Publications by Year: 2007

Clark, D., Gabel, C., Lee, T. & Samuel, A. Short-Term Adaptation and Temporal Processing in the Cryophilic Response of Caenorhabditis elegans. Journal of Neurophysiology 97, 1903-1910 (2007). Publisher's VersionAbstract
When navigating spatial thermal gradients, the nematode C. elegans migrates toward colder temperatures until it reaches its previous cultivation temperature, exhibiting cryophilic movement. The strategy for effecting cryophilic movement is the biased random walk: C. elegans extends (shortens) periods of forward movement that are directed down (up) spatial thermal gradients by modulating the probability of reorientation. Here, we analyze the temporal sensory processor that enables cryophilic movement by quantifying the movements of individual worms subjected to defined temperature waveforms. We show that step increases in temperature as small as 0.05°C lead to transient increases in the probability of reorientation followed by gradual adaptation to the baseline level; temperature downsteps leads to similar but inverted responses. Short-term adaptation is a general property of sensory systems, allowing organisms to maintain sensitivity to sensory variations over broad operating ranges. During cryophilic movement C. elegans also uses the temporal dynamics of its adaptive response to compute the time derivative of gradual temperature variations with exquisite sensitivity. On the basis of the time derivative, the worm determines how it is oriented in spatial thermal gradients during each period of forward movement. We show that the operating range of the cryophilic response extends to lower temperatures in ttx-3 mutants, which affects the development of the AIY interneurons. We show that the temporal sensory processor for the cryophilic response is affected by mutation in the EAT-4 glutamate vesicular transporter. Regulating the operating range of the cryophilic response and executing the cryophilic response may have separate neural mechanisms.
Clark, D., Gabel, C., Gabel, H. & Samuel, A.D. Temporal Activity Patterns in Thermosensory Neurons of Freely Moving Caenorhabditis elegans Encode Spatial Thermal Gradients. Journal of Neuroscience 27, 23, 6083– 6090 (2007). Publisher's VersionAbstract
Our understanding of the operation of neurons and neuronal circuits has come primarily from probing their activity in dissected, anesthetized, or restrained animals. However, the behaviorally relevant operation of neurons and neuronal circuits occurs within intact animals as they freely perform behavioral tasks. The small size and transparency of the nematode Caenorhabditis elegans make it an ideal system for noninvasive, optical measurements of neuronal activity. Here, we use a high signal-to-noise version of cameleon, a fluorescent calcium-binding protein, to quantify the activity of the AFD thermosensory neuron of individual worms freely navigating spatial thermal gradients. We find that AFD activity is directly coupled to the worm's exploratory movements in spatial thermal gradients. We show that the worm is able, in principle, to evaluate and guide its own thermotactic behaviors with respect to ambient spatial thermal gradients by monitoring the activity of this single thermosensory neuron.
Korta, J., Clark, D.A., Gabel, C.V., Mahadevan, L. & Samuel, A.D. Mechanosensation and mechanical load modulate the locomotory gait of swimming C. elegans. Journal of Experimental Biology 210, 13, 2383-2389 (2007). Publisher's VersionAbstract
Animals move through their environments by selecting gaits that are adapted to the physical nature of their surroundings. The nematode Caenorhabditis elegans swims through fluids or crawls on surfaces by propagating flexural waves along its slender body and offers a unique opportunity for detailed analysis of locomotory gait at multiple levels including kinematics,biomechanics and the molecular and physiological operation of sensory and motor systems. Here, we study the swimming gait of C. elegans in viscous fluids in the range 0.05-50 Pa s. We find that the spatial form of the swimming gait does not vary across this range of viscosities and that the temporal frequency of the swimming gait only decreases by about 20% with every 10-fold increase in viscosity. Thus, C. elegans swims in low gear,such that its musculature can deliver mechanical force and power nearly 1000-fold higher than it delivers when swimming in water. We find that mutations that disrupt mechanosensation, or the laser killing of specific touch receptor neurons, increase the temporal frequency of the undulating gait, revealing a novel effect of mechanosensory input in regulating the putative central pattern generator that produces locomotion. The adaptability of locomotory gait in C. elegans may be encoded in sensory and motor systems that allow the worm to respond to its own movement in different physical surroundings.
Gabel, C., et al. Neural Circuits Mediate Electrosensory Behavior in Caenorhabditis elegans. Journal of Neuroscience 27, 28, 7586 –7596 (2007). Publisher's VersionAbstract
The nematode Caenorhabditis elegans deliberately crawls toward the negative pole in an electric field. By quantifying the movements of individual worms navigating electric fields, we show that C. elegans prefers to crawl at specific angles to the direction of the electric field in persistent periods of forward movement and that the preferred angle is proportional to field strength. C. elegans reorients itself in response to time-varying electric fields by using sudden turns and reversals, standard reorientation maneuvers that C. elegans uses during other modes of motile behavior. Mutation or laser ablation that disrupts the structure and function of amphid sensory neurons also disrupts electrosensory behavior. By imaging intracellular calcium dynamics among the amphid sensory neurons of immobilized worms, we show that specific amphid sensory neurons are sensitive to the direction and strength of electric fields. We extend our analysis to the motor level by showing that specific interneurons affect the utilization of sudden turns and reversals during electrosensory steering. Thus, electrosensory behavior may be used as a model system for understanding how sensory inputs are transformed into motor outputs by the C. elegans nervous system.
Chi, C., et al. Temperature and food mediate long-term thermotactic behavioral plasticity by association-independent mechanisms in C. elegans. Journal of Experimental Biology 210, 22, 4043-4052 (2007). WebsiteAbstract
Thermotactic behavior in the nematode Caenorhabditis elegansexhibits long-term plasticity. On a spatial thermal gradient, C. elegans tracks isotherms near a remembered set-point(TS) corresponding to its previous cultivation temperature. When navigating at temperatures above its set-point(T>TS), C. elegans crawls down spatial thermal gradients towards the TS in what is called cryophilic movement. The TS retains plasticity in the adult stage and is reset by ∼4 h of sustained exposure to a new temperature. Long-term plasticity in C. elegans thermotactic behavior has been proposed to represent an associative learning of specific temperatures conditioned in the presence or absence of bacterial food. Here,we use quantitative behavioral assays to define the temperature and food-dependent determinants of long-term plasticity in the different modes of thermotactic behavior. Under our experimental conditions, we find that starvation at a specific temperature neither disrupts TSresetting toward the starvation temperature nor induces learned avoidance of the starvation temperature. We find that prolonged starvation suppresses the cryophilic mode of thermotactic behavior. The hen-1 and tax-6 genes have been reported to affect associative learning between temperature and food-dependent cues. Under our experimental conditions,mutation in the hen-1 gene, which encodes a secreted protein with an LDL receptor motif, does not significantly affect thermotactic behavior or long-term plasticity. Mutation in the tax-6 calcineurin gene abolishes thermotactic behavior altogether. In summary, we do not find evidence that long-term plasticity requires association between temperature and the presence or absence of bacterial food.