scholarly journals Integration of plasticity mechanisms within a single sensory neuron of C. elegans actuates a memory

2017 ◽  
Author(s):  
Josh D. Hawk ◽  
Ana C. Calvo ◽  
Agustin Almoril-Porras ◽  
Ahmad Aljobeh ◽  
Maria Luisa Torruella-Suárez ◽  
...  
Keyword(s):  
Single Cell ◽  
Sensory Neuron ◽  
Neural Plasticity ◽  
Sensory Information ◽  
Sensory Adaptation ◽  
Sensory Stimuli ◽  
C Elegans ◽  
Presynaptic Plasticity ◽  
Behavioral Preference

SummaryNeural plasticity—the ability of a neuron to change its cellular properties in response to past experiences—underpins the nervous system’s capacity to form memories and actuate behaviors. How different plasticity mechanisms act together in vivo and at a cellular level to transform sensory information into behavior is not well understood. Here we show that in the nematode C. elegans two plasticity mechanisms—sensory adaptation and presynaptic plasticity—act within a single cell to encode thermosensory information and actuate a temperature-preference memory. Sensory adaptation enables the primary thermosensory neuron, AFD, to adjust the temperature range of its sensitivity to the local environment, thereby optimizing its ability to detect temperature fluctuations associated with migration. Presynaptic plasticity transforms this thermosensory information into a behavioral preference by gating synaptic communication between sensory neuron AFD and its postsynaptic partner, AIY. The gating of synaptic communication is regulated at AFD presynaptic sites by the conserved kinase nPKCε. Bypassing or altering AFD presynaptic plasticity predictably changes the learned behavioral preferences without affecting sensory responses. Our findings indicate that two distinct and modular neuroplasticity mechanisms function together within a single sensory neuron to encode multiple components of information required to enact thermotactic behavior. The integration of these plasticity mechanisms result in a single-cell logic system that can both represent sensory stimuli and guide memory-based behavioral preference.

FosGFP expression does not capture a sensory learning-related engram in superficial layers of mouse barrel cortex

2021 ◽  
Vol 118 (52) ◽  
pp. e2112212118
Author(s):  
Jiseok Lee ◽  
Joanna Urban-Ciecko ◽  
Eunsol Park ◽  
Mo Zhu ◽  
Stephanie E. Myal ◽  
...  
Keyword(s):  
Pyramidal Neurons ◽  
Barrel Cortex ◽  
Sensory Information ◽  
Learning Task ◽  
Early Gene ◽  
Sensory Stimuli ◽  
Association Learning ◽  
Neural Ensembles ◽  
Dependent Learning

Immediate-early gene (IEG) expression has been used to identify small neural ensembles linked to a particular experience, based on the principle that a selective subset of activated neurons will encode specific memories or behavioral responses. The majority of these studies have focused on “engrams” in higher-order brain areas where more abstract or convergent sensory information is represented, such as the hippocampus, prefrontal cortex, or amygdala. In primary sensory cortex, IEG expression can label neurons that are responsive to specific sensory stimuli, but experience-dependent shaping of neural ensembles marked by IEG expression has not been demonstrated. Here, we use a fosGFP transgenic mouse to longitudinally monitor in vivo expression of the activity-dependent gene c-fos in superficial layers (L2/3) of primary somatosensory cortex (S1) during a whisker-dependent learning task. We find that sensory association training does not detectably alter fosGFP expression in L2/3 neurons. Although training broadly enhances thalamocortical synaptic strength in pyramidal neurons, we find that synapses onto fosGFP+ neurons are not selectively increased by training; rather, synaptic strengthening is concentrated in fosGFP− neurons. Taken together, these data indicate that expression of the IEG reporter fosGFP does not facilitate identification of a learning-specific engram in L2/3 in barrel cortex during whisker-dependent sensory association learning.

scholarly journals Combining single-cell RNA-sequencing with a molecular atlas unveils new markers for Caenorhabditis elegans neuron classes

2020 ◽  
Author(s):  
Ramiro Lorenzo ◽  
Michiho Onizuka ◽  
Matthieu Defrance ◽  
Patrick Laurent
Keyword(s):  
Caenorhabditis Elegans ◽  
Single Cell ◽  
Rna Sequencing ◽  
Cell Fate ◽  
Single Neuron ◽  
Genetic Manipulations ◽  
C Elegans ◽  
Single Cell Rna Sequencing ◽  
Normal Differentiation

Abstract Single-cell RNA-sequencing (scRNA-seq) of the Caenorhabditis elegans nervous system offers the unique opportunity to obtain a partial expression profile for each neuron within a known connectome. Building on recent scRNA-seq data and on a molecular atlas describing the expression pattern of ∼800 genes at the single cell resolution, we designed an iterative clustering analysis aiming to match each cell-cluster to the ∼100 anatomically defined neuron classes of C. elegans. This heuristic approach successfully assigned 97 of the 118 neuron classes to a cluster. Sixty two clusters were assigned to a single neuron class and 15 clusters grouped neuron classes sharing close molecular signatures. Pseudotime analysis revealed a maturation process occurring in some neurons (e.g. PDA) during the L2 stage. Based on the molecular profiles of all identified neurons, we predicted cell fate regulators and experimentally validated unc-86 for the normal differentiation of RMG neurons. Furthermore, we observed that different classes of genes functionally diversify sensory neurons, interneurons and motorneurons. Finally, we designed 15 new neuron class-specific promoters validated in vivo. Amongst them, 10 represent the only specific promoter reported to this day, expanding the list of neurons amenable to genetic manipulations.

scholarly journals Combining single-cell RNA-sequencing with a molecular atlas unveils new markers for C. elegans neuron classes

2019 ◽  
Author(s):  
Ramiro Lorenzo ◽  
Michiho Onizuka ◽  
Matthieu Defrance ◽  
Patrick Laurent
Keyword(s):  
Single Cell ◽  
Rna Sequencing ◽  
Motor Neurons ◽  
Clustering Analysis ◽  
Molecular Signatures ◽  
Functional Diversification ◽  
Genetic Manipulations ◽  
C Elegans ◽  
Single Cell Rna Sequencing

AbstractSingle-cell RNA-sequencing (scRNA-seq) of the Caenorhabditis elegans (C. elegans) nervous system offers the unique opportunity to obtain a partial expression profile for each neuron within a known connectome. Building on recent scRNA-seq data [1] and on a molecular atlas describing the expression pattern of ~800 genes at the single cell resolution [2], we designed an iterative clustering analysis aiming to match each cell-cluster to the ~100 anatomically defined neuron classes of C. elegans. This heuristic approach successfully assigned 58 clusters to their corresponding neuron class. Another 11 clusters grouped neuron classes sharing close molecular signatures and 7 clusters were not assigned. Based on these 76 molecular profiles, we designed 15 new neuron class-specific promoters validated in vivo. Amongst them, 10 represent the only specific promoter reported to this day, expanding the list of neurons amenable to genetic manipulations. Finally, we observed a differential expression of functionally relevant genes between sensory-, inter-, and motor neurons in C. elegans, suggesting the mode of functional diversification may vary accordingly to the neuronal modalities.

scholarly journals Probing Single-Cell Micromechanics In Vivo: The Microrheology of C. elegans Developing Embryos

2006 ◽  
Vol 90 (12) ◽  
pp. 4712-4719 ◽  
Author(s):  
Brian R. Daniels ◽  
Byron C. Masi ◽  
Denis Wirtz
Keyword(s):  
Single Cell ◽  
C Elegans ◽  
Cell Micromechanics

scholarly journals Ca2+/CaM binding to CaMKI promotes IMA-3 importin binding and nuclear translocation in sensory neurons to control behavioral adaptation

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Domenica Ippolito ◽  
Saurabh Thapliyal ◽  
Dominique A Glauser
Keyword(s):  
Cell Activation ◽  
Behavioral Plasticity ◽  
Nuclear Translocation ◽  
Neural Activation ◽  
Sensory Adaptation ◽  
Transcription Control ◽  
C Elegans ◽  
Regulatory Processes ◽  
Slow Kinetics

Sensory and behavioral plasticity are essential for animals to thrive in changing environments. As key effectors of intracellular calcium signaling, Ca2+/Calmodulin-dependent protein kinases (CaMKs) can bridge neural activation with the many regulatory processes needed to orchestrate sensory adaptation, including by relaying signals to the nucleus. Here, we elucidate the molecular mechanism controlling the cell activation-dependent nuclear translocation of CMK-1, the C. elegans ortholog of mammalian CaMKI/IV, in thermosensory neurons in vivo. We show that an intracellular Ca2+ concentration elevation is necessary and sufficient to favor CMK-1 nuclear import. The binding of Ca2+/CaM to CMK-1 increases its affinity for IMA-3 importin, causing a redistribution with a relatively slow kinetics, matching the timescale of sensory adaptation. Furthermore, we show that this mechanism enables the encoding of opposite nuclear signals in neuron types with opposite calcium-responses and that it is essential for experience-dependent behavioral plasticity and gene transcription control in vivo. Since CaMKI/IV are conserved regulators of adaptable behaviors, similar mechanisms could exist in other organisms and for other sensory modalities.

scholarly journals Girdin regulates dendrite morphogenesis and cilium position in two specialized sensory neuron types in C. elegans

2020 ◽  
Author(s):  
Inna Nechipurenko ◽  
Sofia Lavrentyeva ◽  
Piali Sengupta
Keyword(s):  
Sensory Neuron ◽  
Primary Cilia ◽  
Gas Sensing ◽  
Neuron Development ◽  
Dendrite Morphology ◽  
Sensory Stimuli ◽  
Multifunctional Protein ◽  
C Elegans ◽  
Dendrite Development ◽  
Dendrite Morphogenesis

ABSTRACTPrimary cilia are located at the dendritic tips of sensory neurons and house the molecular machinery necessary for detection and transduction of sensory stimuli. The mechanisms that coordinate dendrite extension with cilium position during sensory neuron development are not well understood. Here, we show that GRDN-1, the Caenorhabditis elegans ortholog of the highly conserved scaffold and signaling protein Girdin/GIV, regulates both cilium position and dendrite extension in the postembryonic AQR and PQR gas-sensing neurons. Mutations in grdn-1 disrupt dendrite outgrowth and mislocalize cilia to the soma or proximal axonal segments in AQR, and to a lesser extent, in PQR. GRDN-1 is localized to the basal body and regulates localization of HMR-1/Cadherin to the distal AQR dendrite. However, loss of HMR-1 and/or SAX-7/LICAM, molecules previously implicated in sensory dendrite development in C. elegans, do not alter AQR dendrite morphology or cilium position. We demonstrate that GRDN-1 localization in AQR is regulated by UNC-116/Kinesin-1, and that correspondingly, unc-116 mutants exhibit severe AQR dendrite outgrowth and cilium positioning defects. In contrast, GRDN-1 and cilium localization in PQR is modulated by LIN-44/Wnt signaling. Together, these findings identify upstream regulators of GRDN-1, and describe new cellspecific roles for this multifunctional protein in sensory dendrite development.

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