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Neuroscience May 2022Half a century since their discovery by Llinás and colleagues, dendritic spikes have been observed in various neurons in different brain regions, from the neocortex and... (Review)
Review
Half a century since their discovery by Llinás and colleagues, dendritic spikes have been observed in various neurons in different brain regions, from the neocortex and cerebellum to the basal ganglia. Dendrites exhibit a terrifically diverse but stereotypical repertoire of spikes, sometimes specific to subregions of the dendrite. Despite their prevalence, we only have a glimpse into their role in the behaving animal. This article aims to survey the full range of dendritic spikes found in excitatory and inhibitory neurons, compare themin vivoversusin vitro, and discuss new studies describing dendritic spikes in the human cortex. We focus on neocortical and hippocampal neurons and present a roadmap to identify and understand the broader role of dendritic spikes in single-cell computation.
Topics: Action Potentials; Animals; Dendrites; Mammals; Neocortex; Neurons; Pyramidal Cells
PubMed: 35182699
DOI: 10.1016/j.neuroscience.2022.02.009 -
Current Biology : CB Jan 2002
Topics: Animals; Dendrites; Hippocampus; Microscopy, Fluorescence; Rats
PubMed: 11790313
DOI: 10.1016/s0960-9822(01)00636-4 -
Genes Apr 2020The pseudostratified olfactory epithelium (OE) may histologically appear relatively simple, but the cytological relations among its cell types, especially those between... (Review)
Review
The pseudostratified olfactory epithelium (OE) may histologically appear relatively simple, but the cytological relations among its cell types, especially those between olfactory receptor neurons (ORNs) and olfactory sustentacular cells (OSCs), prove more complex and variable than previously believed. Adding to the complexity is the short lifespan, persistent neurogenesis, and continuous rewiring of the ORNs. Contrary to the common belief that ORN dendrites are mostly positioned between OSCs, recent findings indicate a sustentacular cell enwrapped configuration for a majority of mature ORN dendrites at the superficial layer of the OE. After vertically sprouting out from the borderlines between OSCs, most of the immature ORN dendrites undergo a process of sideways migration and terminal maturation to become completely invaginated into and enwrapped by OSCs. Trailing the course of the dendritic sideways migration is the mesodendrite (mesentery of the enwrapped dendrite) made of closely apposed, cell junction connected plasma membrane layers of neighboring folds of the host sustentacular cell. Only a minority of the mature ORN dendrites at the OE apical surface are found at the borderlines between OSCs (unwrapped). Below I give a brief update on the cytoarchitectonic relations between the ORNs and OSCs of the OE. Emphasis is placed on the enwrapment of ORN dendrites by OSCs, on the sideways migration of immature ORN dendrites after emerging from the OE surface, and on the terminal maturation of the ORNs. Functional implications of ORN dendrite enwrapment and a comparison with myelination or Remak's bundling of axons or axodendrites in the central and peripheral nervous system are also discussed.
Topics: Axons; Dendrites; Humans; Neurogenesis; Olfactory Mucosa; Olfactory Receptor Neurons; Receptors, Odorant; Smell
PubMed: 32365880
DOI: 10.3390/genes11050493 -
Journal of Neurophysiology Jan 2021Dendritic spikes in thin dendritic branches (basal and oblique dendrites) are traditionally inferred from spikelets measured in the cell body. Here, we used laser-spot...
Dendritic spikes in thin dendritic branches (basal and oblique dendrites) are traditionally inferred from spikelets measured in the cell body. Here, we used laser-spot voltage-sensitive dye imaging in cortical pyramidal neurons (rat brain slices) to investigate the voltage waveforms of dendritic potentials occurring in response to spatially restricted glutamatergic inputs. Local dendritic potentials lasted 200-500 ms and propagated to the cell body, where they caused sustained 10- to 20-mV depolarizations. Plateau potentials propagating from dendrite to soma and action potentials propagating from soma to dendrite created complex voltage waveforms in the middle of the thin basal dendrite, comprised of local sodium spikelets, local plateau potentials, and backpropagating action potentials, superimposed on each other. Our model replicated these voltage waveforms across a gradient of glutamatergic stimulation intensities. The model then predicted that somatic input resistance () and membrane time constant (tau) may be reduced during dendritic plateau potential. We then tested these model predictions in real neurons and found that the model correctly predicted the direction of and tau change but not the magnitude. In summary, dendritic plateau potentials occurring in basal and oblique branches put pyramidal neurons into an activated neuronal state ("prepared state"), characterized by depolarized membrane potential and smaller but faster membrane responses. The prepared state provides a time window of 200-500 ms, during which cortical neurons are particularly excitable and capable of following afferent inputs. At the network level, this predicts that sets of cells with simultaneous plateaus would provide cellular substrate for the formation of functional neuronal ensembles. In cortical pyramidal neurons, we recorded glutamate-mediated dendritic plateau potentials with voltage imaging and created a computer model that recreated experimental measures from dendrite and cell body. Our model made new predictions, which were then tested in experiments. Plateau potentials profoundly change neuronal state: a plateau potential triggered in one basal dendrite depolarizes the soma and shortens membrane time constant, making the cell more susceptible to firing triggered by other afferent inputs.
Topics: Action Potentials; Animals; Cerebral Cortex; Dendrites; Female; Glutamic Acid; Male; Models, Neurological; Pyramidal Cells; Rats; Rats, Sprague-Dawley; Synaptic Potentials
PubMed: 33085562
DOI: 10.1152/jn.00734.2019 -
Developmental Cell Jul 2023In developing brains, activity-dependent remodeling facilitates the formation of precise neuronal connectivity. Synaptic competition is known to facilitate synapse...
In developing brains, activity-dependent remodeling facilitates the formation of precise neuronal connectivity. Synaptic competition is known to facilitate synapse elimination; however, it has remained unknown how different synapses compete with one another within a post-synaptic cell. Here, we investigate how a mitral cell in the mouse olfactory bulb prunes all but one primary dendrite during the developmental remodeling process. We find that spontaneous activity generated within the olfactory bulb is essential. We show that strong glutamatergic inputs to one dendrite trigger branch-specific changes in RhoA activity to facilitate the pruning of the remaining dendrites: NMDAR-dependent local signals suppress RhoA to protect it from pruning; however, the subsequent neuronal depolarization induces neuron-wide activation of RhoA to prune non-protected dendrites. NMDAR-RhoA signals are also essential for the synaptic competition in the mouse barrel cortex. Our results demonstrate a general principle whereby activity-dependent lateral inhibition across synapses establishes a discrete receptive field of a neuron.
Topics: Dendrites; Olfactory Bulb; Synapses; Neurons; Cell Differentiation
PubMed: 37290446
DOI: 10.1016/j.devcel.2023.05.004 -
Trends in Cognitive Sciences Jun 2020The first patch-clamp recordings from the dendrites of human neocortical neurons have recently been reported by Beaulieu-Laroche et al. and Gidon et al. These studies...
The first patch-clamp recordings from the dendrites of human neocortical neurons have recently been reported by Beaulieu-Laroche et al. and Gidon et al. These studies have shown that human dendrites are electrically excitable, exhibiting backpropagating action potentials and fast dendritic calcium spikes. This new frontier highlights the potential for interspecies differences in the biophysics of dendritic computation.
Topics: Action Potentials; Dendrites; Humans; Neurons; Patch-Clamp Techniques; Pyramidal Cells
PubMed: 32392467
DOI: 10.1016/j.tics.2020.03.002 -
The Journal of Biological Chemistry 2021Proper dendrite morphogenesis and synapse formation are essential for neuronal development and function. Dasm1, a member of the immunoglobulin superfamily, is known to...
Proper dendrite morphogenesis and synapse formation are essential for neuronal development and function. Dasm1, a member of the immunoglobulin superfamily, is known to promote dendrite outgrowth and excitatory synapse maturation in vitro. However, the in vivo function of Dasm1 in neuronal development and the underlying mechanisms are not well understood. To learn more, Dasm1 knockout mice were constructed and employed to confirm that Dasm1 regulates dendrite arborization and spine formation in vivo. We performed a yeast two-hybrid screen using Dasm1, revealing MRCKβ as a putative partner; additional lines of evidence confirmed this interaction and identified cytoplasmic proline-rich region (823-947 aa) of Dasm1 and MRCKβ self-activated kinase domain (CC1, 410-744 aa) as necessary and sufficient for binding. Using co-immunoprecipitation assay, autophosphorylation assay, and BS3 cross-linking assay, we show that Dasm1 binding triggers a change in MRCKβ's conformation and subsequent dimerization, resulting in autophosphorylation and activation. Activated MRCKβ in turn phosphorylates a class 2 regulatory myosin light chain, which leads to enhanced actin rearrangement, causing the dendrite outgrowth and spine formation observed before. Removal of Dasm1 in mice leads to behavioral abnormalities. Together, these results reveal a crucial molecular pathway mediating cell surface and intracellular signaling communication to regulate actin dynamics and neuronal development in the mammalian brain.
Topics: Actins; Animals; Dendrites; Dendritic Spines; Immunoglobulins; Mice; Nerve Tissue Proteins; Protein Binding; Protein Domains
PubMed: 33933448
DOI: 10.1016/j.jbc.2021.100730 -
PLoS Genetics Aug 2020To remodel functional neuronal connectivity, neurons often alter dendrite arbors through elimination and subsequent regeneration of dendritic branches. However, the...
To remodel functional neuronal connectivity, neurons often alter dendrite arbors through elimination and subsequent regeneration of dendritic branches. However, the intrinsic mechanisms underlying this developmentally programmed dendrite regeneration and whether it shares common machinery with injury-induced regeneration remain largely unknown. Drosophila class IV dendrite arborization (C4da) sensory neurons regenerate adult-specific dendrites after eliminating larval dendrites during metamorphosis. Here we show that the microRNA miR-87 is a critical regulator of dendrite regeneration in Drosophila. miR-87 knockout impairs dendrite regeneration after developmentally-programmed pruning, whereas miR-87 overexpression in C4da neurons leads to precocious initiation of dendrite regeneration. Genetic analyses indicate that the transcriptional repressor Tramtrack69 (Ttk69) is a functional target for miR-87-mediated repression as ttk69 expression is increased in miR-87 knockout neurons and reducing ttk69 expression restores dendrite regeneration to mutants lacking miR-87 function. We further show that miR-87 is required for dendrite regeneration after acute injury in the larval stage, providing a mechanistic link between developmentally programmed and injury-induced dendrite regeneration. These findings thus indicate that miR-87 promotes dendrite regrowth during regeneration at least in part through suppressing Ttk69 in Drosophila sensory neurons and suggest that developmental and injury-induced dendrite regeneration share a common intrinsic mechanism to reactivate dendrite growth.
Topics: Animals; Dendrites; Drosophila Proteins; Drosophila melanogaster; Gene Expression Regulation, Developmental; Larva; Metamorphosis, Biological; MicroRNAs; Nerve Regeneration; Repressor Proteins; Sensory Receptor Cells
PubMed: 32764744
DOI: 10.1371/journal.pgen.1008942 -
Cells Oct 2021Neuronal dendrites receive, integrate, and process numerous inputs and therefore serve as the neuron's "antennae". Dendrites display extreme morphological diversity... (Review)
Review
Neuronal dendrites receive, integrate, and process numerous inputs and therefore serve as the neuron's "antennae". Dendrites display extreme morphological diversity across different neuronal classes to match the neuron's specific functional requirements. Understanding how this structural diversity is specified is therefore important for shedding light on information processing in the healthy and diseased nervous system. Popular models for in vivo studies of dendrite differentiation are the four classes of dendritic arborization (c1da-c4da) neurons of larvae with their class-specific dendritic morphologies. Using da neurons, a combination of live-cell imaging and computational approaches have delivered information on the distinct phases and the time course of dendrite development from embryonic stages to the fully developed dendritic tree. With these data, we can start approaching the basic logic behind differential dendrite development. A major role in the definition of neuron-type specific morphologies is played by dynamic actin-rich processes and the regulation of their properties. This review presents the differences in the growth programs leading to morphologically different dendritic trees, with a focus on the key role of actin modulatory proteins. In addition, we summarize requirements and technological progress towards the visualization and manipulation of such actin regulators in vivo.
Topics: Actins; Animals; Cell Differentiation; Dendrites; Drosophila
PubMed: 34685757
DOI: 10.3390/cells10102777 -
Cell Reports Nov 2019The size of dendrite arbors shapes their function and differs vastly between neuron types. The signals that control dendritic arbor size remain obscure. Here, we find...
The size of dendrite arbors shapes their function and differs vastly between neuron types. The signals that control dendritic arbor size remain obscure. Here, we find that in the retina, starburst amacrine cells (SACs) and rod bipolar cells (RBCs) express the homophilic cell-surface protein AMIGO2. In Amigo2 knockout (KO) mice, SAC and RBC dendrites expand while arbors of other retinal neurons remain stable. SAC dendrites are divided into a central input region and a peripheral output region that provides asymmetric inhibition to direction-selective ganglion cells (DSGCs). Input and output compartments scale precisely with increased arbor size in Amigo2 KO mice, and SAC dendrites maintain asymmetric connectivity with DSGCs. Increased coverage of SAC dendrites is accompanied by increased direction selectivity of DSGCs without changes to other ganglion cells. Our results identify AMIGO2 as a cell-type-specific dendritic scaling factor and link dendrite size and coverage to visual feature detection.
Topics: Action Potentials; Amacrine Cells; Animals; Dendrites; Gene Knockout Techniques; Membrane Proteins; Mice; Mice, Knockout; Nerve Tissue Proteins; Neuronal Plasticity; Retina; Retinal Bipolar Cells; Retinal Ganglion Cells; Synapses
PubMed: 31693896
DOI: 10.1016/j.celrep.2019.09.085