Abstract
Optimization of the types and timing of avoidance behaviors depending on the intensity of a noxious stimulus is essential for survival; however, processing in the central nervous system and its developmental basis are largely unknown. Here, we report that Caenorhabditis elegans preferentially selects one of three different types of avoidance behaviors depending on the strength of the noxious stimulus. We screened 210 neuronal transcription factors using a combination of optogenetics and RNA interference methods and identified 19 candidates required for avoidance behaviors. One candidate, gene lin-32 (abnormal cell LINeage 32), which encodes an atonal homolog, is required for the neural fate determination of AIB interneurons and functions by regulating the expression of electrical and chemical synapse genes, namely, inx-1 (innexin 1) and AMPA-type ionotropic glutamate receptor glr-1. When examined by Ca imaging, AIB showed an OFF calcium increase to the noxious stimulus. The OFF calcium increase was provoked only by strong stimulation, suggesting a role for optimization of the avoidance behavior. However, lin-32 mutants showed an impaired AIB OFF calcium increase, concomitant with a reduced occurrence of the dynamic avoidance behavior called the "omega turn". The AIB neural responses may be transferred to downstream inter/motor neurons projecting to the neck muscles via electrical synapses comprising inx-1. Finally, we found a correlation between powerful contractions of the neck muscles and omega turns. Thus, the central regulation of the magnitude and timing of activation of the AIB interneurons optimizes the probability of omega turn depending on the stimulus context.
Highlights
Animals optimize a behavioral response, such as the mode, strength or duration of the stimulus at the proper time, to sensory stimuli depending on context [1]
We report the neural and molecular mechanisms underlying the optimization of avoidance behaviors depending on the intensity of a mono-modal noxious stimulus in C. elegans
To clarify how C. elegans optimizes avoidance behaviors by selecting one of three types of behaviors depending on the strength of a mono-modal noxious stimulus (Fig 1A), we used optogenetics to activate only the ASH-mediated neural circuit and apply quantitatively controlled stimulation (12.5%, 25%, and 100% blue light) [15]
Summary
Animals optimize a behavioral response, such as the mode, strength or duration of the stimulus at the proper time, to sensory stimuli depending on context [1]. Simple all-or-none reflex responses are well documented for many behaviors, including avoidance behaviors such as touch responses [2,3,4,5,6], the understanding of optimization of avoidance behaviors becomes complicated when apparently similar noxious stimuli induce distinct behavioral patterns Such behaviors may likely involve the central nervous system to develop diverse behavioral repertoires [7,8], and defects in avoidance circuit formation and/or function in the central nervous systems may lead to a life crisis or a bias of the sensory behavior [9]. A simple model animal, C. elegans, basically exhibits three types of avoidance behaviors, namely, the short reversal, long reversal, and omega turn, upon direct contact of the head region with a noxious stimulus [10]. C. elegans must weigh the physical risks due to the nociceptive stimulus and it should choose the deliberate way of avoidance behaviors
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