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The configural association theory and the conflict resolution model propose that hippocampal function is involved in learning negative patterning tasks (A+, B+, AB-). The first theory suggests a critical role of the hippocampus in the formation of configural representations of compound stimuli, in which stimuli A and B are presented simultaneously. The second theory hypothesizes that the hippocampus is important for inhibiting the response to a stimulus that is in conflict with response tendencies. Although these theories propose different interpretations of the link between hippocampal function and non-spatial discrimination tasks, they both predict that the hippocampus is involved in the information processing of compound stimuli in negative patterning tasks. Recently, our electrophysiological approach has shown that the hippocampal theta power correlate with response inhibition in a negative patterning task, positive patterning, simultaneous/serial feature negative task. These findings provide strong support for the assumption of the conflict resolution model that the role of the hippocampus in learning is to inhibit responses to conflicting stimuli during non-spatial stimulus discrimination tasks.

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In natural environments, stimuli and events learned by animals usually occur in a combination of more than one sensory modality. An important problem in experimental psychology has been thus to understand how organisms learn about multimodal compounds and how they discriminate this compounds from their unimodal constituents. Here we tested the ability of honey bees to learn bimodal patterning discriminations in which a visual-olfactory compound (AB) should be differentiated from its visual (A) and olfactory (B) elements. We found that harnessed bees trained in classical conditioning of the proboscis extension reflex (PER) are able to solve bimodal positive and negative patterning (NP) tasks. In positive patterning (PP), bees learned to respond significantly more to a bimodal reinforced compound (AB+) than to non-reinforced presentations of single visual (A-) or olfactory (B-) elements. In NP, bees learned to suppress their responses to a non-reinforced compound (AB-) and increase their responses to reinforced presentations of visual (A+) or olfactory (B+) elements alone. We compared the effect of two different inter-trial intervals (ITI) in our conditioning approaches. Whereas an ITI of 8 min allowed solving both PP and NP, only PP could be solved with a shorter ITI of 3 min. In all successful cases of bimodal PP and NP, bees were still able to discriminate between reinforced and non-reinforced stimuli in memory tests performed one hour after conditioning. The analysis of individual performances in PP and NP revealed that different learning strategies emerged in distinct individuals. Both in PP and NP, high levels of generalization were found between elements and compound at the individual level, suggesting a similar difficulty for bees to solve these bimodal patterning tasks. We discuss our results in light of elemental and configural learning theories that may support the strategies adopted by honey bees to solve bimodal PP or NP discriminations.

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Honeybees are models for studying how animals with relatively small brains accomplish complex cognition, displaying seemingly advanced (or "non-elemental") learning phenomena involving multiple conditioned stimuli. These include "peak shift" [1-4]-where animals not only respond to entrained stimuli, but respond even more strongly to similar ones that are farther away from non-rewarding stimuli. Bees also display negative and positive patterning discrimination [5], responding in opposite ways to mixtures of two odors than to individual odors. Since Pavlov, it has often been assumed that such phenomena are more complex than simple associate learning. We present a model of connections between olfactory sensory input and bees' mushroom bodies [6], incorporating empirically determined properties of mushroom body circuitry (random connectivity [7], sparse coding [8], and synaptic plasticity [9, 10]). We chose not to optimize the model's parameters to replicate specific behavioral phenomena, because we were interested in the emergent cognitive capacities that would pop out of a network constructed solely based on empirical neuroscientific information and plausible assumptions for unknown parameters. We demonstrate that the circuitry mediating "simple" associative learning can also replicate the various non-elemental forms of learning mentioned above and can effectively multi-task by replicating a range of different learning feats. We found that PN-KC synaptic plasticity is crucial in controlling the generalization-discrimination trade-off-it facilitates peak shift and hinders patterning discrimination-and that PN-to-KC connection number can affect this trade-off. These findings question the notion that forms of learning that have been regarded as "higher order" are computationally more complex than "simple" associative learning.

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Identifying statistical patterns between environmental stimuli enables organisms to respond adaptively when cues are later observed. However, stimuli are often obscured from detection, necessitating behavior under conditions of ambiguity. Considerable evidence indicates decisions under ambiguity rely on inference processes that draw on past experiences to generate predictions under novel conditions. Despite the high demand for this process and the observation that it deteriorates disproportionately with age, the underlying mechanisms remain unknown. We developed a rodent model of decision-making during ambiguity to examine features of experience that contribute to inference. Rats learned either a simple (positive patterning) or complex (negative patterning) instrumental discrimination between the illumination of one or two lights. During test, only one light was lit while the other relevant light was blocked from physical detection (covered by an opaque shield, rendering its status ambiguous). We found experience with the complex negative patterning discrimination was necessary for rats to behave sensitively to the ambiguous test situation. These rats behaved as if they inferred the presence of the hidden light, responding differently than when the light was explicitly absent (uncovered and unlit). Differential expression profiles of the immediate early gene cFos indicated hippocampal involvement in the inference process while localized microinfusions of the muscarinic antagonist, scopolamine, into the dorsal hippocampus caused rats to behave as if only one light was present. That is, blocking cholinergic modulation prevented the rat from inferring the presence of the hidden light. Collectively, these results suggest cholinergic modulation mediates recruitment of hippocampal processes related to past experiences and transfer of these processes to make decisions during ambiguous situations. Our results correspond with correlations observed between human brain function and inference abilities, suggesting our experiments may inform interventions to alleviate or prevent cognitive dysfunction. © 2015 Wiley Periodicals, Inc.

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