Highlights d Medial prefrontal cortex (mPFC) persistently encodes valuebased decision variables d Relative value signals are stable, and total value signals decay d Persistent decision variables are weakly represented in premotor cortex d mPFC projections to dorsomedial striatum persistently represent decision variables

Foraging animals must use decision-making strategies that dynamically account for uncertainty in the world. To cope with this uncertainty, animals have developed strikingly convergent strategies that use information about multiple past choices and reward to learn representations of the current state of the world. However, the underlying learning rules that drive the required learning have remained unclear. Here, working in the relatively simple nervous system of Drosophila, we combine behavioral measurements, mathematical modeling, and neural circuit perturbations to show that dynamic foraging depends on a learning rule incorporating reward expectation. Using a novel olfactory dynamic foraging task, we characterize the behavioral strategies used by individual flies when faced with unpredictable rewards and show, for the first time, that they perform operant matching. We build on past theoretical work and demonstrate that this strategy requires the existence of a covariance-based learning rule in the mushroom body - a hub for learning in the fly. In particular, the behavioral consequences of optogenetic perturbation experiments suggest that this learning rule incorporates reward expectation. Our results identify a key element of the algorithm underlying dynamic foraging in flies and suggest a comprehensive mechanism that could be fundamental to these behaviors across species.

No abstract

In neuroscience, the structure of a circuit has often been used to intuit function-an inversion of Louis Kahn's famous dictum, "Form follows function" (Kristan and Katz, 2006). However, different brain networks may use different network architectures to solve the same problem. The olfactory circuits of two insects, the locust, Schistocerca americana, and the fruit fly, Drosophila melanogaster, serve the same function-to identify and discriminate odors. The neural circuitry that achieves this shows marked structural differences. Projection neurons (PNs) in the antennal lobe innervate Kenyon cells (KCs) of the mushroom body. In locust, each KC receives inputs from ;50% of PNs, a scheme that maximizes the difference between inputs to any two of ;50,000 KCs. In contrast, in Drosophila, this number is only 5% and appears suboptimal. Using a computational model of the olfactory system, we show that the activity of KCs is sufficiently high-dimensional that it can separate similar odors regardless of the divergence of PN-KC connections. However, when temporal patterning encodes odor attributes, dense connectivity outperforms sparse connections. Increased separability comes at the cost of reliability. The disadvantage of sparse connectivity can be mitigated by incorporating other aspects of circuit architecture seen in Drosophila. Our simulations predict that Drosophila and locust circuits lie at different ends of a continuum where the Drosophila gives up on the ability to resolve similar odors to generalize across varying environments, while the locust separates odor representations but risks misclassifying noisy variants of the same odor.

Memory guides behavior across widely varying environments and must therefore be both sufficiently specific and general. A memory too specific will be useless in even a slightly different environment, while an overly general memory may lead to suboptimal choices. Animals successfully learn to both distinguish between very similar stimuli and generalize across cues. Rather than forming memories that strike a balance between specificity and generality, Drosophila can flexibly categorize a given stimulus into different groups depending on the options available. We asked how this flexibility manifests itself in the well-characterized learning and memory pathways of the fruit fly. We show that flexible categorization in neuronal activity as well as behavior depends on the order and identity of the perceived stimuli. Our results identify the neural correlates of flexible stimulus-categorization in the fruit fly.

No abstract

Animals can discriminate myriad sensory stimuli but can also generalize from learned experience. You can probably distinguish the favorite teas of your colleagues while still recognizing that all tea pales in comparison to coffee. Tradeoffs between detection, discrimination, and generalization are inherent at every layer of sensory processing. During development, specific quantitative parameters are wired into perceptual circuits and set the playing field on which plasticity mechanisms play out. A primary goal of systems neuroscience is to understand how material properties of a circuit define the logical operations--computations--that it makes, and what good these computations are for survival. A cardinal method in biology--and the mechanism of evolution--is to change a unit or variable within a system and ask how this affects organismal function. Here, we make use of our knowledge of developmental wiring mechanisms to modify hard-wired circuit parameters in the Drosophila melanogaster mushroom body and assess the functional and behavioral consequences. By altering the number of expansion layer neurons (Kenyon cells) and their dendritic complexity, we find that input number, but not cell number, tunes odor selectivity. Simple odor discrimination performance is maintained when Kenyon cell number is reduced and augmented by Kenyon cell expansion.

SummaryMemory guides the choices an animal makes across widely varying conditions in dynamic environments. Consequently, the most adaptive choice depends on the options available. How can the same memory support optimal behavior across different sets of options? We address this using olfactory learning in Drosophila. Even when we restrict an odor-punishment association to a single set of synapses using optogenetics, we find that flies still show choice behavior that depends on the options it encounters. Here we show that how odors are presented to the animal influences memory recall itself. Presenting two similar odors in sequence enabled flies to not only discriminate them behaviorally but also at the level of neural activity. However, when the same odors were encountered as solitary stimuli, no such differences were detectable. These results show that memory recall is not simply a comparison between a stimulus and a learned template, but can be adaptively modulated by stimulus dynamics.