemental task, the negative patterning (NP) problem, and provide the first evidence of NP solving in Drosophila. We show that Drosophila learn to discriminate a simple component (A or B) associated with electric shocks (+) from an odour mixture composed either partly (called ‘feature-negative discrimination’ A⁺ versus AB⁻) or entirely (called ‘NP’ A⁺B⁺ versus AB⁻) of the shock-associated components. Furthermore, we show that conditioning repetition results in a transition from an elemental to a configural representation of the mixture required to solve the NP task, highlighting the cognitive flexibility of Drosophila.     

蜜蜂对复合气味中特征因素的选择性记忆巩固的研究

目的 蜜蜂天生具有丰富的嗅觉辨识能力,觅食、交配、导航以及社交活动均依赖其嗅觉系统,是研究嗅觉感知和学习记忆的行为及神经机制的理想模型。蜜蜂既能够将某个复合气味作为一个整体也可以将复合气味的各组成成分进行辨别和区分,但是在特征依赖的联合记忆中依据何种原则进行加工并存储到长期记忆还不清楚。方法 本文利用特征阳性（feature positive：AB+,B-）和特征阴性（feature negative：AB-,B+）的奖赏性嗅觉条件化,训练蜜蜂对复合气味和成分气味的辨别,并检测蜜蜂对复合气味（AB）、成分气味（B）以及特征气味（A）的中长时记忆（3 h）和长时记忆（24 h）。结果 在特征阳性的奖赏性嗅觉条件化中,蜜蜂对训练过的气味可以形成稳定的中长时和长时记忆,并且对复合气味中的特征气味的记忆与复合气味的记忆呈现高度相似。但在特征阴性的奖赏性嗅觉条件化中,蜜蜂虽能够在3 h和24 h对训练过的两种气味具有显著的伸喙反应差异,且对特征阴性的气味无显著反应,但对复合气味的反应随时间的推移而增加。结论 实验结果表明,蜜蜂选择性地将与奖赏信息联合出现的气味巩固到长时记忆中,但并未依据特征成分加工储存到长时记忆中。奖赏信息预示着食物源,与生存息息相关,表明对环境信息进行选择性的记忆巩固加工并储存可能是低等动物高效地编码生存相关信息的重要策略。     

Effects of conditioning history on selective stimulus control by elements of compound discriminative stimuli

Effects of prior discrimination training on stimulus control by color and shape dimensions of compound stimuli were studied with college students. In Phase 1, single-stimulus discrimination training was conducted for two values of color and shape. Phase 2 discrimination training employed two 2-dimensional compound stimuli composed of the color and shape stimuli trained in Phase 1. For conflict-compound stimuli, the stimulus-response-consequence contingency was altered between phases for one stimulus dimension (target dimension), but not for the other, non-target, dimension. Level of congruence (100%, 25%, and 0%) of the contingency for the target dimension between phases was manipulated across groups. When each stimulus value was tested in Phase 3, level of Phase-2-consistent responding to the target dimension varied with level of Phase-1-to-Phase-2 congruence. In Experiment 2, training history for the non-target dimension was altered across three conditions: (a) Correlated with reinforcement, as in Experiment 1, (b) No-Training, or (c) Not-Correlated. Phase-2-consistent responding to the target cue in Phase 3 was lower under the latter conditions than under the Correlated condition, indicating that the non-target dimension modulated control by the target dimension, consistent with stimulus competition. The data suggest elemental, rather than configural processing of the compound stimuli during Phase 2.     

Transverse patterning in pigeons

The ability of pigeons to form configural stimulus representations was assessed in two operant discrimination experiments. In Experiment 1 the transverse patterning problem of Spence (1952) was trained. In Phase 1, subjects had to choose stimulus A on A + B — trials; B + C — trials were added in Phase 2. In Phase 3, the first two pairs were combined with C + A — trials. The success of the subjects was simulated by a model assuming that elemental and configural stimulus representations coexist in a stable proportion, even in the phases of the experiment which do not require configural stimulus representations for successful solution. Experiment 2 replicated the first two phases of Experiment 1, but trained A + C — in Phase 3. Comparison of the results of this experiment with simulations of the model showed that elemental and configural stimulus representations coexisted in similar proportions as in Experiment 1, even though they were not necessary for successful task solution.     

Blue colour preference in honeybees distracts visual attention for learning closed shapes

Spatial vision is an important cue for how honeybees (Apis mellifera) find flowers, and previous work has suggested that spatial learning in free-flying bees is exclusively mediated by achromatic input to the green photoreceptor channel. However, some data suggested that bees may be able to use alternative channels for shape processing, and recent work shows conditioning type and training length can significantly influence bee learning and cue use. We thus tested the honeybees’ ability to discriminate between two closed shapes considering either absolute or differential conditioning, and using eight stimuli differing in their spectral characteristics. Consistent with previous work, green contrast enabled reliable shape learning for both types of conditioning, but surprisingly, we found that bees trained with appetitive-aversive differential conditioning could additionally use colour and/or UV contrast to enable shape discrimination. Interestingly, we found that a high blue contrast initially interferes with bee shape learning, probably due to the bees innate preference for blue colours, but with increasing experience bees can learn a variety of spectral and/or colour cues to facilitate spatial learning. Thus, the relationship between bee pollinators and the spatial and spectral cues that they use to find rewarding flowers appears to be a more rich visual environment than previously thought.     

Chromatic and achromatic stimulus discrimination of long wavelength (red) visual stimuli by the honeybee Apis mellifera

It has long been assumed that bees cannot see red. However, bees visit red flowers, and the visual spectral sensitivity of bees extends into wavelengths to provide sensitivity to such flowers. We thus investigated whether bees can discriminate stimuli reflecting wavelengths above 560 nm, i.e., which appear orange and red to a human observer. Flowers do not reflect monochromatic (single wavelength) light; specifically orange and red flowers have reflectance patterns which are step functions, we thus used colored stimuli with such reflectance patterns. We first conditioned honey bees Apis mellifera to detect six stimuli reflecting light mostly above 560 nm and found that bees learned to detect only stimuli which were perceptually very different from a bee achromatic background. In a second experiment we conditioned bees to discriminate stimuli from a salient, negative (un-rewarded) yellow stimulus. In subsequent unrewarded tests we presented the bees with the trained situation and with five other tests in which the trained stimulus was presented against a novel one. We found that bees learned to discriminate the positive from the negative stimulus, and could unambiguously discriminate eight out of fifteen stimulus pairs. The performance of bees was positively correlated with differences between the trained and the novel stimulus in the receptor contrast for the long-wavelength bee photoreceptor and in the color distance (calculated using two models of the honeybee colors space). We found that the differential conditioning resulted in a concurrent inhibitory conditioning of the negative stimulus, which might have improved discrimination of stimuli which are perceptually similar. These results show that bees can detect long wavelength stimuli which appear reddish to a human observer. The mechanisms underlying discrimination of these stimuli are discussed. Handling Editor: Lars Chittka.     

The forest or the trees: preference for global over local image processing is reversed by prior experience in honeybees

Traditional models of insect vision have assumed that insects are only capable of low-level analysis of local cues and are incapable of global, holistic perception. However, recent studies on honeybee (Apis mellifera) vision have refuted this view by showing that this insect also processes complex visual information by using spatial configurations or relational rules. In the light of these findings, we asked whether bees prioritize global configurations or local cues by setting these two levels of image analysis in competition. We trained individual free-flying honeybees to discriminate hierarchical visual stimuli within a Y-maze and tested bees with novel stimuli in which local and/or global cues were manipulated. We demonstrate that even when local information is accessible, bees prefer global information, thus relying mainly on the object''s spatial configuration rather than on elemental, local information. This preference can be reversed if bees are pre-trained to discriminate isolated local cues. In this case, bees prefer the hierarchical stimuli with the local elements previously primed even if they build an incorrect global configuration. Pre-training with local cues induces a generic attentional bias towards any local elements as local information is prioritized in the test, even if the local cues used in the test are different from the pre-trained ones. Our results thus underline the plasticity of visual processing in insects and provide new insights for the comparative analysis of visual recognition in humans and animals.     

Neonatal representation of odour objects: distinct memories of the whole and its parts

Extraction of relevant information from highly complex environments is a prerequisite to survival. Within odour mixtures, such information is contained in the odours of specific elements or in the mixture configuration perceived as a whole unique odour. For instance, an AB mixture of the element A (ethyl isobutyrate) and the element B (ethyl maltol) generates a configural AB percept in humans and apparently in another species, the rabbit. Here, we examined whether the memory of such a configuration is distinct from the memory of the individual odorants. Taking advantage of the newborn rabbit''s ability to learn odour mixtures, we combined behavioural and pharmacological tools to specifically eliminate elemental memory of A and B after conditioning to the AB mixture and evaluate consequences on configural memory of AB. The amnesic treatment suppressed responsiveness to A and B but not to AB. Two other experiments confirmed the specific perception and particular memory of the AB mixture. These data demonstrate the existence of configurations in certain odour mixtures and their representation as unique objects: after learning, animals form a configural memory of these mixtures, which coexists with, but is relatively dissociated from, memory of their elements. This capability emerges very early in life.     

Elemental and configural olfactory coding by antennal lobe neurons of the honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

When smelling an odorant mixture, olfactory systems can be analytical (i.e. extract information about the mixture elements) or synthetic (i.e. creating a configural percept of the mixture). Here, we studied elemental and configural mixture coding in olfactory neurons of the honeybee antennal lobe, local neurons in particular. We conducted intracellular recordings and stimulated with monomolecular odorants and their coherent or incoherent binary mixtures to reproduce a temporally dynamic environment. We found that about half of the neurons responded as ‘elemental neurons’, i.e. responses evoked by mixtures reflected the underlying feature information from one of the components. The other half responded as ‘configural neurons’, i.e. responses to mixtures were clearly different from responses to their single components. Elemental neurons divided in late responders (above 60 ms) and early responder neurons (below 60 ms), whereas responses of configural coding neurons concentrated in-between these divisions. Latencies of neurons with configural responses express a tendency to be faster for coherent stimuli which implies employment in different processing circuits.     

Localization of the violet and yellow receptor cells in the crayfish retinula

Cellular identification of color receptors in crayfish compound eyes has been made by selective adaptation at 450 nm and 570 nm, wavelengths near the λ_max''s of the two retinular cell classes previously demonstrated. By utilizing earlier evidence, the concentration of lysosome-related bodies (LRB) was used to measure relative light adaptation and thus wavelength sensitivity in 665 retinular cells from six eyes. The observed particle distributions demonstrate the following. Both violet and yellow receptors occur ordinarily in each retinula. Of the seven regular retinular cells two (R₃ and R₄ using Eguchi''s numbering [1965]) have mean sensitivities significantly greater to violet and less to yellow than the other five. The latter apparently comprise "pure" yellow receptors (R₁ and R₇) and mixed yellow and violet receptors (R₂, R₅, and R₆). Explanations of such ambiguity requiring two visual pigments in single retinular cells or intercellular coupling of adjacent neuroreceptors are apparently precluded by previous evidence. Present data imply alternatively some positional variability in the violet pair''s location in individual retinulas. Thus R₃ and R₄ are predominantly the violet receptors but in some retinulas R₂ and R₃ or R₄ and R₅ (or rarely some other cell pairs) may be. The retinal distribution of such variations has yet to be determined. In agreement with intracellular recordings the blue and yellow cells here identified belong to both the vertical and horizontal e-vector sensitive channels.     

Input coding in animal and human associative learning

Two appetitive conditioning experiments with rats investigated whether the degree of generalization between a compound and its component parts is fixed or variable. Both experiments used a two-stage transfer design. In Stage 1, the elemental groups learned that a compound and its component parts signaled the same outcome (i.e. C+, D+, CD+), whereas the configural groups learned that a compound and its component parts signaled different outcomes (i.e. C+, D+, CD-, where '+' is pellets and '-' is no pellets). In Stage 2, the rats were tested for reductions in generalization. Experiment 1 found no evidence that past configural learning reduced generalization when a new set of alike-treated A and B elements were presented in compound for the first time. Experiment 2 found no evidence that past configural learning reduced generalization when the stimuli of Stage 1 were presented in a new C-, D-, CD+ relation. In contrast to findings with humans, these results suggest that past experience plays a minor role in how stimuli are encoded in animal conditioning.     

Pattern recognition in honeybees: eidetic imagery and orientation discrimination

The roles of eidetic imagery and orientational cues, respectively, in the discrimination of visual patterns by honeybees (Apis mellifera) were evaluated by training the bees to discriminate between patterns consisting of periodic, black and white square wave gratings. Training and tests with a number of different pairs of patterns revealed that bees use orientational cues almost exclusively, if such are present, and make use of eidetic images only when orientational cues are not available. On the other hand, if a pattern carries strong orientational cues, bees learn the orientation even if it is irrelevant to the discrimination task on which they are trained.     

Olfactory learning in the stingless bee Tetragonisca angustula (Hymenoptera, Apidae, Meliponini)

Tetragonisca angustula stingless bees are considered as solitary foragers that lack specific communication strategies. In their orientation towards a food source, these social bees use chemical cues left by co-specifics and the information obtained in previous foraging trips by the association of visual stimuli with the food reward. Here, we investigated their ability to learn the association between odors and reward (sugar solution) and the effect on learning of previous encounters with scented food either inside the hive or during foraging. During food choice experiments, when the odor associated with the food was encountered at the feeding site, the bees’ choice is biased to the same odor afterwards. The same was not the case when scented food was placed inside the nest. We also performed a differential olfactory conditioning of proboscis extension response with this species for the first time. Inexperienced bees did not show significant discrimination levels. However, when they had had already interacted with scented food inside the hive, they were able to learn the association with a specific odor. Possible olfactory information circulation inside the hive and its use in their foraging strategies is discussed.     

Visual discrimination abilities in the gray bamboo shark (Chiloscyllium griseum)

This study assessed visual discrimination abilities in bamboo sharks (Chiloscyllium griseum). In a visual discrimination task using two-dimensional (2D) geometric stimuli, sharks learned to distinguish between a square, being the positive (rewarded) stimulus, and several negative stimuli, such as two differently sized triangles, a circle, a rhomboid and a cross. Although the amount of sessions to reach the learning criterion and the average trial time needed to solve each new task did not vary significantly, the number of correct choices per session increased significantly with on-going experiments. The results indicate that the sharks did not simply remember the positive stimulus throughout the different training phases. Instead, individuals also seemed to learn each negative symbol and possibly had to “relearn” at least some aspects of the positive stimulus during each training phase. The sharks were able to distinguish between the 2D stimulus pairs at a learning rate corresponding to that found in teleosts. As expected, it took the sharks longer to learn a reversal task (with the positive stimulus now being the negative one) than to discriminate between the other stimulus pairs. Nevertheless, the present results suggest that bamboo sharks can learn visual discrimination tasks, succeed in a reversal task and probably retain (some) information about a previously learned task when progressing to a new one.     

Goldfish's visual information processing patterns in food-reinforced discrimination learning between compound visual stimuli

Summary To examine how goldfish process and store information on compound visual stimuli, goldfish were trained with visual discriminative stimuli composed of varied colors and patterns using a Y-maze instrumental conditioning technique. The fish showed some very different types of information processing patterns depending upon the degree of discrimination difficulty of each constituent aspect (color and pattern). Those trained with compound stimuli with both a more easily discriminated aspect and a more difficult aspect learned the former selectively but did not learn the latter at all in spite of a high rate of training. Contrary to this, the fish trained with compound stimuli composed of two aspects with similar degrees of discrimination difficulty learned both aspects. In this case, only when fish were trained with compound stimuli composed of relatively more difficult aspects did they learn to discriminate between the stimuli more rapidly than the fish in each group trained with the constituent colored or patterned stimuli. These results were discussed in relation to visual processing patterns reported in other species and the mechanism of aspect selection.Abbreviations CP compound stimuli composed of VR and HB (7-mm ISBBs) - Cp compound stimuli composed of VR and HB (14-mm ISBBs) - cP compound stimuli composed of VG and HB (7-mm ISBBs) - cp compound stimuli composed of VG and HB (14-mm ISBBs) - HB horizontal patterns on blue background - HGra horizontal patterns on gray background - ISBBs interval spaces between bars - VG vertical patterns on green background - VGra vertical patterns on gray background - VR vertical patterns on red background     

Olfactory learning and behaviour are ‘insulated’ against visual processing in larval Drosophila

We investigate the organization of behaviour across sensory modalities, using larval Drosophila melanogaster. We ask whether olfactory learning and behaviour are affected by visual processing. We find that: (1) Visual choice does not affect concomitant odour choice. (2) Visual context does not influence odour learning, nor do changes of visual context between training and test affect retrieval of odour memory. (3) Larvae cannot solve a biconditional discrimination task, despite generally permissive conditions. In this task, larvae are required to establish conditional associations: in light, one odour is rewarded and the other one is not, whereas in dark the opposite contingency is established. After such training, choice between the two odours is equal under light and dark testing conditions, suggesting that larvae do not establish odour memories specifically for one visual context only. Together, these data suggest that, in larval Drosophila, olfactory learning and behaviour are ‘insulated’ against visual processing.     

No evidence for early modulation of evoked responses in primary visual cortex to irrelevant probe stimuli presented during the attentional blink

Background

During rapid serial visual presentation (RSVP), observers often miss the second of two targets if it appears within 500 ms of the first. This phenomenon, called the attentional blink (AB), is widely held to reflect a bottleneck in the processing of rapidly sequential stimuli that arises after initial sensory registration is complete (i.e., at a relatively late, post-perceptual stage of processing). Contrary to this view, recent fMRI studies have found that activity in the primary visual area (V1), which represents the earliest cortical stage of visual processing, is attenuated during the AB. Here we asked whether such changes in V1 activity during the AB arise in the initial feedforward sweep of stimulus input, or instead reflect the influence of feedback signals from higher cortical areas.

Methodology/Principal Findings

EEG signals were recorded while participants monitored a sequential stream of distractor letters for two target digits (T1 and T2). Neural responses associated with an irrelevant probe stimulus presented simultaneously with T2 were measured using an ERP marker – the C1 component – that reflects initial perceptual processing of visual information in V1. As expected, T2 accuracy was compromised when the inter-target interval was brief, reflecting an AB deficit. Critically, however, the magnitude of the early C1 component evoked by the probe was not reduced during the AB.

Conclusions/Significance

Our finding that early sensory processing of irrelevant probe stimuli is not suppressed during the AB is consistent with theoretical models that assume that the bottleneck underlying the AB arises at a post-perceptual stage of processing. This suggests that reduced neural activity in V1 during the AB is driven by re-entrant signals from extrastriate areas that regulate early cortical activity via feedback connections with V1.