Thermotaxis inCaenorhabditis elegansAnalyzed by Measuring Responses to Defined Thermal Stimuli

William S. Ryu, Aravinthan D. T. Samuel
2002 Journal of Neuroscience  
In a spatial thermal gradient, Caenorhabditis elegans migrates toward and then isothermally tracks near its cultivation temperature. A current model for thermotactic behavior involves a thermophilic drive (involving the neurons AFD and AIY) and cryophilic drive (involving the neuron AIZ) that balance at the cultivation temperature. Here, we analyze the movements of individual worms responding to defined thermal gradients. We found evidence for a mechanism for migration down thermal gradients
more » ... t is active at temperatures above the cultivation temperature, and a mechanism for isothermal tracking that is active near the cultivation temperature. However, we found no evidence for a mechanism for migration up thermal gradients at temperatures below the cultivation temperature that might have supported the model of opposing drives. The mechanisms for migration down gradients and isothermal tracking control the worm's movements in different manners. Migration down gradients works by shortening (lengthening) the duration of forward movement in response to positive (negative) temperature changes. Isothermal tracking works by orienting persistent forward movement to offset temperature changes. We believe preference for the cultivation temperature is not at the balance between two drives. Instead, the worm activates the mechanism for isothermal tracking near the cultivation temperature and inactivates the mechanism for migration down gradients near or below the cultivation temperature. Inactivation of the mechanism for migration down gradients near or below the cultivation temperature requires the neurons AFD and AIY. In their classic study of thermotaxis in Caenorhabditis elegans, Hedgecock and Russell (1975) demonstrated that worms navigating spatial thermal gradients aggregate near their cultivation temperature (T c ). Within 3°C of this temperature, worms track isotherms, deviating from a given isotherm by as little as ϳ0.05°C. Hedgecock and Russell (1975) also harvested mutants that failed to aggregate at T c and found that they could be classified as thermophilic (aggregating in warmer regions of a plate), cryophilic (aggregating in colder regions of a plate), or atactic (not aggregating at all). On the basis of this classification, Hedgecock and Russell (1975) suggested that competing thermophilic and cryophilic drives produce thermotactic behavior and that isothermal tracking occurs at their balance. Mori and Ohshima (1995) identified neurons involved in thermotaxis by laser ablation. The resulting defects in behavior could be organized in the same manner as the mutant behaviors shown by Hedgecock and Russell (1975) , namely thermophilic (obtained by lesion of the AIZ neuron), cryophilic (obtained by lesion of the AFD and/or AIY neuron), or atactic (obtained by lesion of the RIA neuron or multiple neurons). Thus, Mori and Ohshima (1995) proposed that the AFD and AIY neurons comprise the thermophilic drive, AIZ comprises the cryophilic drive, and RIA compares the two drives. Although the labels thermophilic, cryophilic, and atactic describe aberrant aggregation patterns on spatial gradients, they do not explain how putative thermophilic and cryophilic drives direct the worm's movements toward the cultivation temperature. Also, it is unclear whether thermophilic and cryophilic drives are active during isothermal tracking or whether isothermal tracking represents a distinct mechanism. The present study aimed to determine the mechanisms underlying thermotaxis, the manner in which they direct the worm's movements, and the roles of participating neurons. We studied the movements of worms as they performed thermotaxis by (1) tracking worms crawling on the surface of agar plates with defined spatial or temporal thermal gradients and (2) monitoring the swimming motions of a worm suspended in a droplet subjected to thermal stimuli. In addition to wild-type (N2) worms, we studied thermotaxis mutants that have been shown to have developmental defects in AFD or AIY neurons, which have been identified by Mori and Ohshima (1995) to be involved in thermotaxis. We found strong evidence for a mechanism for migration down gradients toward the cultivation temperature that might correspond to the cryophilic drive of the prevailing model, but no compelling evidence for a mechanism for migration up gradients that might correspond to the thermophilic drive. The mechanism for migration down gradients modulates run duration but not run orientation, shortening runs in response to positive changes in temperature and lengthening runs in response to negative changes in temperature. The mechanism for isothermal tracking modulates run orientation to offset either positive or negative
doi:10.1523/jneurosci.22-13-05727.2002 pmid:12097525 fatcat:kfplt7zlhnch3cptufnfgoxbjy