A Single Set of Interneurons Drives Opposite Behaviors in C. elegans

Guillermin, Manon L.; Carrillo, Mayra A.; Hallem, Elissa A.

doi:10.1016/j.cub.2017.07.023

Cited by 46 publications

(85 citation statements)

References 76 publications

(87 reference statements)

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“…Because of such robustness in the deficient circuits, previous studies might have faced difficulties in identifying and defining neural circuits for thermotaxis (Beverly et al, 2011; Luo et al, 2014a). Similar problems might have appeared in the studies on other types of behavior such as isothermal tracking (Mori and Ohshima, 1995), chemotaxis (Guillermin et al, 2017; Iino and Yoshida, 2009; Luo et al, 2014b), and exploratory behavior (Gray et al, 2005). Also in crustacean and mammalian brain networks, robustness is an obstacle for inferring functional connections that can only be resolved by applying statistical methods (Schwab et al, 2010; Srinivasan and Stevens, 2011).…”

Section: Discussionmentioning

confidence: 56%

“…One candidate source for this flexibility is the neurotransmission from sensory neurons to interneurons. Several studies have reported that a single sensory neuron can evoke different kind of responses in an identical interneuron through glutamatergic and/or peptidergic transmissions (Guillermin et al, 2017; Kuhara et al, 2011; Narayan et al, 2011; Tsunozaki et al, 2008). Such alterations in synaptic activity can drive opposite behaviors in response to identical stimuli (Cho et al, 2016; Guillermin et al, 2017; Hawk et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

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

Ikeda

Nakano

et al. 2018

Preprint

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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 TT 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...

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Section: Discussionmentioning

confidence: 56%

Section: Discussionmentioning

confidence: 99%

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

Ikeda

Nakano

et al. 2018

Preprint

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“…A number of previous studies indicated that the opposing valences of sensory stimuli are encoded by two separate populations of neurons, each of which represents either positive or negative valence of the stimuli 37,38 . By contrast, recent studies proposed an alternative strategy, wherein a single population of neurons responds to appetitive or aversive stimuli and represents the positive or negative valence of the stimuli by increasing or decreasing neuronal activity 39,40 . Specifically, CRF (corticotropin-releasing factor)-releasing neurons in the paraventricular nucleus of the hypothalamus are activated by aversive stimuli and inhibited by appetitive stimuli 40 .…”

Section: Discussionmentioning

confidence: 99%

“…Specifically, CRF (corticotropin-releasing factor)-releasing neurons in the paraventricular nucleus of the hypothalamus are activated by aversive stimuli and inhibited by appetitive stimuli 40 . Likewise, in C. elegans , experience-dependent modulation enables a single set of interneurons to elicit bidirectional responses to carbon dioxide, which can be either attractive or aversive, depending on prior experience 39 . Thus, these observations indicate a previously unrecognized mechanism of valence coding for even a single modality of stimulus, in which the bidirectional activity in a single population of neurons can be modulated by prior experience and environment to represent stimulus valence.…”

Section: Discussionmentioning

confidence: 99%

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

Nakano

Ikeda

Tsukada

et al. 2019

Preprint

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24Presynaptic plasticity is known to modulate the strength of synaptic transmission. 25However, it remains unknown whether regulation in presynaptic neurons alters the 26 directionality -positive or negative-of postsynaptic responses. We report here that the 27 C. elegans homologs of MAST kinase, Stomatin and Diacylglycerol kinase act in a 28 thermosensory neuron to elicit in its postsynaptic neuron an excitatory or inhibitory 29 response that correlates with the valence of thermal stimuli. By monitoring neural 30 activity of the valence-coding interneuron in freely behaving animals, we show that 31 the alteration between excitatory and inhibitory responses of the interneuron is 32 mediated by controlling the balance of two opposing signals released from the 33 presynaptic neuron. These alternative transmissions further generate opposing 34 behavioral outputs necessary for the navigation on thermal gradients. Our findings 35 reveal the previously unrecognized capability of presynaptic regulation to evoke 36 bidirectional postsynaptic responses and suggest a molecular mechanism of 37 determining stimulus valence. 38 4 neural circuit that promotes or inhibits feeding behaviors. 54Contrary to these developmentally programmed, stereotyped behaviors, the 55 valence associated with certain sensory stimuli can vary depending on the past experience, 56 the current environmental context and the stimulus intensity 9 . For example, olfactory 57 preferences to the same odorants can differ depending on the odorant concentration 10 . 58Studies of worms, flies and mammals suggested a common feature of neural mechanism 59 underlying the change in these odorant valences, wherein different concentrations of the 60 same odorants recruit distinct sets of olfactory neurons and consequently change the 61 perception of the same odorants [11][12][13] . However, the extent to which the brain utilizes 62 different encoding strategies for alternating stimulus valence remains largely unexplored. In 63 particular, the molecular and circuit mechanisms underlying the perception of altering 64 valence for other sensory modalities are not yet understood. 65The compact nervous system of C. elegans consisting of only 302 neurons 66 provides an excellent opportunity to explore these questions 14 . C. elegans exhibits 67 thermotaxis behavior 15 , in which the valence of thermal information varies depending on 68 5 the past experience, current temperature environment and feeding states. Specifically, the 69 temperature preference of C. elegans is plastic and determined by the cultivation 70 temperature, in which animals that are cultivated at a constant temperature with food 71 migrate toward that cultivation temperature on a thermal gradient without food 15 . When 72 animals were placed at the temperature below the cultivation temperature they migrate up 73 the thermal gradient, while above the cultivation temperature they move down the gradient, 74indicating that the valence associated with thermal stimuli alternates in opposing manners 75 dependin...

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“…103 pmk-3 mutants fail to express the BAG-neuron-specific FMRF-amide neuropeptide flp-17 104 ( Figure 1A). FLP-17 peptides activate the Gi/o-coupled receptor EGL-6 to inhibit motor neurons 105 in the C. elegans egg laying system (Ringstad and Horvitz 2008), and were recently shown to 106 also be required for BAG-neuron-dependent CO2 avoidance behavior (Guillermin et al 2017; 107 Lee et al 2017). To determine whether the behavioral defect of pmk-3 mutants can be explained 108 by their failure to express flp-17 neuropeptides, we compared the CO2 avoidance defects of 109 pmk-3 and flp-17 mutants.…”

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confidence: 99%

Repression of an activity-dependent autocrine insulin signal is required for sensory neuron development inC. elegans

Horowitz¹,

Brandt²,

Ringstad³

2018

Preprint

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24Nervous system development is instructed both by genetic programs and activity-dependent 25 refinement of gene expression and connectivity. How these mechanisms are integrated remains 26 poorly understood. Here, we report that the regulated release of insulin-like peptides (ILPs) 27 during development of the C. elegans nervous system accomplishes such an integration. We 28 find that the p38 MAP kinase PMK-3, which is required for the differentiation of chemosensory 29 BAG neurons, functions by limiting expression of an autocrine ILP signal that represses a 30 chemosensory-neuron fate. ILPs are released from BAGs in an activity-dependent manner 31 during embryonic development, and regulate neurodifferentiation through a non-canonical 32 insulin receptor signaling pathway. The differentiation of a specialized neuron-type is, therefore, 33 coordinately regulated by a genetic program that controls ILP expression and by neural activity, 34 which regulates ILP release. Autocrine signals of this kind may have general and conserved 35 functions as integrators of deterministic genetic programs with activity-dependent mechanisms 36 during neurodevelopment. 37 38 2017). How these two different mechanisms -one specified and the other activity-dependent -47 are integrated during nervous system development remains poorly understood. 48The C. elegans nervous system displays a wide range of neuronal diversity, and is a 49 powerful model to study neuronal differentiation (White et al. 1986;Hobert et al. 2016). The 50 mostly invariant cell lineage that generates the C. elegans nervous system (Sulston 1977; 51 Sulston 1983) suggests that neuronal differentiation in C. elegans is principally determined by 52 genetic programs intrinsic to the cell-lineage. Indeed, many studies have identified transcription 53 factors that act in specific sub-lineages to promote specific neural fates (Hobert 2016). However, 54there are also important roles for neuronal activity during development of the C. elegans nervous 55 system. For example, there is a striking role for activity of embryonic AWC chemosensory 56 neurons in determining their differentiation into functionally distinct subtypes (Troemel 1999; 57 Sagasti 2001). More recently, it has been found that there is a critical period during which neural 58 activity instructs circuit assembly in the C. elegans motor system (Barbagallo et al. 2017). Post-59 developmentally, neural and sensory activity is required for maintaining the proper morphology 60 of chemosensory neurons (Peckol 1999; Mukhopadhyay et al. 2008), and for expression of 61 chemosensory receptors and neuropeptides that define specific chemosensory neuron fates 62 (Peckol et al. 2001; Gruner et al. 2014; Rojo Romanos et al. 2017). Like the vertebrate nervous 63 system, therefore, development of the C. elegans nervous system requires both lineally 64 programmed gene regulation and neural activity. 65 We have investigated mechanisms required for the development of a pair of C. elegans 66 sensory neurons -the BAGs, which se...

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A Single Set of Interneurons Drives Opposite Behaviors in C. elegans

Cited by 46 publications

References 76 publications

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

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

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

Repression of an activity-dependent autocrine insulin signal is required for sensory neuron development inC. elegans

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