Abstract
C. elegans will orient and travel in a straight uninterrupted path directly towards the negative pole of a DC electric field. We have sought to understand the strategy worms use to navigate to the negative pole in a uniform electric field that is fixed in both direction and magnitude. We examined this behavior by quantifying three aspects of electrotaxis behavior in response to different applied field strengths: the mean approach trajectory angles of the animals’ tracks, turning behavior (pirouettes) and average population speeds. We determined that C. elegans align directly to the negative pole of an electric field at sub-preferred field strength and alter approach trajectories at higher field strengths to maintain taxis within a preferred range we have calculated to be ~ 5V/cm. We sought to identify the sensory neurons responsible for the animals’ tracking to a preferred field strength. eat-4 mutant animals defective in glutamatergic signaling of the amphid sensory neurons are severely electrotaxis defective and ceh-36 mutant animals, which are defective in the terminal differentiation of two types of sensory neurons, AWC and ASE, are partially defective in electrotaxis. To further elucidate the role of the AWC neurons, we examined the role of each of the pair of AWC neurons (AWCOFF and AWCON), which are functionally asymmetric and express different genes. nsy-5/inx-19 mutant animals, which express both neurons as AWCOFF, are severely impaired in electrotaxis behavior while nsy-1 mutants, which express both neurons as AWCON, are able to differentiate field strengths required for navigation to a specific field strength within an electric field. We also tested a strain with targeted genetic ablation of AWC neurons and found that these animals showed only slight disruption of directionality and turning behavior. These results suggest a role for AWC neurons in which complete loss of function is less disruptive than loss of functional asymmetry in electrotaxis behavior within a uniform fixed field.
Highlights
An underlying question in understanding behavior is how a sensory stimulus is integrated into the neural signals and pathways needed to elicit a motor response
We have found that mutant animals that are defective in expression of genes involved in late differentiation and/or functional asymmetry of the AWC neuron display defects in electrotaxis
To determine which of the EAT-4 expressing amphid sensory neurons might be required for response to a uniform electric field, we examined ceh-36 mutant animals, which are defective in an OTD/OTX homeodomain protein transcription factor that is required for terminal differentiation of AWC neurons and ASE neurons [42, 43]
Summary
An underlying question in understanding behavior is how a sensory stimulus is integrated into the neural signals and pathways needed to elicit a motor response. We were interested in the behavioral strategies and sensory pathway needed for this animal to integrate electric field stimuli into a motor response in a fixed uniform electric field under different field strengths. Previous studies examining electrotaxis behavior [7, 18] utilized a rotating field, which measures the worm’s ability to respond to a field varying in both direction and strength requiring reorientation and reversal maneuvers. Our studies utilize a uniform field fixed in direction to measure the ability of the worm to sense field strength and alter its approach trajectory by small shallow anterior head movements. Using an automated tracking system [23], we measured the animals’ directionality, speed and turning behavior to determine the neural basis for the widening of animal trajectories at higher field strengths in an approximate uniform electric field
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