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Color and polarization provide complementary information about the world and are detected by specialized photoreceptors. However, the downstream neural circuits that process these distinct modalities are incompletely understood in any animal. Using electron microscopy, we have systematically reconstructed the synaptic targets of the photoreceptors specialized to detect color and skylight polarization in Drosophila , and we have used light microscopy to confirm many of our findings. We identified known and novel downstream targets that are selective for different wavelengths or polarized light, and followed their projections to other areas in the optic lobes and the central brain. Our results revealed many synapses along the photoreceptor axons between brain regions, new pathways in the optic lobes, and spatially segregated projections to central brain regions. Strikingly, photoreceptors in the polarization-sensitive dorsal rim area target fewer cell types, and lack strong connections to the lobula, a neuropil involved in color processing. Our reconstruction identifies shared wiring and modality-specific specializations for color and polarization vision, and provides a comprehensive view of the first steps of the pathways processing color and polarized light inputs.

The evolutionary expansion of sensory neuron populations detecting important environmental cues is widespread, but functionally enigmatic. We investigated this phenomenon through comparison of homologous olfactory pathways of Drosophila melanogaster and its close relative Drosophila sechellia , an extreme specialist for Morinda citrifolia noni fruit. D. sechellia has evolved species-specific expansions in select, noni-detecting olfactory sensory neuron (OSN) populations, through multigenic changes. Activation and inhibition of defined proportions of neurons demonstrate that OSN number increases contribute to stronger, more persistent, noni-odour tracking behaviour. These expansions result in increased synaptic connections of sensory neurons with their projection neuron (PN) partners, which are conserved in number between species. Surprisingly, having more OSNs does not lead to greater odour-evoked PN sensitivity or reliability. Rather, pathways with increased sensory pooling exhibit reduced PN adaptation, likely through weakened lateral inhibition. Our work reveals an unexpected functional impact of sensory neuron population expansions to explain ecologically-relevant, species-specific behaviour. Sensory neuron population expansions are common in evolution but of unclear function. Here, the authors show that, in drosophilid olfactory systems, increased sensory neuron number impacts interneuron dynamics, but not sensitivity, to promote olfactory-guided behaviour.

Specialized ommatidia harboring polarization-sensitive photoreceptors exist in the ‘dorsal rim area’ (DRA) of virtually all insects. Although downstream elements have been described both anatomically and physiologically throughout the optic lobes and the central brain of different species, little is known about their cellular and synaptic adaptations and how these shape their functional role in polarization vision. We have previously shown that in the DRA of Drosophila melanogaster, two distinct types of modality-specific ‘distal medulla’ cell types (Dm-DRA1 and Dm-DRA2) are post-synaptic to long visual fiber photoreceptors R7 and R8, respectively. Here we describe additional neuronal elements in the medulla neuropil that manifest modality-specific differences in the DRA region, including DRA-specific neuronal morphology, as well as differences in the structure of pre- or post-synaptic membranes. Furthermore, we show that certain cell types (medulla tangential cells and octopaminergic neuromodulatory cells) specifically avoid contacts with polarization-sensitive photoreceptors. Finally, while certain transmedullary cells are specifically absent from DRA medulla columns, other subtypes show specific wiring differences while still connecting the DRA to the lobula complex, as has previously been described in larger insects. This hints towards a complex circuit architecture with more than one pathway connecting polarization-sensitive DRA photoreceptors with the central brain.

Many animals use visual information to navigate 1 – 4 , but how such information is encoded and integrated by the navigation system remains incompletely understood. In Drosophila melanogaster , EPG neurons in the central complex compute the heading direction 5 by integrating visual input from ER neurons 6 – 12 , which are part of the anterior visual pathway (AVP) 10 , 13 – 16 . Here we densely reconstruct all neurons in the AVP using electron-microscopy data 17 . The AVP comprises four neuropils, sequentially linked by three major classes of neurons: MeTu neurons 10 , 14 , 15 , which connect the medulla in the optic lobe to the small unit of the anterior optic tubercle (AOTUsu) in the central brain; TuBu neurons 9 , 16 , which connect the AOTUsu to the bulb neuropil; and ER neurons 6 – 12 , which connect the bulb to the EPG neurons. On the basis of morphologies, connectivity between neural classes and the locations of synapses, we identify distinct information channels that originate from four types of MeTu neurons, and we further divide these into ten subtypes according to the presynaptic connections in the medulla and the postsynaptic connections in the AOTUsu. Using the connectivity of the entire AVP and the dendritic fields of the MeTu neurons in the optic lobes, we infer potential visual features and the visual area from which any ER neuron receives input. We confirm some of these predictions physiologically. These results provide a strong foundation for understanding how distinct sensory features can be extracted and transformed across multiple processing stages to construct higher-order cognitive representations. Electron-microscopy data are used to reconstruct the neurons that make up the anterior visual pathway in the Drosophila brain, providing insight into how visual features are encoded to guide navigation.

A catalogue of neuronal cell types has often been called a ‘parts list’ of the brain 1 , and regarded as a prerequisite for understanding brain function 2 , 3 . In the optic lobe of Drosophila , rules of connectivity between cell types have already proven to be essential for understanding fly vision 4 , 5 . Here we analyse the fly connectome to complete the list of cell types intrinsic to the optic lobe, as well as the rules governing their connectivity. Most new cell types contain 10 to 100 cells, and integrate information over medium distances in the visual field. Some existing type families (Tm, Li, and LPi) 6 – 10 at least double in number of types. A new serpentine medulla (Sm) interneuron family contains more types than any other. Three families of cross-neuropil types are revealed. The consistency of types is demonstrated by analysing the distances in high-dimensional feature space, and is further validated by algorithms that select small subsets of discriminative features. We use connectivity to hypothesize about the functional roles of cell types in motion, object and colour vision. Connectivity with ‘boundary types’ that straddle the optic lobe and central brain is also quantified. We showcase the advantages of connectomic cell typing: complete and unbiased sampling, a rich array of features based on connectivity and reduction of the connectome to a substantially simpler wiring diagram of cell types, with immediate relevance for brain function and development. An analysis of the Drosophila connectome yields all cell types intrinsic to the optic lobe, and their rules of connectivity.

The fly eye contains different subtypes of unit eyes (ommatidia) with molecularly and morphologically specialized photoreceptors for comparing either between different wavelengths (color vision) or between different angles of the linearly polarized skylight (polarization vision). However, microcircuit differences between those parts of the columnar medulla neuropil computing color versus polarization remain largely unknown. There is virtually nothing known about the circuit elements immediately downstream of polarization-sensitive photoreceptors in the ‘dorsal rim area’ (DRA). In this work, I described the cellular and synaptic architecture of medulla columns that receive skylight polarization input from DRA photoreceptors. I showed that only in the DRA region, R7 and R8 photoreceptors resemble each other by targeting their axons to the same medulla layer. However, within this layer DRA R7 and R8 connect to morphologically distinct Dm target cells (called Dm-DRA1 and Dm-DRA2, respectively). Both Dm-DRA cell types are modality-specific by avoiding contact with color-sensitive photoreceptors. Using the genetic toolbox of Drosophila such as activity-dependent GFP-reconstitution across synaptic partners (GRASP) and the genetically inducible trans-synaptic tracer ‘trans-Tango’, I confirmed that Dm-DRA1 and Dm-DRA2 are the specific post-synaptic targets of DRA.R7 or DRA.R8, respectively. Neither Dm-DRAs overlap with the main synaptic targets of color-sensitive R7 cells (called Dm8 cells), revealing for the first time that skylight polarization is processed by separate modality-specific circuits in the early visual system. These modality-specific differences are not limited only Dm-DRA cells. I described modality-specific cellular and synaptic specializations in other optic lobe cell types in the DRA region of the medulla: the dendritic arbors of certain cell types (neuromodulatory cells and visual projection neurons) specifically avoid the DRA region. Furthermore, Transmedullary (Tm) cells that are post-synaptic to color-sensitive photoreceptors showed modality-specific differences in connectivity or were absent from the DRA. Finally, I contributed a study describing the cellular organization of the ‘anterior visual pathway’ that carries skylight information from the eye to the central brain. In this study, I showed that an optic glomerulus called the anterior optic tubercle (AOTU) receives direct information via different classes of medulla-to-tubercle (MeTu) neurons, terminating in different subdomains of the AOTU. Finally, we hypothesize that different classes of MeTu cells carry different types of skylight information to the central brain via parallel pathways.

Extracting relevant features of a complex sensory signal typically involves sequential processing through multiple brain regions. However, identifying the logic and mechanisms of these transformations has been difficult, due to the challenges of measuring both activity within and long-range connectivity between multiple neural populations. Here, we investigate the reformatting of odor information across two stages of the olfactory system. We measure the odor tuning of 20 types of anatomically-defined third order lateral horn neuron (LHN) and compare to predictions based on the odor tuning of second-order projection neurons (PNs) and PN-LHN connectivity. We find that LHNs reformat PN activity in two distinct ways. First, LHNs selectively discard information about odor identities with similar valence (i.e., attractiveness or aversiveness). This emerges from a precise alignment of PN odor tuning and PN-LHN connectivity, as well as odor-specific inhibition and boosting of LHN activity. This creates a population code for valence that is more explicit than in PNs. Second, a subset of LHNs selectively discard information about continuing odor presence, by responding only transiently to odor onset. This creates a population code for odor dynamics that is more explicit than in PNs. Across LHNs, valence and dynamics are independent of each other. Thus, feedforward connectivity and local inhibition combine to extract two orthogonal dimensions of olfactory information.

Many animals, including humans, navigate their surroundings by visual input, yet we understand little about how visual information is transformed and integrated by the navigation system. In , compass neurons in the donut-shaped ellipsoid body of the central complex generate a sense of direction by integrating visual input from ring neurons, a part of the anterior visual pathway (AVP). Here, we densely reconstruct all neurons in the AVP using FlyWire, an AI-assisted tool for analyzing electron-microscopy data. The AVP comprises four neuropils, sequentially linked by three major classes of neurons: MeTu neurons, which connect the medulla in the optic lobe to the small unit of anterior optic tubercle (AOTUsu) in the central brain; TuBu neurons, which connect the anterior optic tubercle to the bulb neuropil; and ring neurons, which connect the bulb to the ellipsoid body. Based on neuronal morphologies, connectivity between different neural classes, and the locations of synapses, we identified non-overlapping channels originating from four types of MeTu neurons, which we further divided into ten subtypes based on the presynaptic connections in medulla and postsynaptic connections in AOTUsu. To gain an objective measure of the natural variation within the pathway, we quantified the differences between anterior visual pathways from both hemispheres and between two electron-microscopy datasets. Furthermore, we infer potential visual features and the visual area from which any given ring neuron receives input by combining the connectivity of the entire AVP, the MeTu neurons' dendritic fields, and presynaptic connectivity in the optic lobes. These results provide a strong foundation for understanding how distinct visual features are extracted and transformed across multiple processing stages to provide critical information for computing the fly's sense of direction.

A catalog of neuronal cell types has often been called a \"parts list\" of the brain, and regarded as a prerequisite for understanding brain function. In the optic lobe of , rules of connectivity between cell types have already proven essential for understanding fly vision. Here we analyze the fly connectome to complete the list of cell types intrinsic to the optic lobe, as well as the rules governing their connectivity. We more than double the list of known types. Most new cell types contain between 10 and 100 cells, and integrate information over medium distances in the visual field. Some existing type families (Tm, Li, and LPi) at least double in number of types. We introduce a new Sm interneuron family, which contains more types than any other, and three new families of cross-neuropil types. Self-consistency of cell types is demonstrated through automatic assignment of cells to types by distance in high-dimensional feature space, and further validation is provided by algorithms that select small subsets of discriminative features. Cell types with similar connectivity patterns divide into clusters that are interpretable in terms of motion, object, and color vision. Our work showcases the advantages of connectomic cell typing: complete and unbiased sampling, a rich array of features based on connectivity, and reduction of the connectome to a drastically simpler wiring diagram of cell types, with immediate relevance for brain function and development.

The evolutionary expansion of sensory neuron populations detecting important environmental cues is widespread, but functionally enigmatic. We investigated this phenomenon through comparison of homologous neural pathways of and its close relative , an extreme specialist for noni fruit. has evolved species-specific expansions in select, noni-detecting olfactory sensory neuron (OSN) populations, through multigenic changes. Activation and inhibition of defined proportions of neurons demonstrate that OSN population increases contribute to stronger, more persistent, noni-odor tracking behavior. These sensory neuron expansions result in increased synaptic connections with their projection neuron (PN) partners, which are conserved in number between species. Surprisingly, having more OSNs does not lead to greater odor-evoked PN sensitivity or reliability. Rather, pathways with increased sensory pooling exhibit reduced PN adaptation, likely through weakened lateral inhibition. Our work reveals an unexpected functional impact of sensory neuron expansions to explain ecologically-relevant, species-specific behavior.