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Luo grew up in Shanghai, China, and earned his bachelor's degree in molecular biology from the University of Science and Technology of China. After obtaining his PhD in Brandeis University, and postdoctoral training at the University of California, adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule, San Francisco, Dr.
Luo started his own lab in the Department of Biology, Stanford University in December Together with his postdoctoral fellows and graduate students, Dr. Luo studies how neural circuits are organized to perform specific functions in adults, and how they are assembled during development. Luo is currently the Ann and Bill Swindells Professor in the School of Humanities and Sciences, Professor of Biology, and Professor of Neurobiology by courtesy at Stanford University, and a Howard Hughes Medical Institute Investigator.
He teaches neurobiology to Stanford undergraduate and graduate students, adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule. Luo has served on the editorial boards of adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule scientific journals, including Neuron, eLife, and Annual Review of Neuroscience, Cell, and PNAS.
He has also served on the Pew Scholar National Committee and Scientific Advisory Committee of Damon Runyon Cancer Research Foundation. He is recipient of the McKnight Technological Innovation in Neuroscience Award, the Society for Neuroscience Young Investigator Award, the Jacob Javits Award from National Institute of Neurological Disorders and Stroke, HW Mossman Award from American Association of Anatomists, the Lawrence Katz Prize, the Pradel Award of National Academy of Sciences, and the Education in Neuroscience award from Society for Neuroscience.
Luo is a Member of the National Academy of Sciences and a Fellow of the American Academy of Arts and Sciences. Assembly of the fly olfactory circuit A central question in neural circuit assembly is how neurons connect specifically with their synaptic partners.
We are using the fly olfactory circuit to investigate the general principles by which wiring specificity is established during development. The assembly of the fly olfactory circuit requires precise matching between axons from 50 olfactory receptor neuron types and dendrites from 50 projection neuron types. In the past 20 years, we adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule identified key cellular interactions and molecular mechanisms at specific steps of olfactory circuit assembly.
More recently, we have also taken transcriptomic, proteomic, and live imaging approaches to complement genetic analyses of individual genes. We are currently integrating these approaches to deepen our understanding of the combinatorial cell-surface codes that instruct connection specificity.
Assembly of neural circuits in the mouse brain We have studied a broad range of developmental processes in rodent brains using genetic tools we have developed. Some of these studies extend what we are learning in the fly, whereas others explore processes more prevalent in vertebrates. For example, cerebellar Purkinje cells have highly elaborate and planar dendritic trees, each of which receives presynaptic inputs from tens of thousands of granule cells. Our investigations of Purkinje cell dendrite morphogenesis have highlighted the importance of competitive interactions adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule dendritic growth and branching.
Our studies of hippocampal network assembly have revealed that the same cell-surface proteins, teneurin-3 and latrophilin-2, can serve both as ligands and receptors to mediate attraction and repulsion, and these molecules are likely reused in the assembly of multiple nodes of the hippocampal networks.
We are investigating the function of these molecules in the assembly of additional circuits as well as how they work both as ligands and receptors. Organization and function of neural circuits We have used genetic and viral strategies to decipher the organizational principles of the fly and mouse olfactory systems, as well as the input—output architecture of norepinephrine, dopamine, and serotonin systems at the scale of the entire mouse brain.
We are now also combining single-cell transcriptomics with activity recording, manipulation, and TRAPing, as well as behavioral analyses, to interrogate the functional organization of a variety of neural circuits.
Recent discoveries include the dissection of dorsal raphe serotonin neuron subsystems, adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule, reward representation in cerebellar granule cells and shared cortex-cerebellum dynamics, the unit of organization and evolution of the cerebellar nuclei, differential encoding of task variables by prefrontal cortical projection neuron classes, temporal evolution of prefrontal cortical neuron ensembles that promote remote memory retrieval, and neural basis of thirst drive for motivated behavior.
Tool development We continue to develop tools to interrogate neural circuit assembly and organization with increasing precision. The MARCM mosaic analysis with a repressible cell marker method in flies and MADM mosaic analysis with double markers method in mice allow the visualization and genetic manipulation of isolated single neurons. The Q system further expanded binary expression tools in flies.
We recently developed tools to map circuit organization in mammals. The TRIO tracing the relationship between input and output and cTRIO cell-type-specific TRIO methods allow rabies virus—based input tracing to neurons defined by projection, or by cell type and projection.
The TRAP targeted recombination in active population method enables genetic access to neurons based on their activity, which in combination with tools for labeling, tracing, recording, and manipulating neurons, offers a powerful approach for understanding how neural circuits process information and generate behavior.
View details for DOI View details for PubMedID The Drosophila olfactory system provides an excellent model to investigate this process since 50 types of olfactory receptor neurons ORNs from the antennae and maxillary palps project their axons to 50 identifiable adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule in the antennal lobe and form synaptic connections with dendrites from 50 types of second-order projection neurons PNs. Previous studies mainly focused on identifying important molecules that regulate the precise targeting in the olfactory circuit using fixed tissues, adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule.
Here, an antennae-brain explant system that recapitulates key adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule milestones of olfactory circuit assembly in culture is described. Through dissecting the external cuticle and cleaning opaque fat bodies covering the developing pupal brain, high quality images of single neurons from live brains can be collected using two-photon microscopy.
This allows time-lapse imaging of single ORN axon targeting from live tissue. This approach will help reveal important cell biological contexts and functions of previously identified important genes and identify mechanisms underpinning the dynamic process of circuit assembly.
Neural circuit assembly features simultaneous targeting of numerous neuronal processes from constituent neuron types, yet the dynamics is poorly understood. Here, we use the Drosophila olfactory circuit to investigate dynamic cellular processes by which olfactory receptor neurons ORNs target axons precisely to specific glomeruli in the ipsi- and contralateral antennal lobes.
Time-lapse imaging of individual axons from 30 ORN types revealed a rich diversity in extension speed, innervation timing, and ipsilateral branch locations and identified that ipsilateral targeting occurs via stabilization of transient interstitial branches.
Fast imaging using adaptive optics-corrected lattice light-sheet microscopy showed that upon approaching target, many ORN types exhibiting "exploring branches" consisted of parallel microtubule-based terminal branches emanating from an F-actin-rich hub. Antennal nerve ablations uncovered essential roles for bilateral axons in contralateral target selection and for ORN axons to facilitate dendritic refinement of postsynaptic partner neurons.
Altogether, these observations provide cellular bases for wiring specificity establishment. View details for Web of Science ID Infection-induced aversion against enteropathogens is a conserved sickness behaviour that can promote host survival1,2.
The aetiology of this behaviour remains poorly understood, but studies in Drosophila have linked olfactory and gustatory perception to avoidance behaviours against toxic microorganisms Whether and how enteric infections directly influence sensory perception to induce or modulate such behaviours remains unknown.
Here we show that enteropathogen infection in Drosophila can modulate olfaction through metabolic reprogramming of ensheathing glia of the antennal lobe. Infection-induced unpaired cytokine expression in the intestine activates JAK-STAT signalling in ensheathing glia, inducing the expression of glial monocarboxylate transporters and the apolipoprotein glial lazarillo GLazand affecting metabolic coupling of glia and neurons at the antennal lobe.
This modulates olfactory discrimination, promotes the avoidance of bacteria-laced food and increases fly survival. Although transient in young flies, gut-induced metabolic reprogramming of ensheathing glia becomes constitutive in old flies owing to age-related intestinal inflammation, which contributes to an age-related decline in olfactory discrimination.
Our findings identify adaptive glial metabolic reprogramming by gut-derived cytokines as a mechanism that causes lasting changes in a sensory system in ageing flies. In motor neuroscience, state changes are hypothesized to time-lock neural assemblies coordinating complex movements, but evidence for this remains slender. We tested whether a discrete change from more autonomous to coherent spiking underlies skilled movement by imaging cerebellar Purkinje neuron complex spikes in mice making targeted forelimb-reaches.
As mice learned the task, millimeter-scale spatiotemporally coherent spiking emerged ipsilateral to the reaching forelimb, and consistent neural synchronization became predictive of kinematic stereotypy.
Before reach onset, spiking switched from more disordered to internally time-locked concerted spiking and silence. Optogenetic manipulations of cerebellar feedback to the inferior olive bi-directionally modulated neural synchronization and reaching direction. A simple model explained the reorganization of spiking during reaching as reflecting a discrete bifurcation in olivary network dynamics.
These findings argue that to prepare learned movements, olivo-cerebellar circuits enter a self-regulated, synchronized state promoting motor coordination. State changes facilitating behavioral transitions may generalize across neural systems. Mosaic analysis with double markers MADM offers one approach to visualize and concomitantly manipulate genetically defined cells in mice with single-cell resolution. MADM applications include the analysis of lineage, single-cell morphology and physiology, genomic imprinting phenotypes, adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule, and dissection of cell-autonomous gene functions invivo in health and disease.
Beyond a proof of principle, we apply our MADM library to systematically trace sister chromatid segregation in distinct mitotic cell lineages.
We find striking chromosome-specific biases in segregation patterns, reflecting a putative mechanism for the asymmetric segregation of genetic determinants in somatic stem cell division. Cerebellar granule cells GrCs are usually regarded as a uniform cell type that collectively expands the coding space of the cerebellum by integrating diverse combinations of mossy fiber inputs, adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule. Adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule, stable molecularly or physiologically defined GrC subtypes within a single cerebellar region have not been reported.
The only known cellular property that distinguishes otherwise homogeneous GrCs is the correspondence between GrC birth timing and the depth of the molecular layer to which their axons project. To determine the role birth timing plays in GrC wiring and function, we developed genetic strategies to access early- and late-born GrCs. We initiated retrograde monosynaptic rabies virus tracing from control birth timing unrestrictedearly-born, and late-born GrCs, revealing the different patterns of mossy fiber input to GrCs in vermis lobule 6 and simplex, as well as to early- and late-born GrCs of vermis lobule 6: sensory and motor nuclei provide more input to early-born GrCs, while basal pontine and cerebellar nuclei provide more input to late-born GrCs, adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule.
Our results suggest neither organized parallel processing nor completely random organization of mossy fiberGrC circuitry but instead a moderate influence of birth timing on GrC wiring and encoding.
Our imaging data also provide evidence that GrCs can represent generalized responses to aversive stimuli, in addition to recently described reward representations. Mammalian medial and lateral hippocampal networks preferentially process spatial- and object-related information, respectively. However, the mechanisms underlying the assembly of such parallel networks during development remain largely unknown.
Our study shows that, in mice, complementary expression of cell surface molecules teneurin-3 Ten3 and latrophilin-2 Lphn2 in the medial and lateral hippocampal networks, respectively, guides the precise assembly of CA1-to-subiculum connections in both networks.
Our findings demonstrate that assembly of parallel hippocampal networks follows a "Ten3Ten3, Lphn2Lphn2" rule instructed by reciprocal repulsions. Neurons undergo substantial morphological and functional changes during development to form precise synaptic connections and acquire specific physiological properties.
What are the underlying transcriptomic bases? Here, we obtained the single-cell transcriptomes of Drosophila olfactory projection neurons PNs at four developmental stages. We decoded the identity of 21 transcriptomic clusters corresponding to 20 PN types and developed methods to match transcriptomic clusters representing the same PN type across development.
We discovered that PN transcriptomes reflect unique biological processes unfolding at each stage-neurite growth and pruning during metamorphosis at an early pupal stage; peaked transcriptomic diversity during olfactory circuit assembly at mid-pupal stages; and neuronal signaling in adults. At early developmental stages, adhesion among cadherin cell dissertation heterophilic homophilic interaction molecule, PN types with adjacent birth order share similar transcriptomes.
Together, our work reveals principles of cellular diversity during brain development and provides a resource for future studies of neural development in PNs and other neuronal types. Recognition of environmental cues is essential for the survival of all organisms. Transcriptional changes occur to enable the generation and function of the neural circuits underlying sensory perception.
To gain insight into these changes, we generated single-cell transcriptomes of Drosophila olfactory- ORNsthermo- and hygro-sensory neurons at an early developmental and adult stage using single-cell and single-nucleus RNA sequencing.
We discovered that ORNs maintain expression of the same olfactory receptors across development. Using receptor expression and computational approaches, we matched transcriptomic clusters corresponding to anatomically and physiologically defined neuron types across multiple developmental stages. We found that cell-type-specific transcriptomes partly reflected axon trajectory choices in development and sensory modality in adults.
We uncovered stage-specific genes that could regulate the wiring and sensory responses of distinct ORN types. Collectively, our data reveal transcriptomic features of sensory neuron biology and provide a resource for future studies of their development and physiology.
Dopaminergic projections exert widespread influence over multiple brain regions and modulate various behaviors including movement, reward learning, and motivation.
It is increasingly appreciated that dopamine neurons are heterogeneous in their gene expression, circuitry, physiology, and function. Current approaches to target dopamine neurons are largely based on single gene drivers, which either label all dopamine neurons or mark a subset but concurrently label non-dopaminergic neurons. Here, we establish a mouse line with Flpo recombinase expressed from the endogenous Slc6a3 dopamine active transporter [DAT] locus.
We demonstrate the utility of this approach by generating DAT-P2A-Flpo;NEX-Cre mice that specifically label Neurod6-expressing dopamine neurons, which project to the nucleus accumbens medial shell. DAT-P2A-Flpo mice add to a growing toolbox of genetic resources that will help parse the diverse functions mediated by dopaminergic circuits.
Cell Adhesion Molecules - Structure and Types
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