Vogt, Katrin
0000-0002-8763-342X Berufsbeschreibung
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Neuroscience : Merging multisensory memories
How animals form and retain memories across multiple sensory modalities and how multisensory learning can enhance memory is largely unknown. A recent study sheds light on the neural mechanism underlying multisensory memory convergence in the Drosophila melanogaster brain.
Towards a functional connectome in Drosophila
The full functionality of the brain is determined by its molecular, cellular and circuit structure. Modern neuroscience now prioritizes the mapping of whole brain connectomes by detecting all direct neuron to neuron synaptic connections, a feat first accomplished for C. elegans, a full reconstruction of a 302-neuron nervous system. Efforts at Janelia Research Campus will soon reconstruct the whole brain connectomes of a larval and an adult Drosophila. These connectomes will provide a framework for incorporating detailed neural circuit information that Drosophila neuroscientists have gathered over decades. But when viewed in the context of a whole brain, it becomes difficult to isolate the contributions of distinct circuits, whether sensory systems or higher brain regions. The complete wiring diagram tells us that sensory information is not only processed in separate channels, but that even the earliest sensory layers are strongly synaptically interconnected. In the higher brain, long-range projections densely interconnect major brain regions and convergence centers that integrate input from different sensory systems. Furthermore, we also need to understand the impact of neuronal communication beyond direct synaptic modulation. Nevertheless, all of this can be pursued with Drosophila, combining connectomics with a diverse array of genetic tools and behavioral paradigms that provide effective approaches to entire brain function.
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila
Animals discriminate stimuli, learn their predictive value and use this knowledge to modify their behavior. In Drosophila, the mushroom body (MB) plays a key role in these processes. Sensory stimuli are sparsely represented by ∼2000 Kenyon cells, which converge onto 34 output neurons (MBONs) of 21 types. We studied the role of MBONs in several associative learning tasks and in sleep regulation, revealing the extent to which information flow is segregated into distinct channels and suggesting possible roles for the multi-layered MBON network. We also show that optogenetic activation of MBONs can, depending on cell type, induce repulsion or attraction in flies. The behavioral effects of MBON perturbation are combinatorial, suggesting that the MBON ensemble collectively represents valence. We propose that local, stimulus-specific dopaminergic modulation selectively alters the balance within the MBON network for those stimuli. Our results suggest that valence encoded by the MBON ensemble biases memory-based action selection.
Appetitive and aversive visual learning in freely moving Drosophila
To compare appetitive and aversive visual memories of the fruit fly Drosophila melanogaster, we developed a new paradigm for classical conditioning. Adult flies are trained en masse to differentially associate one of two visual conditioned stimuli (CS) (blue and green light as CS) with an appetitive or aversive chemical substance (unconditioned stimulus or US). In a test phase, flies are given a choice between the paired and the unpaired visual stimuli. Associative memory is measured based on altered visual preference in the test. If a group of flies has, for example, received a sugar reward with green light in the training, they show a significantly higher preference for the green stimulus during the test than another group of flies having received the same reward with blue light. We demonstrate critical parameters for the formation of visual appetitive memory, such as training repetition, order of reinforcement, starvation, and individual conditioning. Furthermore, we show that formic acid can act as an aversive chemical reinforcer, yielding weak, yet significant, aversive memory. These results provide a basis for future investigations into the cellular and molecular mechanisms underlying visual memory and perception in Drosophila.
Navigational strategies underlying temporal phototaxis in Drosophila larvae
Navigating across light gradients is essential for survival for many animals. However, we still have a poor understanding of the algorithms that underlie such behaviors. Here, we developed a novel closed-loop phototaxis assay for Drosophila larvae in which light intensity is always spatially uniform but updates depending on the location of the animal in the arena. Even though larvae can only rely on temporal cues during runs, we find that they are capable of finding preferred areas of low light intensity. Further detailed analysis of their behavior reveals that larvae turn more frequently and that heading angle changes increase when they experience brightness increments over extended periods of time. We suggest that temporal integration of brightness change during runs is an important – and so far largely unexplored – element of phototaxis.
Direct neural pathways convey distinct visual information to Drosophila mushroom bodies
Previously, we demonstrated that visual and olfactory associative memories of Drosophila share mushroom body (MB) circuits (Vogt et al., 2014). Unlike for odor representation, the MB circuit for visual information has not been characterized. Here, we show that a small subset of MB Kenyon cells (KCs) selectively responds to visual but not olfactory stimulation. The dendrites of these atypical KCs form a ventral accessory calyx (vAC), distinct from the main calyx that receives olfactory input. We identified two types of visual projection neurons (VPNs) directly connecting the optic lobes and the vAC. Strikingly, these VPNs are differentially required for visual memories of color and brightness. The segregation of visual and olfactory domains in the MB allows independent processing of distinct sensory memories and may be a conserved form of sensory representations among insects.
Shared mushroom body circuits underlie visual and olfactory memories in Drosophila
In nature, animals form memories associating reward or punishment with stimuli from different sensory modalities, such as smells and colors. It is unclear, however, how distinct sensory memories are processed in the brain. We established appetitive and aversive visual learning assays for Drosophila that are comparable to the widely used olfactory learning assays. These assays share critical features, such as reinforcing stimuli (sugar reward and electric shock punishment), and allow direct comparison of the cellular requirements for visual and olfactory memories. We found that the same subsets of dopamine neurons drive formation of both sensory memories. Furthermore, distinct yet partially overlapping subsets of mushroom body intrinsic neurons are required for visual and olfactory memories. Thus, our results suggest that distinct sensory memories are processed in a common brain center. Such centralization of related brain functions is an economical design that avoids the repetition of similar circuit motifs.
Internal state configures olfactory behavior and early sensory processing in Drosophila larvae
Animals exhibit different behavioral responses to the same sensory cue depending on their internal state at a given moment. How and where in the brain are sensory inputs combined with state information to select an appropriate behavior? Here, we investigate how food deprivation affects olfactory behavior in Drosophila larvae. We find that certain odors repel well-fed animals but attract food-deprived animals and that feeding state flexibly alters neural processing in the first olfactory center, the antennal lobe. Hunger differentially modulates two output pathways required for opposing behavioral responses. Upon food deprivation, attraction-mediating uniglomerular projection neurons show elevated odor-evoked activity, whereas an aversion-mediating multiglomerular projection neuron receives odor-evoked inhibition. The switch between these two pathways is regulated by the lone serotonergic neuron in the antennal lobe, CSD. Our findings demonstrate how flexible behaviors can arise from state-dependent circuit dynamics in an early sensory processing center.
Reversing Stimulus Timing in Visual Conditioning Leads to Memories with Opposite Valence in Drosophila
Animals need to associate different environmental stimuli with each other regardless of whether they temporally overlap or not. Drosophila melanogaster displays olfactory trace conditioning, where an odor is followed by electric shock reinforcement after a temporal gap, leading to conditioned odor avoidance. Reversing the stimulus timing in olfactory conditioning results in the reversal of memory valence such that an odor that follows shock is later on approached (i.e. relief conditioning). Here, we explored the effects of stimulus timing on memory in another sensory modality, using a visual conditioning paradigm. We found that flies form visual memories of opposite valence depending on stimulus timing and can associate a visual stimulus with reinforcement despite being presented with a temporal gap. These results suggest that associative memories with non-overlapping stimuli and the effect of stimulus timing on memory valence are shared across sensory modalities.
The Similarity between Odors and Their Binary Mixtures in Drosophila
How are odor mixtures perceived? We take a behavioral approach toward this question, using associative odor-recognition experiments in Drosophila. We test how strongly flies avoid a binary mixture after punishment training with one of its constituent elements and how much, in turn, flies avoid an odor element if it had been a component of a previously punished binary mixture. A distinguishing feature of our approach is that we first adjust odors for task-relevant behavioral potency, that is, for equal learnability. Doing so, we find that 1) generalization between mixture and elements is symmetrical and partial, 2) elements are equally similar to all mixtures containing it and that 3) mixtures are equally similar to both their constituent elements. As boundary conditions for the applicability of these rules, we note that first, although variations in learnability are small and remain below statistical cut-off, these variations nevertheless correlate with the elements' perceptual "weight" in the mixture; thus, even small differences in learnability between the elements have the potential to feign mixture asymmetries. Second, the more distant the elements of a mixture are to each other in terms of their physicochemical properties, the more distant the flies regard the elements from the mixture. Thus, titrating for task-relevant behavioral potency and taking into account physicochemical relatedness of odors reveals rules of mixture perception that, maybe surprisingly, appear to be fairly simple.