Circuit Degeneracy Facilitates Robustness and Flexibility of Navigation Behavior in C.elegans

Abstract

20Animal behaviors are robust and flexible. To elucidate how these two conflicting 21 features of behavior are encoded in the nervous system, we analyzed the neural circuits 22 generating a C. elegans thermotaxis behavior, in which animals migrate toward the past 23 cultivation temperature (T c ). We identified multiple circuits that are highly overlapping 24 but individually regulate distinct behavioral components to achieve thermotaxis. When 25 the regulation of a behavioral component is disrupted following single cell ablations, the 26 other components compensate the deficit, enabling the animals to robustly migrate 27 toward the T c . Depending on whether the environmental temperature surrounding the 28 animals is above or below the T c , different circuits regulate the same behavioral 29 components, mediating the flexible switch between migration up or down toward the T c . 30These context-dependencies within the overlapping sub-circuits reveal the 31 implementation of degeneracy in the nervous system, providing a circuit-level basis for 32 the robustness and flexibility of behavior. 105C. elegans animals are known to navigate using a series of stereotyped movements, 106 designated behavioral components (Croll, 1975; Iino and Yoshida, 2009; 107 Pierce- Shimomura et al., 1999). We first attempted to extract the behavioral components 108 during thermotaxis by employing a Multi-Worm Tracker (MWT) (Swierczek et al., 109 2011). MWT simultaneously captured the positions and postures of approximately 120 110 animals ( Figure 1A), and these data were further analyzed by a custom-built MATLAB 111 script to detect the behavioral components (see Materials and methods). 112For the thermotaxis assays, we set cultivation temperature (T c ) as 20°C and the 113 temperature of the center in the assay plate as either 17°C or 23°C ( Figure 1B). Animals 114 were placed at the center of the plate, and then we evaluated the animals' migrations by 115 calculating thermotaxis index (TTX index), according to the equation shown in Figure 116 1C. TTX index is 1 when all the animals are in the coldest fraction of the plate and 8 117 when all the animals are in the warmest fraction. Consistent with our previous report 118 (Ito et al., 2006), the animals reached their T c within approximately 30 minutes in two 119 conditions ( Figure 1D and Movie S1), plate centered at 17°C or 23°C. In this study, we 120 thus focused on the first 30 minutes from the start of the assays. To analyze the 121 behaviors during the migrations toward the T c , we analyzed the animals that were 122 distributed in the center four fractions of the assay plate; 15.5-18.5°C for the T<T c 123 condition and 21.5-24.5°C for the T>T c condition (Figure 2A). Behaviors were 124 essentially classified into three behavioral components: turns, reversals, and curves 125 ( Figure 2B). Turns were further classified into omega turns and shallow turns (Kim et 126 al., 2011; Schild and Glauser, 2013), and reversals were further classified into reversals 127 and reve...

Presynaptic MAST kinase controls opposing postsynaptic responses to convey stimulus valence in Caenorhabditis elegans

“…To address how the alteration in the modes of the AFD-AIY communication contributes to the regulation of TTX behavior, we undertook multiworm tracking analysis (42). We classified the animal behavior into several behavioral components discernable during C. elegans locomotion, such as forward locomotion, omega turn, shallow turn, reversal, and reversal turn (43)(44)(45)(46)(47). Previous studies showed that the wild-type animals modulate the run durations such that the duration of run toward the cultivation temperature would be lengthened (20, 48-50).…”

“…S8A, and see also ref. 43). In addition, consistent with the previous reports of regulation of run duration during TTX (20, 48-50), we observed that the wild-type animals exhibited a significant bias in the frequency of reversal turn.…”

Presynaptic MAST Kinase Controls Bidirectional Post-Synaptic Responses to Convey Stimulus Valence in C. elegans

“…6), we found that the curve, change in the moving direction during forward locomotion, was one such component (Fig. 6a): the wild-type animals behaving below the cultivation temperature showed curving bias toward warmer temperature when migrating up the thermal gradient, while they curve toward colder temperature above the cultivation temperature 36 (Fig. 6a), suggesting that this regulation of the curve would drive the animals toward the cultivation temperature.…”

“…To address how the alteration in the modes of the AFD-AIY communication contributes to the regulation of thermotaxis behavior, we undertook multi-worm tracking analysis 35 . We classified the animal behavior into several behavioral components discernable during C. elegans locomotion, such as forward locomotion, turns and reversals 36 . We sought the behavioral components that were oppositely biased below or above the cultivation temperature in the wild-type animals, and were oppositely affected by the cryophilic ( kin-4 and dgk-1 ) or thermophilic ( mec-2 ) mutations.…”

“…Multi worm tracking analysis was performed as described 36 . Animals were cultivated at 20 °C and were placed on the thermal gradient with the center temperature of 18.5 °C or 21.5 °C to monitor their behaviors below or above the cultivation temperature, respectively.…”