Artificial dirt: microfluidic substrates for nematode neurobiology and behavior.

With a nervous system of only 302 neurons, the free-living nematode Caenorhabditis elegans is a powerful experimental organism for neurobiology. However, the laboratory substrate commonly used in C. elegans research, a planar agarose surface, fails to reflect the complexity of this organism's natural environment, complicates stimulus delivery, and is incompatible with high-resolution optophysiology experiments. Here we present a new class of microfluidic devices for C. elegans neurobiology and behavior: agarose-free, micron-scale chambers and channels that allow the animals to crawl as they would on agarose. One such device mimics a moist soil matrix and facilitates rapid delivery of fluid-borne stimuli. A second device consists of sinusoidal channels that can be used to regulate the waveform and trajectory of crawling worms. Both devices are thin and transparent, rendering them compatible with high-resolution microscope objectives for neuronal imaging and optical recording. Together, the new devices are likely to accelerate studies of the neuronal basis of behavior in C. elegans.

[1]  N. A. Croll Components and patterns in the behaviour of the nematode Caenorhabditis elegans , 2009 .

[2]  K. Kiontke,et al.  Phylogeny of Rhabditis subgenus Caenorhabditis (Rhabditidae, Nematoda)* , 2009 .

[3]  Sreekanth H. Chalasani,et al.  Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans , 2008, Nature.

[4]  Sreekanth H. Chalasani,et al.  Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans , 2007, Nature.

[5]  J. Apfeld,et al.  A microfabricated array of clamps for immobilizing and imaging C. elegans. , 2007, Lab on a chip.

[6]  Cori Bargmann,et al.  Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans , 2007, Nature Methods.

[7]  Mehmet Fatih Yanik,et al.  Microfluidic system for on-chip high-throughput whole-animal sorting and screening at subcellular resolution , 2007, Proceedings of the National Academy of Sciences.

[8]  Damon A. Clark,et al.  Temporal Activity Patterns in Thermosensory Neurons of Freely Moving Caenorhabditis elegans Encode Spatial Thermal Gradients , 2007, The Journal of Neuroscience.

[9]  M. Félix,et al.  Temporal Dynamics and Linkage Disequilibrium in Natural Caenorhabditis elegans Populations , 2007, Genetics.

[10]  Jim Zoval,et al.  Automated microfluidic compact disc (CD) cultivation system of Caenorhabditis elegans , 2007 .

[11]  J. Qin,et al.  Maze exploration and learning in C. elegans. , 2007, Lab on a chip.

[12]  Demetri Psaltis,et al.  Optofluidic microscopy--a method for implementing a high resolution optical microscope on a chip. , 2006, Lab on a chip.

[13]  G. Whitesides The origins and the future of microfluidics , 2006, Nature.

[14]  P. Sternberg,et al.  A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue , 2006, Nature.

[15]  Hongkai Wu,et al.  Phospholipid biotinylation of polydimethylsiloxane (PDMS) for protein immobilization. , 2006, Lab on a chip.

[16]  K. Kiontke,et al.  Ecology of Caenorhabditis species. , 2006, WormBook : the online review of C. elegans biology.

[17]  E. Bamberg,et al.  Light Activation of Channelrhodopsin-2 in Excitable Cells of Caenorhabditis elegans Triggers Rapid Behavioral Responses , 2005, Current Biology.

[18]  Cornelia I. Bargmann,et al.  Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans , 2005, Nature.

[19]  Marie-Anne Félix,et al.  High Local Genetic Diversity and Low Outcrossing Rate in Caenorhabditis elegans Natural Populations , 2005, Current Biology.

[20]  Cori Bargmann,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A circuit for navigation in Caenorhabditis elegans , 2005 .

[21]  Cornelia I. Bargmann,et al.  Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue , 2004, Nature.

[22]  G. Whitesides,et al.  Microfluidic devices fabricated in Poly(dimethylsiloxane) for biological studies , 2003, Electrophoresis.

[23]  J. Bessereau,et al.  [C. elegans: of neurons and genes]. , 2003, Medecine sciences : M/S.

[24]  S. Lockery,et al.  Step-Response Analysis of Chemotaxis in Caenorhabditis elegans , 2003, The Journal of Neuroscience.

[25]  Aravinthan D. T. Samuel,et al.  Thermotaxis in Caenorhabditis elegans Analyzed by Measuring Responses to Defined Thermal Stimuli , 2002, The Journal of Neuroscience.

[26]  Nancy Allbritton,et al.  Surface modification of poly(dimethylsiloxane) microfluidic devices by ultraviolet polymer grafting. , 2002, Analytical chemistry.

[27]  R. Kerr,et al.  Optical Imaging of Calcium Transients in Neurons and Pharyngeal Muscle of C. elegans , 2000, Neuron.

[28]  Thomas M. Morse,et al.  The Fundamental Role of Pirouettes in Caenorhabditis elegans Chemotaxis , 1999, The Journal of Neuroscience.

[29]  K. Matsumoto,et al.  A Caenorhabditis elegans JNK signal transduction pathway regulates coordinated movement via type‐D GABAergic motor neurons , 1999, The EMBO journal.

[30]  William R. Schafer,et al.  Control of Alternative Behavioral States by Serotonin in Caenorhabditis elegans , 1998, Neuron.

[31]  R. Tsien,et al.  Fluorescent indicators for Ca2+based on green fluorescent proteins and calmodulin , 1997, Nature.

[32]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[33]  R. Waterston,et al.  Interaction Between a Putative Mechanosensory Membrane Channel and a Collagen , 1996, Science.

[34]  V. Ambros,et al.  Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. , 1991, The EMBO journal.

[35]  Cori Bargmann,et al.  Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans , 1991, Neuron.

[36]  D B Dusenbery,et al.  A Promising Indicator of Neurobehavioral Toxicity Using the Nematode Caenorhabditis Elegans and Computer Tracking , 1990, Toxicology and industrial health.

[37]  S. Brenner,et al.  The structure of the nervous system of the nematode Caenorhabditis elegans. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[38]  David B. Dusenbery,et al.  Responses of the nematodeCaenorhabditis elegans to controlled chemical stimulation , 1980, Journal of comparative physiology.

[39]  J. Culotti,et al.  Osmotic avoidance defective mutants of the nematode Caenorhabditis elegans. , 1978, Genetics.

[40]  R. L. Russell,et al.  Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[41]  S. Brenner The genetics of Caenorhabditis elegans. , 1974, Genetics.

[42]  S. Ward Chemotaxis by the nematode Caenorhabditis elegans: identification of attractants and analysis of the response by use of mutants. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[43]  G. Fraenkel Orientation of Animals , 1940 .

[44]  W. Ryu,et al.  Enhanced locomotion caenorhabditis elegans in structured microfluidic environments , 2007 .

[45]  Stéphane Colin,et al.  A novel fabrication method of flexible and monolithic 3D microfluidic structures using lamination of SU-8 films , 2005 .

[46]  Bryan S. Griffiths,et al.  Nematode movement along a chemical gradient in a structurally heterogeneous environment. 1. Experiment , 1997 .

[47]  N. A. Croll Behavioural analysis of nematode movement. , 1975, Advances in parasitology.

[48]  The FASEB Journal • Research Communication Fabrication of 3D hepatic tissues by additive photopatterning of cellular hydrogels , 2022 .