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6 Publications

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    11/03/16 | Illuminating the neuronal architecture underlying context in fear memory.
    Cembrowski MS, Spruston N
    Cell. 2016 Nov 3;167(4):888-9

    Context plays a foundational role in determining how to interpret potentially fear-producing stimuli, yet the precise neurobiological substrates of context are poorly understood. In this issue of Cell, Xu et al. elegantly show that parallel neuronal circuits are necessary for two distinct roles of context in fear conditioning.

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    11/02/16 | To the cloud! A grassroots proposal to accelerate brain science discovery.
    Neuro Cloud Consortium
    Neuron. 2016 Nov 2;92(3):622-7

    The revolution in neuroscientific data acquisition is creating an analysis challenge. We propose leveraging cloud-computing technologies to enable large-scale neurodata storing, exploring, analyzing, and modeling. This utility will empower scientists globally to generate and test theories of brain function and dysfunction.

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    05/04/16 | Brain derived neurotrophic factor differentially modulates excitability of two classes of hippocampal output neurons.
    Graves AR, Moore SJ, Spruston N, Tryba AK, Kaczorowski CC
    Journal of Neurophysiology. 2016 May 4;116(2):466-71. doi: 10.1152/jn.00186.2016

    Brain-derived neurotrophic factor (BDNF) plays an important role in hippocampus-dependent learning and memory. Canonically, this has been ascribed to an enhancing effect on neuronal excitability and synaptic plasticity in the CA1 region. However, it is the pyramidal neurons in the subiculum that form the primary efferent pathways conveying hippocampal information to other areas of the brain, and yet the effect of BDNF on these neurons has remained unexplored. We present new data that BDNF regulates neuronal excitability and cellular plasticity in a much more complex manner than previously suggested. Subicular pyramidal neurons can be divided into two major classes, which have different electrophysiological and morphological properties, different requirements for the induction of plasticity and different extra-hippocampal projections. We found that BDNF increases excitability in one class of subicular pyramidal neurons, yet decreases excitability of the other class. Further, while endogenous BDNF was necessary for the induction of synaptic plasticity in both cell types, BDNF enhanced intrinsic plasticity in one class of pyramidal neurons, yet suppressed intrinsic plasticity in the other. Taken together, these data suggest a novel role for BDNF signaling, as it appears to dynamically and bidirectionally regulate the output of hippocampal information to different regions of the brain.

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    04/26/16 | Hipposeq: a comprehensive RNA-seq database of gene expression in hippocampal principal neurons.
    Cembrowski MS, Wang L, Sugino K, Shields BC, Spruston N
    eLife. 2016;5:. doi: 10.7554/eLife.14997

    Clarifying gene expression in narrowly defined neuronal populations can provide insight into cellular identity, computation, and functionality. Here, we used next-generation RNA sequencing (RNA-seq) to produce a quantitative, whole genome characterization of gene expression for the major excitatory neuronal classes of the hippocampus; namely, granule cells and mossy cells of the dentate gyrus, and pyramidal cells of areas CA3, CA2, and CA1. Moreover, for the canonical cell classes of the trisynaptic loop, we profiled transcriptomes at both dorsal and ventral poles, producing a cell-class- and region-specific transcriptional description for these populations. This dataset clarifies the transcriptional properties and identities of lesser-known cell classes, and moreover reveals unexpected variation in the trisynaptic loop across the dorsal-ventral axis. We have created a public resource, Hipposeq (http://hipposeq.janelia.org), which provides analysis and visualization of these data and will act as a roadmap relating molecules to cells, circuits, and computation in the hippocampus.

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    02/18/16 | Structured dendritic inhibition supports branch-selective integration in CA1 pyramidal cells.
    Bloss EB, Cembrowski MS, Karsh B, Colonell J, Fetter RD, Spruston N
    Neuron. 2016 Feb 18:. doi: 10.1016/j.neuron.2016.01.029

    Neuronal circuit function is governed by precise patterns of connectivity between specialized groups of neurons. The diversity of GABAergic interneurons is a hallmark of cortical circuits, yet little is known about their targeting to individual postsynaptic dendrites. We examined synaptic connectivity between molecularly defined inhibitory interneurons and CA1 pyramidal cell dendrites using correlative light-electron microscopy and large-volume array tomography. We show that interneurons can be highly selective in their connectivity to specific dendritic branch types and, furthermore, exhibit precisely targeted connectivity to the origin or end of individual branches. Computational simulations indicate that the observed subcellular targeting enables control over the nonlinear integration of synaptic input or the initiation and backpropagation of action potentials in a branch-selective manner. Our results demonstrate that connectivity between interneurons and pyramidal cell dendrites is more precise and spatially segregated than previously appreciated, which may be a critical determinant of how inhibition shapes dendritic computation.

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    01/13/16 | Spatial gene-expression gradients underlie prominent heterogeneity of CA1 pyramidal neurons.
    Cembrowski MS, Bachman JL, Wang L, Sugino K, Shields BC, Spruston N
    Neuron. 2016 Jan 13:. doi: 10.1016/j.neuron.2015.12.013

    Tissue and organ function has been conventionally understood in terms of the interactions among discrete and homogeneous cell types. This approach has proven difficult in neuroscience due to the marked diversity across different neuron classes, but it may be further hampered by prominent within-class variability. Here, we considered a well-defined canonical neuronal population-hippocampal CA1 pyramidal cells (CA1 PCs)-and systematically examined the extent and spatial rules of transcriptional heterogeneity. Using next-generation RNA sequencing, we identified striking variability in CA1 PCs, such that the differences within CA1 along the dorsal-ventral axis rivaled differences across distinct pyramidal neuron classes. This variability emerged from a spectrum of continuous gene-expression gradients, producing a transcriptional profile consistent with a multifarious continuum of cells. This work reveals an unexpected amount of variability within a canonical and narrowly defined neuronal population and suggests that continuous, within-class heterogeneity may be an important feature of neural circuits.

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