Behavioral evidence for chemosensory and thermosensory pathway convergence in the Caenorhabditis elegans nervous system

Georgia Journal of Science, 2002 by Davis, Bowman O Jr, VanBrackle, Lewis, Pittard, Darren

Abstract

The nematode, Caenorhabditis elegans, is an established model system to explore the ways simple nervous systems detect and direct organismal responses to environmental changes. C. elegans possesses specialized receptor cells for the detection of a variety of environmental stimuli. Separate cell types respond to volatile chemical and thermal stimuli and the neural pathways for these show anatomical evidence of convergence. This work reports findings from behavioral assays during simultaneous exposure of nematodes to both thermal differences and attractant volatile chemicals. Combined exposure to benzaldehyde and cold neutralized the behavioral responses to both stimuli in 24 deg C acclimated worms. Diacetyl and mild thermal stimulation produced the same effect with 16 deg C acclimated worms. Benzaldehyde appears to interfere with thermophilic circuitry while diacetyl acts similarly with cryophilic circuitry.

Keywords: Caenorhabditis elegans, neurobiology, chemosensory, thermosensory.

Introduction

As organisms interact successfully with their surroundings, certain environmental cues generate specific and appropriate behaviors. Sensory neurons detect environmental changes, encode the information, and pass this information into neural circuits where it is integrated and ultimately produces an appropriate behavioral response. Details of the mechanisms by which this is accomplished have been poorly understood. However, recent studies using the model Caenorhabditis elegans nervous system have begun to shed light on the ways that innate, "hard wired" neural circuits generate predictable behavioral responses (1).

For a number of reasons the nematode Caenorhabditis elegans has become a favored laboratory model for neurobiological studies. It is the only organism for which the entire nervous system, consisting of 302 neurons, has been completely mapped by serial section electron microscopy, elucidating the various chemical synapses and gap junction connections (2). C. elegans also exhibits a simple behavioral repertoire consisting primarily of forward movements (backward waves), backward movements (reversals), and omega waves, which produce 180 deg changes in direction (3, 4). These behavioral elements can be monitored to distinguish between chemical attractants and repellents. Rutherford and Croll (5) found reversal activity to increase in repellent chemicals (D-tryptophan) and to decrease in attractant chemicals (NaCl) making it possible to distinguish between attractant and repellent chemicals by the behaviors they elicit. It was also observed that D-tryptophan had no effect on thermal orientation in a gradient or on isothermal tracking in which a worm moves circularly in a radial gradient at its preferred temperature, suggesting that chemical and thermal stimulation operate through separate, nonconvergent pathways.

Chemosensation in C. elegans exhibits both gustatory and olfactory components associated with the amphid sensilla. Phasmid and inner labial sensilla do not appear to be essential for chemotaxis. Water-soluble chemicals are detected by a group of amphid neurons (ASE, ADF, ASG, ASI, and ASK), in which ciliated endings are exposed to the external environment via the amphid channel and comprise the "gustatory" sensory mechanism of the nematode (6). Another pair of chemosensory amphid neurons (AWA and AWC) does not have exposed dendritic endings and comprise an "olfactory" mechanism sensitive to volatile organic attractants. Similarly, the AWB amphid neuron is part of the olfactory mechanism but senses volatile organic repellents instead (4, 1). The thermosensory neurons, AFD, of the amphids also have no exposed dendritic endings (8). The chemosensory AWA, AWB, and AWC neurons and the thermosensory AFD neurons all show strong connections to the AIY and AIZ interneurons, representing an anatomical convergence between olfactory and thermosensory pathways (2, 4).

Laser ablation studies, along with mutant isolation and genetic analysis, have begun to reveal the functions of many of these neurons and their associated circuits (9, 10, 11, 12, 1, 13). It has also been demonstrated that interactions exist between chemosensory and thermosensory mechanisms within the C. elegans nervous system. Dusenberry and Barr (14) tested thermophilic (EH61 and EH71) and cyrophilic (EH65 and EH6) mutants and found them to be abnormal in some of their water-soluble chemical responses suggesting some overlap in chemosensory and thermosensory mechanisms. Komatsu, et al., (9) found that thermotaxis deficient mutants (tax-4) also failed to respond to AWC sensed odorants. Since behavioral and genetic similarities apparently exist between the mechanisms for chemotaxis and thermotaxis, shared cellular and molecular components have been suggested (10). In fact, Mori and Oshima (11) proposed a model neural circuit to explain cryophilic, "down gradient" movement, thermophilic, "up gradient" movement, and isothermal movement where the nematode remains at its culture temperature. Their model demonstrated that the interneurons AN and AIZ respectively were primarily responsible for "up" and "down" gradient movements. A thermosensory neuron, AFD, inputs directly to AIY, but its cryophilic counterpart, connecting to AIZ, remains unidentified.