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1.
bioRxiv ; 2024 Jun 01.
Article in English | MEDLINE | ID: mdl-38659887

ABSTRACT

Vision provides animals with detailed information about their surroundings, conveying diverse features such as color, form, and movement across the visual scene. Computing these parallel spatial features requires a large and diverse network of neurons, such that in animals as distant as flies and humans, visual regions comprise half the brain's volume. These visual brain regions often reveal remarkable structure-function relationships, with neurons organized along spatial maps with shapes that directly relate to their roles in visual processing. To unravel the stunning diversity of a complex visual system, a careful mapping of the neural architecture matched to tools for targeted exploration of that circuitry is essential. Here, we report a new connectome of the right optic lobe from a male Drosophila central nervous system FIB-SEM volume and a comprehensive inventory of the fly's visual neurons. We developed a computational framework to quantify the anatomy of visual neurons, establishing a basis for interpreting how their shapes relate to spatial vision. By integrating this analysis with connectivity information, neurotransmitter identity, and expert curation, we classified the ~53,000 neurons into 727 types, about half of which are systematically described and named for the first time. Finally, we share an extensive collection of split-GAL4 lines matched to our neuron type catalog. Together, this comprehensive set of tools and data unlock new possibilities for systematic investigations of vision in Drosophila, a foundation for a deeper understanding of sensory processing.

3.
Elife ; 102021 10 26.
Article in English | MEDLINE | ID: mdl-34696823

ABSTRACT

Flexible behaviors over long timescales are thought to engage recurrent neural networks in deep brain regions, which are experimentally challenging to study. In insects, recurrent circuit dynamics in a brain region called the central complex (CX) enable directed locomotion, sleep, and context- and experience-dependent spatial navigation. We describe the first complete electron microscopy-based connectome of the Drosophila CX, including all its neurons and circuits at synaptic resolution. We identified new CX neuron types, novel sensory and motor pathways, and network motifs that likely enable the CX to extract the fly's head direction, maintain it with attractor dynamics, and combine it with other sensorimotor information to perform vector-based navigational computations. We also identified numerous pathways that may facilitate the selection of CX-driven behavioral patterns by context and internal state. The CX connectome provides a comprehensive blueprint necessary for a detailed understanding of network dynamics underlying sleep, flexible navigation, and state-dependent action selection.


Subject(s)
Connectome , Spatial Navigation , Animals , Brain/physiology , Drosophila/physiology , Drosophila melanogaster/physiology , Neurons/physiology , Spatial Navigation/physiology
4.
Nature ; 599(7883): 147-151, 2021 11.
Article in English | MEDLINE | ID: mdl-34616045

ABSTRACT

Understanding cellular architecture is essential for understanding biology. Electron microscopy (EM) uniquely visualizes cellular structures with nanometre resolution. However, traditional methods, such as thin-section EM or EM tomography, have limitations in that they visualize only a single slice or a relatively small volume of the cell, respectively. Focused ion beam-scanning electron microscopy (FIB-SEM) has demonstrated the ability to image small volumes of cellular samples with 4-nm isotropic voxels1. Owing to advances in the precision and stability of FIB milling, together with enhanced signal detection and faster SEM scanning, we have increased the volume that can be imaged with 4-nm voxels by two orders of magnitude. Here we present a volume EM atlas at such resolution comprising ten three-dimensional datasets for whole cells and tissues, including cancer cells, immune cells, mouse pancreatic islets and Drosophila neural tissues. These open access data (via OpenOrganelle2) represent the foundation of a field of high-resolution whole-cell volume EM and subsequent analyses, and we invite researchers to explore this atlas and pose questions.


Subject(s)
Datasets as Topic , Information Dissemination , Microscopy, Electron, Scanning , Organelles/ultrastructure , Animals , Cell Line , Cells, Cultured , Drosophila melanogaster/cytology , Drosophila melanogaster/ultrastructure , Female , Golgi Apparatus/ultrastructure , Humans , Interphase , Islets of Langerhans/cytology , Male , Mice , Microscopy, Electron, Scanning/methods , Microscopy, Electron, Scanning/standards , Microtubules/ultrastructure , Neuroglia/ultrastructure , Neurons/ultrastructure , Open Access Publishing , Ovarian Neoplasms/immunology , Ovarian Neoplasms/ultrastructure , Ribosomes/ultrastructure , Synaptic Vesicles/ultrastructure , T-Lymphocytes, Cytotoxic/cytology , T-Lymphocytes, Cytotoxic/immunology , T-Lymphocytes, Cytotoxic/ultrastructure
5.
Elife ; 92020 12 14.
Article in English | MEDLINE | ID: mdl-33315010

ABSTRACT

Making inferences about the computations performed by neuronal circuits from synapse-level connectivity maps is an emerging opportunity in neuroscience. The mushroom body (MB) is well positioned for developing and testing such an approach due to its conserved neuronal architecture, recently completed dense connectome, and extensive prior experimental studies of its roles in learning, memory, and activity regulation. Here, we identify new components of the MB circuit in Drosophila, including extensive visual input and MB output neurons (MBONs) with direct connections to descending neurons. We find unexpected structure in sensory inputs, in the transfer of information about different sensory modalities to MBONs, and in the modulation of that transfer by dopaminergic neurons (DANs). We provide insights into the circuitry used to integrate MB outputs, connectivity between the MB and the central complex and inputs to DANs, including feedback from MBONs. Our results provide a foundation for further theoretical and experimental work.


Subject(s)
Connectome , Drosophila melanogaster/physiology , Mushroom Bodies/physiology , Animals , Brain Mapping , Mushroom Bodies/innervation
6.
Elife ; 92020 09 07.
Article in English | MEDLINE | ID: mdl-32880371

ABSTRACT

The neural circuits responsible for animal behavior remain largely unknown. We summarize new methods and present the circuitry of a large fraction of the brain of the fruit fly Drosophila melanogaster. Improved methods include new procedures to prepare, image, align, segment, find synapses in, and proofread such large data sets. We define cell types, refine computational compartments, and provide an exhaustive atlas of cell examples and types, many of them novel. We provide detailed circuits consisting of neurons and their chemical synapses for most of the central brain. We make the data public and simplify access, reducing the effort needed to answer circuit questions, and provide procedures linking the neurons defined by our analysis with genetic reagents. Biologically, we examine distributions of connection strengths, neural motifs on different scales, electrical consequences of compartmentalization, and evidence that maximizing packing density is an important criterion in the evolution of the fly's brain.


Animal brains of all sizes, from the smallest to the largest, work in broadly similar ways. Studying the brain of any one animal in depth can thus reveal the general principles behind the workings of all brains. The fruit fly Drosophila is a popular choice for such research. With about 100,000 neurons ­ compared to some 86 billion in humans ­ the fly brain is small enough to study at the level of individual cells. But it nevertheless supports a range of complex behaviors, including navigation, courtship and learning. Thanks to decades of research, scientists now have a good understanding of which parts of the fruit fly brain support particular behaviors. But exactly how they do this is often unclear. This is because previous studies showing the connections between cells only covered small areas of the brain. This is like trying to understand a novel when all you can see is a few isolated paragraphs. To solve this problem, Scheffer, Xu, Januszewski, Lu, Takemura, Hayworth, Huang, Shinomiya et al. prepared the first complete map of the entire central region of the fruit fly brain. The central brain consists of approximately 25,000 neurons and around 20 million connections. To prepare the map ­ or connectome ­ the brain was cut into very thin 8nm slices and photographed with an electron microscope. A three-dimensional map of the neurons and connections in the brain was then reconstructed from these images using machine learning algorithms. Finally, Scheffer et al. used the new connectome to obtain further insights into the circuits that support specific fruit fly behaviors. The central brain connectome is freely available online for anyone to access. When used in combination with existing methods, the map will make it easier to understand how the fly brain works, and how and why it can fail to work correctly. Many of these findings will likely apply to larger brains, including our own. In the long run, studying the fly connectome may therefore lead to a better understanding of the human brain and its disorders. Performing a similar analysis on the brain of a small mammal, by scaling up the methods here, will be a likely next step along this path.


Subject(s)
Connectome/methods , Drosophila melanogaster/physiology , Neurons/physiology , Synapses/physiology , Animals , Brain/physiology , Female , Male
7.
Elife ; 82019 11 06.
Article in English | MEDLINE | ID: mdl-31692445

ABSTRACT

Drosophila R7 UV photoreceptors (PRs) are divided into yellow (y) and pale (p) subtypes. yR7 PRs express the Dpr11 cell surface protein and are presynaptic to Dm8 amacrine neurons (yDm8) that express Dpr11's binding partner DIP-γ, while pR7 PRs synapse onto DIP-γ-negative pDm8. Dpr11 and DIP-γ expression patterns define 'yellow' and 'pale' color vision circuits. We examined Dm8 neurons in these circuits by electron microscopic reconstruction and expansion microscopy. DIP-γ and dpr11 mutations affect the morphologies of yDm8 distal ('home column') dendrites. yDm8 neurons are generated in excess during development and compete for presynaptic yR7 PRs, and interactions between Dpr11 and DIP-γ are required for yDm8 survival. These interactions also allow yDm8 neurons to select yR7 PRs as their appropriate home column partners. yDm8 and pDm8 neurons do not normally compete for survival signals or R7 partners, but can be forced to do so by manipulation of R7 subtype fate.


Subject(s)
Amacrine Cells/metabolism , Drosophila Proteins/genetics , Drosophila melanogaster/metabolism , Membrane Proteins/genetics , Photoreceptor Cells, Invertebrate/metabolism , Synapses/metabolism , Visual Pathways/physiology , Amacrine Cells/cytology , Animals , Color Vision/physiology , Dendrites/metabolism , Dendrites/ultrastructure , Drosophila Proteins/metabolism , Drosophila melanogaster/cytology , Drosophila melanogaster/genetics , Gene Expression , Membrane Proteins/metabolism , Mutation , Photoreceptor Cells, Invertebrate/cytology , Protein Binding , Synapses/ultrastructure , Visual Pathways/cytology
8.
Elife ; 62017 07 18.
Article in English | MEDLINE | ID: mdl-28718765

ABSTRACT

Understanding memory formation, storage and retrieval requires knowledge of the underlying neuronal circuits. In Drosophila, the mushroom body (MB) is the major site of associative learning. We reconstructed the morphologies and synaptic connections of all 983 neurons within the three functional units, or compartments, that compose the adult MB's α lobe, using a dataset of isotropic 8 nm voxels collected by focused ion-beam milling scanning electron microscopy. We found that Kenyon cells (KCs), whose sparse activity encodes sensory information, each make multiple en passant synapses to MB output neurons (MBONs) in each compartment. Some MBONs have inputs from all KCs, while others differentially sample sensory modalities. Only 6% of KC>MBON synapses receive a direct synapse from a dopaminergic neuron (DAN). We identified two unanticipated classes of synapses, KC>DAN and DAN>MBON. DAN activation produces a slow depolarization of the MBON in these DAN>MBON synapses and can weaken memory recall.


Subject(s)
Connectome , Drosophila/anatomy & histology , Drosophila/physiology , Mushroom Bodies/anatomy & histology , Mushroom Bodies/physiology , Animals , Learning , Memory
9.
Elife ; 62017 04 22.
Article in English | MEDLINE | ID: mdl-28432786

ABSTRACT

Analysing computations in neural circuits often uses simplified models because the actual neuronal implementation is not known. For example, a problem in vision, how the eye detects image motion, has long been analysed using Hassenstein-Reichardt (HR) detector or Barlow-Levick (BL) models. These both simulate motion detection well, but the exact neuronal circuits undertaking these tasks remain elusive. We reconstructed a comprehensive connectome of the circuits of Drosophila's motion-sensing T4 cells using a novel EM technique. We uncover complex T4 inputs and reveal that putative excitatory inputs cluster at T4's dendrite shafts, while inhibitory inputs localize to the bases. Consistent with our previous study, we reveal that Mi1 and Tm3 cells provide most synaptic contacts onto T4. We are, however, unable to reproduce the spatial offset between these cells reported previously. Our comprehensive connectome reveals complex circuits that include candidate anatomical substrates for both HR and BL types of motion detectors.


Subject(s)
Connectome , Drosophila melanogaster/anatomy & histology , Drosophila melanogaster/physiology , Motion Perception , Visual Pathways/anatomy & histology , Visual Pathways/physiology , Animals , Models, Neurological
10.
Cell ; 163(7): 1756-69, 2015 Dec 17.
Article in English | MEDLINE | ID: mdl-26687360

ABSTRACT

Information processing relies on precise patterns of synapses between neurons. The cellular recognition mechanisms regulating this specificity are poorly understood. In the medulla of the Drosophila visual system, different neurons form synaptic connections in different layers. Here, we sought to identify candidate cell recognition molecules underlying this specificity. Using RNA sequencing (RNA-seq), we show that neurons with different synaptic specificities express unique combinations of mRNAs encoding hundreds of cell surface and secreted proteins. Using RNA-seq and protein tagging, we demonstrate that 21 paralogs of the Dpr family, a subclass of immunoglobulin (Ig)-domain containing proteins, are expressed in unique combinations in homologous neurons with different layer-specific synaptic connections. Dpr interacting proteins (DIPs), comprising nine paralogs of another subclass of Ig-containing proteins, are expressed in a complementary layer-specific fashion in a subset of synaptic partners. We propose that pairs of Dpr/DIP paralogs contribute to layer-specific patterns of synaptic connectivity.


Subject(s)
Drosophila Proteins/metabolism , Immunoglobulins/metabolism , Neurons/metabolism , Receptors, Immunologic/metabolism , Synapses , Animals , Drosophila , Flow Cytometry , Sequence Analysis, RNA , Vision, Ocular
11.
Proc Natl Acad Sci U S A ; 112(44): 13711-6, 2015 Nov 03.
Article in English | MEDLINE | ID: mdl-26483464

ABSTRACT

We reconstructed the synaptic circuits of seven columns in the second neuropil or medulla behind the fly's compound eye. These neurons embody some of the most stereotyped circuits in one of the most miniaturized of animal brains. The reconstructions allow us, for the first time to our knowledge, to study variations between circuits in the medulla's neighboring columns. This variation in the number of synapses and the types of their synaptic partners has previously been little addressed because methods that visualize multiple circuits have not resolved detailed connections, and existing connectomic studies, which can see such connections, have not so far examined multiple reconstructions of the same circuit. Here, we address the omission by comparing the circuits common to all seven columns to assess variation in their connection strengths and the resultant rates of several different and distinct types of connection error. Error rates reveal that, overall, <1% of contacts are not part of a consensus circuit, and we classify those contacts that supplement (E+) or are missing from it (E-). Autapses, in which the same cell is both presynaptic and postsynaptic at the same synapse, are occasionally seen; two cells in particular, Dm9 and Mi1, form ≥ 20-fold more autapses than do other neurons. These results delimit the accuracy of developmental events that establish and normally maintain synaptic circuits with such precision, and thereby address the operation of such circuits. They also establish a precedent for error rates that will be required in the new science of connectomics.


Subject(s)
Drosophila melanogaster/physiology , Synapses/physiology , Vision, Ocular/physiology , Animals
12.
Article in English | MEDLINE | ID: mdl-26217193

ABSTRACT

Synaptic circuits for identified behaviors in the Drosophila brain have typically been considered from either a developmental or functional perspective without reference to how the circuits might have been inherited from ancestral forms. For example, two candidate pathways for ON- and OFF-edge motion detection in the visual system act via circuits that use respectively either T4 or T5, two cell types of the fourth neuropil, or lobula plate (LOP), that exhibit narrow-field direction-selective responses and provide input to wide-field tangential neurons. T4 or T5 both have four subtypes that terminate one each in the four strata of the LOP. Representatives are reported in a wide range of Diptera, and both cell types exhibit various similarities in: (1) the morphology of their dendritic arbors; (2) their four morphological and functional subtypes; (3) their cholinergic profile in Drosophila; (4) their input from the pathways of L3 cells in the first neuropil, or lamina (LA), and by one of a pair of LA cells, L1 (to the T4 pathway) and L2 (to the T5 pathway); and (5) their innervation by a single, wide-field contralateral tangential neuron from the central brain. Progenitors of both also express the gene atonal early in their proliferation from the inner anlage of the developing optic lobe, being alone among many other cell type progeny to do so. Yet T4 receives input in the second neuropil, or medulla (ME), and T5 in the third neuropil or lobula (LO). Here we suggest that these two cell types were originally one, that their ancestral cell population duplicated and split to innervate separate ME and LO neuropils, and that a fiber crossing-the internal chiasma-arose between the two neuropils. The split most plausibly occurred, we suggest, with the formation of the LO as a new neuropil that formed when it separated from its ancestral neuropil to leave the ME, suggesting additionally that ME input neurons to T4 and T5 may also have had a common origin.


Subject(s)
Biological Evolution , Motion Perception/physiology , Neurons/physiology , Neuropil/physiology , Orientation/physiology , Visual Pathways/physiology , Animals , Choline O-Acetyltransferase/metabolism , Drosophila , Neurons/classification , Vesicular Inhibitory Amino Acid Transport Proteins/metabolism
13.
Microscopy (Oxf) ; 64(1): 37-44, 2015 Feb.
Article in English | MEDLINE | ID: mdl-25525121

ABSTRACT

Recent powerful tools for reconstructing connectomes using electron microscopy (EM) have made outstanding contributions to the field of neuroscience. As a prime example, the detection of visual motion is a classic problem of neural computation, yet our understanding of the exact mechanism has been frustrated by our incomplete knowledge of the relevant neurons and synapses. Recent connectomic studies have successfully identified the concrete neuronal circuit in the fly's visual system that computes the motion signals. This identification was greatly aided by the comprehensiveness of the EM reconstruction. Compared with light microscopy, which gives estimated connections from arbor overlap, EM gives unequivocal connections with precise synaptic counts. This paper reviews the recent study of connectomics in a brain of the fruit fly Drosophila and highlights how connectomes can provide a foundation for understanding the mechanism of neuronal functions by identifying the underlying neural circuits.


Subject(s)
Connectome/methods , Drosophila/anatomy & histology , Visual Pathways/anatomy & histology , Animals , Brain/anatomy & histology , Microscopy, Electron, Transmission/methods , Neurons/cytology , Synapses/ultrastructure
14.
Nature ; 500(7461): 175-81, 2013 Aug 08.
Article in English | MEDLINE | ID: mdl-23925240

ABSTRACT

Animal behaviour arises from computations in neuronal circuits, but our understanding of these computations has been frustrated by the lack of detailed synaptic connection maps, or connectomes. For example, despite intensive investigations over half a century, the neuronal implementation of local motion detection in the insect visual system remains elusive. Here we develop a semi-automated pipeline using electron microscopy to reconstruct a connectome, containing 379 neurons and 8,637 chemical synaptic contacts, within the Drosophila optic medulla. By matching reconstructed neurons to examples from light microscopy, we assigned neurons to cell types and assembled a connectome of the repeating module of the medulla. Within this module, we identified cell types constituting a motion detection circuit, and showed that the connections onto individual motion-sensitive neurons in this circuit were consistent with their direction selectivity. Our results identify cellular targets for future functional investigations, and demonstrate that connectomes can provide key insights into neuronal computations.


Subject(s)
Connectome , Drosophila/physiology , Models, Biological , Motion Perception/physiology , Visual Pathways/physiology , Animals , Female , Visual Pathways/cytology
15.
Proc Biol Sci ; 279(1742): 3482-90, 2012 Sep 07.
Article in English | MEDLINE | ID: mdl-22628477

ABSTRACT

The eye of the Glacial Apollo butterfly, Parnassius glacialis, a 'living fossil' species of the family Papilionidae, contains three types of spectrally heterogeneous ommatidia. Electron microscopy reveals that the Apollo rhabdom is tiered. The distal tier is composed exclusively of photoreceptors expressing opsins of ultraviolet or blue-absorbing visual pigments, and the proximal tier consists of photoreceptors expressing opsins of green or red-absorbing visual pigments. This organization is unique because the distal tier of other known butterflies contains two green-sensitive photoreceptors, which probably function in improving spatial and/or motion vision. Interspecific comparison suggests that the Apollo rhabdom retains an ancestral tiered pattern with some modification to enhance its colour vision towards the long-wavelength region of the spectrum.


Subject(s)
Butterflies/ultrastructure , Compound Eye, Arthropod/ultrastructure , Photoreceptor Cells, Invertebrate/ultrastructure , Animals , Biological Evolution , Butterflies/anatomy & histology , Butterflies/genetics , Butterflies/physiology , Compound Eye, Arthropod/anatomy & histology , Compound Eye, Arthropod/physiology , Japan , Male , Microscopy, Electron, Transmission , Microscopy, Fluorescence , Photoreceptor Cells, Invertebrate/cytology , Photoreceptor Cells, Invertebrate/physiology , Species Specificity , Ultraviolet Rays
16.
Curr Biol ; 21(24): 2077-84, 2011 Dec 20.
Article in English | MEDLINE | ID: mdl-22137471

ABSTRACT

Detecting motion is a feature of all advanced visual systems [1], nowhere more so than in flying animals, like insects [2, 3]. In flies, an influential autocorrelation model for motion detection, the elementary motion detector circuit (EMD; [4, 5]), compares visual signals from neighboring photoreceptors to derive information on motion direction and velocity. This information is fed by two types of interneuron, L1 and L2, in the first optic neuropile, or lamina, to downstream local motion detectors in columns of the second neuropile, the medulla. Despite receiving carefully matched photoreceptor inputs, L1 and L2 drive distinct, separable pathways responding preferentially to moving "on" and "off" edges, respectively [6, 7]. Our serial electron microscopy (EM) identifies two types of transmedulla (Tm) target neurons, Tm1 and Tm2, that receive apparently matched synaptic inputs from L2. Tm2 neurons also receive inputs from two retinotopically posterior neighboring columns via L4, a third type of lamina neuron. Light microscopy reveals that the connections in these L2/L4/Tm2 circuits are highly determinate. Single-cell transcript profiling suggests that nicotinic acetylcholine receptors mediate transmission within the L2/L4/Tm2 circuits, whereas L1 is apparently glutamatergic. We propose that Tm2 integrates sign-conserving inputs from neighboring columns to mediate the detection of front-to-back motion generated during forward motion.


Subject(s)
Drosophila melanogaster/physiology , Vision, Ocular/physiology , Visual Pathways/physiology , Adaptation, Physiological , Animals , Drosophila melanogaster/cytology , Drosophila melanogaster/metabolism , Drosophila melanogaster/radiation effects , Interneurons/physiology , Microscopy, Electron , Motion Perception , Optic Lobe, Nonmammalian/cytology , Optic Lobe, Nonmammalian/physiology , Optic Lobe, Nonmammalian/radiation effects , Photoreceptor Cells, Invertebrate/cytology , Photoreceptor Cells, Invertebrate/metabolism , Photoreceptor Cells, Invertebrate/radiation effects , Receptors, Glutamate/physiology , Receptors, Nicotinic/physiology , Signal Transduction , Vision, Ocular/radiation effects , Visual Pathways/cytology , Visual Pathways/radiation effects
17.
Curr Biol ; 21(23): 2000-5, 2011 Dec 06.
Article in English | MEDLINE | ID: mdl-22119527

ABSTRACT

Wiring economy has successfully explained the individual placement of neurons in simple nervous systems like that of Caenorhabditis elegans [1-3] and the locations of coarser structures like cortical areas in complex vertebrate brains [4]. However, it remains unclear whether wiring economy can explain the placement of individual neurons in brains larger than that of C. elegans. Indeed, given the greater number of neuronal interconnections in larger brains, simply minimizing the length of connections results in unrealistic configurations, with multiple neurons occupying the same position in space. Avoiding such configurations, or volume exclusion, repels neurons from each other, thus counteracting wiring economy. Here we test whether wiring economy together with volume exclusion can explain the placement of neurons in a module of the Drosophila melanogaster brain known as lamina cartridge [5-13]. We used newly developed techniques for semiautomated reconstruction from serial electron microscopy (EM) [14] to obtain the shapes of neurons, the location of synapses, and the resultant synaptic connectivity. We show that wiring length minimization and volume exclusion together can explain the structure of the lamina microcircuit. Therefore, even in brains larger than that of C. elegans, at least for some circuits, optimization can play an important role in individual neuron placement.


Subject(s)
Brain/anatomy & histology , Drosophila melanogaster/physiology , Models, Neurological , Neurons/physiology , Synapses/ultrastructure , Animals , Microscopy, Electron/methods , Neural Pathways/physiology , Neurons/cytology , Synapses/physiology
18.
J Neurogenet ; 23(1-2): 68-77, 2009.
Article in English | MEDLINE | ID: mdl-19132600

ABSTRACT

The shape of a neuron, its morphological signature, dictates the neuron's function by establishing its synaptic partnerships. Here, we review various anatomical methods used to reveal neuron shape and the contributions these have made to our current understanding of neural function in the Drosophila brain, especially the optic lobe. These methods, including Golgi impregnation, genetic reporters, and electron microscopy (EM), necessarily incorporate biases of various sorts that are easy to overlook, but that filter the morphological signatures we see. Nonetheless, the application of these methods to the optic lobe has led to reassuringly congruent findings on the number and shapes of neurons and their connection patterns, indicating that morphological classes are actually genetic classes. Genetic methods using, especially, GAL4 drivers and associated reporters have largely superceded classical Golgi methods for cellular analyses and, moreover, allow the manipulation of neuronal activity, thus enabling us to establish a bridge between morphological studies and functional ones. While serial-EM reconstruction remains the only reliable, albeit labor-intensive, method to determine actual synaptic connections, genetic approaches in combination with EM or high-resolution light microscopic techniques are promising methods for the rapid determination of synaptic circuit function.


Subject(s)
Drosophila/cytology , Neurons/ultrastructure , Optic Lobe, Nonmammalian/ultrastructure , Animals , Cell Shape/physiology , Golgi Apparatus/ultrastructure , Microscopy, Electron , Neurons/physiology , Synapses/physiology , Terminology as Topic
19.
Neuron ; 60(2): 328-42, 2008 Oct 23.
Article in English | MEDLINE | ID: mdl-18957224

ABSTRACT

Drosophila vision is mediated by inputs from three types of photoreceptor neurons; R1-R6 mediate achromatic motion detection, while R7 and R8 constitute two chromatic channels. Neural circuits for processing chromatic information are not known. Here, we identified the first-order interneurons downstream of the chromatic channels. Serial EM revealed that small-field projection neurons Tm5 and Tm9 receive direct synaptic input from R7 and R8, respectively, and indirect input from R1-R6, qualifying them to function as color-opponent neurons. Wide-field Dm8 amacrine neurons receive input from 13-16 UV-sensing R7s and provide output to projection neurons. Using a combinatorial expression system to manipulate activity in different neuron subtypes, we determined that Dm8 neurons are necessary and sufficient for flies to exhibit phototaxis toward ultraviolet instead of green light. We propose that Dm8 sacrifices spatial resolution for sensitivity by relaying signals from multiple R7s to projection neurons, which then provide output to higher visual centers.


Subject(s)
Color Vision/physiology , Compound Eye, Arthropod/physiology , Drosophila melanogaster/physiology , Interneurons/physiology , Photoreceptor Cells, Invertebrate/physiology , Visual Pathways/physiology , Amacrine Cells/cytology , Amacrine Cells/physiology , Amacrine Cells/radiation effects , Animals , Color Vision/radiation effects , Compound Eye, Arthropod/cytology , Compound Eye, Arthropod/radiation effects , Drosophila melanogaster/cytology , Interneurons/cytology , Interneurons/radiation effects , Light Signal Transduction/physiology , Light Signal Transduction/radiation effects , Optic Lobe, Nonmammalian/cytology , Optic Lobe, Nonmammalian/physiology , Photic Stimulation , Photoreceptor Cells, Invertebrate/cytology , Photoreceptor Cells, Invertebrate/radiation effects , Synapses/physiology , Synapses/radiation effects , Synapses/ultrastructure , Synaptic Transmission/physiology , Synaptic Transmission/radiation effects , Ultraviolet Rays , Visual Pathways/cytology , Visual Pathways/radiation effects
20.
J Comp Neurol ; 509(5): 493-513, 2008 Aug 10.
Article in English | MEDLINE | ID: mdl-18537121

ABSTRACT

Understanding the visual pathways of the fly's compound eye has been blocked for decades at the second optic neuropil, the medulla, a two-part relay comprising 10 strata (M1-M10), and the largest neuropil in the fly's brain. Based on the modularity of its composition, and two previous reports, on Golgi-impregnated cell types (Fischbach and Dittrich, Cell Tissue Res.,1989; 258:441-475) and their synaptic circuits in the first neuropil, the lamina, we used serial-section electron microscopy to examine inputs to the distal strata M1-M6. We report the morphology of the reconstructed medulla terminals of five lamina cells, L1-L5, two photoreceptors, R7 and R8, and three neurons, medulla cell T1 and centrifugal cells C2 and C3. The morphology of these conforms closely to previous reports from Golgi impregnation. This fidelity provides assurance that our reconstructions are complete and accurate. Synapses of these terminals broadly localize to the terminal and provide contacts to unidentified targets, mostly medulla cells, as well as sites of connection between the terminals themselves. These reveal that R8 forms contacts upon R7 and thus between these two spectral inputs; that L3 provides input upon both pathways, adding an achromatic input; that the terminal of L5 reciprocally connects to that of L1, thus being synaptic in the medulla despite lacking synapses in the lamina; that the motion-sensing input cells L1 and L2 lack direct interconnection but both receive input from C2 and C3, resembling lamina connections of these cells; and that, as in the lamina, T1 provides no output chemical synapses.


Subject(s)
Drosophila/physiology , Medulla Oblongata/physiology , Nerve Net/physiology , Optic Lobe, Nonmammalian/physiology , Synapses/physiology , Visual Pathways/physiology , Animals , Drosophila/cytology , Drosophila/ultrastructure , Medulla Oblongata/cytology , Medulla Oblongata/ultrastructure , Nerve Net/cytology , Nerve Net/ultrastructure , Optic Lobe, Nonmammalian/cytology , Optic Lobe, Nonmammalian/ultrastructure , Synapses/ultrastructure , Visual Pathways/cytology , Visual Pathways/ultrastructure
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