Molecular and cellular modulators for multisensory integration in C. elegans

Harris, Graham P.; Wu, Taihong; Linfield, Gaia; Choi, Myung-Kyu; Li, He; Zhang, Yun

doi:10.1371/journal.pgen.1007706

Cited by 24 publications

(18 citation statements)

References 114 publications

(152 reference statements)

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“…Figure 4421C), similarly to the observations made using the repellent 2-nonanone(Harris et al, 2019),443 suggesting the multisensory integration of attractive and aversive impulses for decision making.…”

supporting

confidence: 71%

Toxic stress-specific cytoprotective responses regulate learned behavioral decisions inC. elegans

Hajdú

Gecse

Taisz

et al. 2020

Preprint

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19Background 20 Protection of organismal integrity involve physiological stress responses and behavioral 21 defenses. Recent studies in the roundworm Caenorhabditis elegans have shown that pathogen 22 and toxin exposure simultaneously stimulate cellular stress and detoxification responses and 23 aversive behavior. However, whether a coordinate regulation exists between cellular and 24 neurobehavioral defenses remains unclear. 25 Results 26Here we show that exposure of C. elegans to high concentrations of naturally attractive food-27 derived odors, benzaldehyde and diacetyl, induces toxicity and aversive behavior. 28 Benzaldehyde preconditioning activates systemic cytoprotective stress responses involving 29 DAF-16/FOXO, SKN-1/Nrf and Hsp90 in somatic cells, which confer behavioral tolerance to 30 benzaldehyde and cross-tolerance to the structurally similar methyl-salicylate, but not to the 31 structurally unrelated diacetyl. In contrast, diacetyl preconditioning augments diacetyl 32 avoidance and does not induce apparent molecular defenses. Reinforcement of the experiences 33 using massed training forms relevant associative memories. Memory retrieval by the odor 34 olfactory cues leads to avoidance of food contaminated by diacetyl and context-dependent 35 behavioral decision to avoid benzaldehyde only if there is an alternative, food-indicative odor. 36 Conclusions 37 Our findings reveal a regulatory link between physiological stress responses and learned 38 behavior which facilitates self-protection in real and anticipated stresses. The potential 39 conservation of this somato-neuronal connection might have relevance in maladaptive avoidant 40 human behaviors.41 3 Background 42Adequate, coordinated responses of multicellular organisms are key to adapt to and 43 overcome fundamental alterations of the environment (1-3). These responses originate from 44 intracellular molecular defenses, such as the oxidative, xenobiotic, metabolic and proteotoxic 45 stress responses, which guard homeostasis and confer cytoprotection against the respective 46 stresses, promoting physiological adaptation, fitness and longevity at the organismal level (4). 47Adaptation also involve complex behavioral responses orchestrated by the neuroendocrine 48 system (5-7). For instance, sensory cues representing danger evoke aversive behavior as a result 49 of perception of multiple sensory stimuli, neuronal processing and decision making both in 50 humans and in other species (8-10). In some cases, the neural impulse of perceived danger is 51 so intense that the organism decides to avoid co-occurring cues representing life-sustaining 52 qualities such as food (6, 11). Besides external sensory cues, decision making is modulated by 53 neural context like arousal, motivation, and reward (12, 13). Importantly, behavioral decisions 54 are also influenced by sensory cues that evoke associative memories of past events (14). 55Moreover, exaggerated, inadequate avoidant behavior is characteristic to human anxiety 56 disorders such as phobias (11)...

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supporting

confidence: 71%

Toxic stress-specific cytoprotective responses regulate learned behavioral decisions inC. elegans

Hajdú

Gecse

Taisz

et al. 2020

Preprint

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“…The consensus of the past two decades holds that ‘core affect’, considered necessary but insufficient for emotion, is composed of valence plus arousal (physiological activation, intensity) [12,15], roughly conceived as two, independent bipolar dimensions (valence = positive/negative; arousal = high/low). While research into valence during that period increasingly admitted non-mammalian models, including insects [16], worms [17] and other invertebrates [18], to date aneural systems (e.g. plants, microbes and some animals) have not figured in any aspect of affective research.…”

Section: Introduction: the Problem With Affectmentioning

confidence: 99%

Valuing what happens: a biogenic approach to valence and (potentially) affect

Lyon

Kuchling

2021

Phil. Trans. R. Soc. B

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Valence is half of the pair of properties that constitute core affect, the foundation of emotion. But what is valence, and where is it found in the natural world? Currently, this question cannot be answered. The idea that emotion is the body's way of driving the organism to secure its survival, thriving and reproduction runs like a leitmotif from the pathfinding work of Antonio Damasio through four book-length neuroscientific accounts of emotion recently published by the field's leading practitioners. Yet while Damasio concluded 20 years ago that the homeostasis–affect linkage is rooted in unicellular life, no agreement exists about whether even non-human animals with brains experience emotions. Simple neural animals—those less brainy than bees, fruit flies and other charismatic invertebrates—are not even on the radar of contemporary affective research, to say nothing of aneural organisms. This near-sightedness has effectively denied the most productive method available for getting a grip on highly complex biological processes to a scientific domain whose importance for understanding biological decision-making cannot be underestimated. Valence arguably is the fulcrum around which the dance of life revolves. Without the ability to discriminate advantage from harm, life very quickly comes to an end. In this paper, we review the concept of valence, where it came from, the work it does in current leading theories of emotion, and some of the odd features revealed via experiment. We present a biologically grounded framework for investigating valence in any organism and sketch a preliminary pathway to a computational model. This article is part of the theme issue ‘Basal cognition: conceptual tools and the view from the single cell’.

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“…The border and the texture of a bacterial lawn may also generate mechanical stimulation to moving worms. These bacteriaderived sensory cues act in a combinatorial manner to elicit behavioral responses in C. elegans [ (Bargmann, Hartwieg, & Horvitz, 1993;Brandt & Ringstad, 2015;Bretscher et al, 2008;Calhoun et al, 2015;Cheung et al, 2005;Flavell et al, 2013;Kim & Flavell, 2020;Gramstrup Petersen et al, 2013;Gray et al, 2004;Ha et al, 2010;Hallem et al, 2011;Hao et al, 2018;Harris et al, 2019;Meisel, Panda, Mahanti, Schroeder, & Kim, 2014;Ooi & Prahlad, 2017;Pradel et al, 2007;Reddy et al, 2011;Rhoades et al, 2019;Sawin, Ranganathan, & Horvitz, 2000;Tran et al, 2017) and the references therein]. The diversity of the sensory cues is consistent with multiple signaling pathways that are identified to mediate bacteria-worm interactions.…”

Section: Experimental Power Of C Elegans Facilitates Dissection Of Pmentioning

confidence: 73%

What can a worm learn in a bacteria-rich habitat?

Zhang

2020

Journal of Neurogenetics

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With a nervous system that has only a few hundred neurons, Caenorhabditis elegans was initially not regarded as a model for studies on learning. However, the collective effort of the C. elegans field in the past several decades has shown that the worm displays plasticity in its behavioral response to a wide range of sensory cues in the environment. As a bacteria-feeding worm, C. elegans is highly adaptive to the bacteria enriched in its habitat, especially those that are pathogenic and pose a threat to survival. It uses several common forms of behavioral plasticity that last for different amounts of time, including imprinting and adult-stage associative learning, to modulate its interactions with pathogenic bacteria. Probing the molecular, cellular and circuit mechanisms underlying these forms of experience-dependent plasticity has identified signaling pathways and regulatory insights that are conserved in more complex animals.

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Molecular and cellular modulators for multisensory integration in C. elegans

Cited by 24 publications

References 114 publications

Toxic stress-specific cytoprotective responses regulate learned behavioral decisions inC. elegans

Toxic stress-specific cytoprotective responses regulate learned behavioral decisions inC. elegans

Valuing what happens: a biogenic approach to valence and (potentially) affect

What can a worm learn in a bacteria-rich habitat?

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