Regulation of distinct attractive and aversive mechanisms mediating benzaldehyde chemotaxis in Caenorhabditis elegans.

Olfactory-mediated chemotaxis in nematodes provides a relatively simple system to study biological mechanisms of information processing. Analysis of the kinetics of chemotaxis in response to 100% benzaldehyde revealed an initial attractive response that is followed by a strong aversion to the odorant. We show that this behavior is mediated by two genetically separable attraction- and aversion-mediating response pathways. The attraction initially dominates behavior but with prolonged exposure habituation leads to a behavioral change, such that the odorant becomes repulsive. This olfactory habituation is susceptible to dishabituation, thereby re-establishing the attractive response to the odorant. Re-examination of the putative olfactory adaptation mutant adp-1(ky20) revealed that the phenotype observed in this line is due to a supersensitivity to a dishabituating stimulus, rather than a defect in the adaptation to odorants per se. A modified benzaldehyde chemotaxis assay was developed and used for the isolation of a mutant with a specific defect in habituation kinetics, expressed as a persistence of the attractive response.

[1]  W. Schafer,et al.  Long-Term Nicotine Adaptation in Caenorhabditis elegans Involves PKC-Dependent Changes in Nicotinic Receptor Abundance , 2000, The Journal of Neuroscience.

[2]  M. Ehlers,et al.  Reinsertion or Degradation of AMPA Receptors Determined by Activity-Dependent Endocytic Sorting , 2000, Neuron.

[3]  Christian Rosenmund,et al.  Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons , 2000, Nature.

[4]  M. Dong,et al.  Multiple RGS proteins alter neural G protein signaling to allow C. elegans to rapidly change behavior when fed. , 2000, Genes & development.

[5]  R. Fremeau,et al.  Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. , 2000, Science.

[6]  D. van der Kooy,et al.  A behavioral and genetic dissection of two forms of olfactory plasticity in Caenorhabditis elegans: adaptation and habituation. , 2000, Learning & memory.

[7]  Catharine H. Rankin,et al.  Mutations of the Caenorhabditis elegansBrain-Specific Inorganic Phosphate Transporter eat-4Affect Habituation of the Tap–Withdrawal Response without Affecting the Response Itself , 2000, The Journal of Neuroscience.

[8]  R. Plasterk,et al.  The complete family of genes encoding G proteins of Caenorhabditis elegans , 1999, Nature Genetics.

[9]  H. Horvitz,et al.  EAT-4, a Homolog of a Mammalian Sodium-Dependent Inorganic Phosphate Cotransporter, Is Necessary for Glutamatergic Neurotransmission in Caenorhabditis elegans , 1999, The Journal of Neuroscience.

[10]  Cori Bargmann.  Neurobiology of the Caenorhabditis elegans genome. , 1998, Science.

[11]  A. Basbaum,et al.  The Cloned Capsaicin Receptor Integrates Multiple Pain-Producing Stimuli , 1998, Neuron.

[12]  D. Storm,et al.  Phosphorylation and Inhibition of Olfactory Adenylyl Cyclase by CaM Kinase II in Neurons a Mechanism for Attenuation of Olfactory Signals , 1998, Neuron.

[13]  H. Robertson.  Two large families of chemoreceptor genes in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae reveal extensive gene duplication, diversification, movement, and intron loss. , 1998, Genome research.

[14]  Cori Bargmann,et al.  The Gα Protein ODR-3 Mediates Olfactory and Nociceptive Function and Controls Cilium Morphogenesis in C. elegans Olfactory Neurons , 1998, Neuron.

[15]  Cori Bargmann,et al.  OSM-9, A Novel Protein with Structural Similarity to Channels, Is Required for Olfaction, Mechanosensation, and Olfactory Adaptation inCaenorhabditis elegans , 1997, The Journal of Neuroscience.

[16]  Cornelia I Bargmann,et al.  Reprogramming Chemotaxis Responses: Sensory Neurons Define Olfactory Preferences in C. elegans , 1997, Cell.

[17]  Cori Bargmann,et al.  Environmental signals modulate olfactory acuity, discrimination, and memory in Caenorhabditis elegans. , 1997, Learning & memory.

[18]  T. Kurahashi,et al.  Mechanism of odorant adaptation in the olfactory receptor cell , 1997, Nature.

[19]  Cori Bargmann,et al.  odr-10 Encodes a Seven Transmembrane Domain Olfactory Receptor Required for Responses to the Odorant Diacetyl , 1996, Cell.

[20]  Cori Bargmann,et al.  Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans , 1995, Cell.

[21]  I. Mori,et al.  Neural regulation of thermotaxis in Caenorhabditis elegans , 1995, Nature.

[22]  Cornelia I Bargmann,et al.  Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans , 1995, Neuron.

[23]  S. R. Wicks,et al.  Integration of mechanosensory stimuli in Caenorhabditis elegans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  Cori Bargmann,et al.  Odorant-selective genes and neurons mediate olfaction in C. elegans , 1993, Cell.

[25]  H. Horvitz,et al.  A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[26]  P. Groves,et al.  Habituation: a dual-process theory. , 1970, Psychological review.

[27]  Cori Bargmann,et al.  Signal transduction in the Caenorhabditis elegans nervous system. , 1998, Annual review of neuroscience.

[28]  Cori Bargmann,et al.  Chemotaxis and Thermotaxis , 1997 .

[29]  D. Riddle,et al.  Neural Plasticity -- C. elegans II , 1997 .

[30]  Cori Bargmann,et al.  Chemosensory cell function in the behavior and development of Caenorhabditis elegans. , 1990, Cold Spring Harbor symposia on quantitative biology.

[31]  W. Wood.  The Nematode Caenorhabditis elegans , 1988 .