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Natural sensory context drives diverse brain-wide activity during C. elegans mating.

ABSTRACT: Natural goal-directed behaviors often involve complex sequences of many stimulus-triggered components. Understanding how brain circuits organize such behaviors requires mapping the interactions between an animal, its environment, and its nervous system. Here, we use brain-wide neuronal imaging to study the full performance of mating by the C. elegans male. We show that as mating unfolds in a sequence of component behaviors, the brain operates similarly between instances of each component but distinctly between different components. When the full sensory and behavioral context is taken into account, unique roles emerge for each neuron. Functional correlations between neurons are not fixed but change with behavioral dynamics. From individual neurons to circuits, our study shows how diverse brain-wide dynamics emerge from the integration of sensory perception and motor actions in their natural context.

SUBMITTER: Susoy V

PROVIDER: S-EPMC8488019 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Natural sensory context drives diverse brain-wide activity during C. elegans mating.

Susoy Vladislav V Hung Wesley W Witvliet Daniel D Whitener Joshua E JE Wu Min M Park Core Francisco CF Graham Brett J BJ Zhen Mei M Venkatachalam Vivek V Samuel Aravinthan D T ADT

Cell 20210916 20

Natural goal-directed behaviors often involve complex sequences of many stimulus-triggered components. Understanding how brain circuits organize such behaviors requires mapping the interactions between an animal, its environment, and its nervous system. Here, we use brain-wide neuronal imaging to study the full performance of mating by the C. elegans male. We show that as mating unfolds in a sequence of component behaviors, the brain operates similarly between instances of each component but dis ...[more]

PMID: 34534446

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Project description:Many neurocognitive studies on the role of motor structures in action-language processing have implicitly adopted a "dictionary-like" framework within which lexical meaning is constructed on the basis of an invariant set of semantic features. The debate has thus been centered on the question of whether motor activation is an integral part of the lexical semantics (embodied theories) or the result of a post-lexical construction of a situation model (disembodied theories). However, research in psycholinguistics show that lexical semantic processing and context-dependent meaning construction are narrowly integrated. An understanding of the role of motor structures in action-language processing might thus be better achieved by focusing on the linguistic contexts under which such structures are recruited. Here, we therefore analyzed online modulations of grip force while subjects listened to target words embedded in different linguistic contexts. When the target word was a hand action verb and when the sentence focused on that action (John signs the contract) an early increase of grip force was observed. No comparable increase was detected when the same word occurred in a context that shifted the focus toward the agent's mental state (John wants to sign the contract). There mere presence of an action word is thus not sufficient to trigger motor activation. Moreover, when the linguistic context set up a strong expectation for a hand action, a grip force increase was observed even when the tested word was a pseudo-verb. The presence of a known action word is thus not required to trigger motor activation. Importantly, however, the same linguistic contexts that sufficed to trigger motor activation with pseudo-verbs failed to trigger motor activation when the target words were verbs with no motor action reference. Context is thus not by itself sufficient to supersede an "incompatible" word meaning. We argue that motor structure activation is part of a dynamic process that integrates the lexical meaning potential of a term and the context in the online construction of a situation model, which is a crucial process for fluent and efficient online language comprehension.

Dataset Information

Natural sensory context drives diverse brain-wide activity during C. elegans mating.

Publications

Natural sensory context drives diverse brain-wide activity during C. elegans mating.

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