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      Compartmentalized calcium dynamics in a C. elegans interneuron encode head movement

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          Abstract

          Confining neuronal activity to specific subcellular regions is a mechanism for expanding the computational properties of neurons. While the circuit organization underlying compartmentalized activity has been studied in several systems 14 , its cellular basis remains elusive. Here, we characterize compartmentalized activity in Caenorhabditis elegans RIA interneurons, which display multiple reciprocal connections to head motor neurons and receive input from sensory pathways. We show that RIA spatially encodes head movement on a subcellular scale through axonal compartmentalization. This subcellular axonal activity is dependent on cholinergic input from head motor neurons and is simultaneously present and additive with glutamate-dependent globally synchronized activity evoked by sensory inputs. Postsynaptically, the muscarinic acetylcholine receptor (mAchR) GAR-3 acts in RIA to compartmentalize axonal activity through mobilization of intracellular calcium stores. The compartmentalized activity functions independently from the synchronized activity to modulate locomotory behavior.

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          Most cited references23

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          Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences.

          We describe a dominant behavioral marker, rol-6(su-1006), and an efficient microinjection procedure which facilitate the recovery of Caenorhabditis elegans transformants. We use these tools to study the mechanism of C.elegans DNA transformation. By injecting mixtures of genetically marked DNA molecules, we show that large extrachromosomal arrays assemble directly from the injected molecules and that homologous recombination drives array assembly. Appropriately placed double-strand breaks stimulated homologous recombination during array formation. Our data indicate that the size of the assembled transgenic structures determines whether or not they will be maintained extrachromosomally or lost. We show that low copy number extrachromosomal transformation can be achieved by adjusting the relative concentration of DNA molecules in the injection mixture. Integration of the injected DNA, though relatively rare, was reproducibly achieved when single-stranded oligonucleotide was co-injected with the double-stranded DNA.
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            Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans.

            Although many properties of the nervous system are shared among animals and systems, it is not known whether different neuronal circuits use common strategies to guide behaviour. Here we characterize information processing by Caenorhabditis elegans olfactory neurons (AWC) and interneurons (AIB and AIY) that control food- and odour-evoked behaviours. Using calcium imaging and mutations that affect specific neuronal connections, we show that AWC neurons are activated by odour removal and activate the AIB interneurons through AMPA-type glutamate receptors. The level of calcium in AIB interneurons is elevated for several minutes after odour removal, a neuronal correlate to the prolonged behavioural response to odour withdrawal. The AWC neuron inhibits AIY interneurons through glutamate-gated chloride channels; odour presentation relieves this inhibition and results in activation of AIY interneurons. The opposite regulation of AIY and AIB interneurons generates a coordinated behavioural response. Information processing by this circuit resembles information flow from vertebrate photoreceptors to 'OFF' bipolar and 'ON' bipolar neurons, indicating a conserved or convergent strategy for sensory information processing.
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              Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans.

              The nematode C. elegans is an excellent model organism for studying behavior at the neuronal level. Because of the organism's small size, it is challenging to deliver stimuli to C. elegans and monitor neuronal activity in a controlled environment. To address this problem, we developed two microfluidic chips, the 'behavior' chip and the 'olfactory' chip for imaging of neuronal and behavioral responses in C. elegans. We used the behavior chip to correlate the activity of AVA command interneurons with the worm locomotion pattern. We used the olfactory chip to record responses from ASH sensory neurons exposed to high-osmotic-strength stimulus. Observation of neuronal responses in these devices revealed previously unknown properties of AVA and ASH neurons. The use of these chips can be extended to correlate the activity of sensory neurons, interneurons and motor neurons with the worm's behavior.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                17 April 2012
                5 July 2012
                05 January 2013
                : 487
                : 7405
                : 99-103
                Affiliations
                Department of Organismic and Evolutionary Biology, Center for Brain Science, Harvard University, Cambridge MA 02138, USA
                Author notes
                Correspondence should be addressed to Y.Z. ( yzhang@ 123456oeb.harvard.edu )
                Article
                NIHMS365855
                10.1038/nature11081
                3393794
                22722842
                e8ef8550-dac1-4340-a667-5b9b335ac409

                Users may view, print, copy, download and text and data- mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms

                History
                Funding
                Funded by: National Institute on Deafness and Other Communication Disorders : NIDCD
                Award ID: R01 DC009852-01A1 || DC
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