Dataset Information

Coherent Multimodal Sensory Information Allows Switching between Gravitoinertial Contexts.

ABSTRACT: Whether the central nervous system is capable to switch between contexts critically depends on experimental details. Motor control studies regularly adopt robotic devices to perturb the dynamics of a certain task. Other approaches investigate motor control by altering the gravitoinertial context itself as in parabolic flights and human centrifuges. In contrast to conventional robotic experiments, where only the hand is perturbed, these gravitoinertial or immersive settings coherently plunge participants into new environments. However, radically different they are, perfect adaptation of motor responses are commonly reported. In object manipulation tasks, this translates into a good matching of the grasping force or grip force to the destabilizing load force. One possible bias in these protocols is the predictability of the forthcoming dynamics. Here we test whether the successful switching and adaptation processes observed in immersive environments are a consequence of the fact that participants can predict the perturbation schedule. We used a short arm human centrifuge to decouple the effects of space and time on the dynamics of an object manipulation task by adding an unnatural explicit position-dependent force. We created different dynamical contexts by asking 20 participants to move the object at three different paces. These contextual sessions were interleaved such that we could simulate concurrent learning. We assessed adaptation by measuring how grip force was adjusted to this unnatural load force. We found that the motor system can switch between new unusual dynamical contexts, as reported by surprisingly well-adjusted grip forces, and that this capacity is not a mere consequence of the ability to predict the time course of the upcoming dynamics. We posit that a coherent flow of multimodal sensory information born in a homogeneous milieu allows switching between dynamical contexts.

SUBMITTER: Barbiero M

PROVIDER: S-EPMC5425486 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Coherent Multimodal Sensory Information Allows Switching between Gravitoinertial Contexts.

Barbiero Marie M Rousseau Célia C Papaxanthis Charalambos C White Olivier O

Frontiers in physiology 20170511

Whether the central nervous system is capable to switch between contexts critically depends on experimental details. Motor control studies regularly adopt robotic devices to perturb the dynamics of a certain task. Other approaches investigate motor control by altering the gravitoinertial context itself as in parabolic flights and human centrifuges. In contrast to conventional robotic experiments, where only the hand is perturbed, these gravitoinertial or immersive settings coherently plunge part ...[more]

PMID: 28553233

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Project description:A ubiquitous feature of the nervous system is the processing of simultaneously arriving sensory inputs from different modalities. Yet, because of the difficulties of monitoring large populations of neurons with the single resolution required to determine their sensory responses, the cellular mechanisms of how populations of neurons encode different sensory modalities often remain enigmatic. We studied multimodal information encoding in a small sensorimotor system of the crustacean stomatogastric nervous system that drives rhythmic motor activity for the processing of food. This system is experimentally advantageous, as it produces a fictive behavioral output in vitro, and distinct sensory modalities can be selectively activated. It has the additional advantage that all sensory information is routed through a hub ganglion, the commissural ganglion, a structure with fewer than 220 neurons. Using optical imaging of a population of commissural neurons to track each individual neuron's response across sensory modalities, we provide evidence that multimodal information is encoded via a combinatorial code of recruited neurons. By selectively stimulating chemosensory and mechanosensory inputs that are functionally important for processing of food, we find that these two modalities were processed in a distributed network comprising the majority of commissural neurons imaged. In a total of 12 commissural ganglia, we show that 98% of all imaged neurons were involved in sensory processing, with the two modalities being processed by a highly overlapping set of neurons. Of these, 80% were multimodal, 18% were unimodal, and only 2% of the neurons did not respond to either modality. Differences between modalities were represented by the identities of the neurons participating in each sensory condition and by differences in response sign (excitation versus inhibition), with 46% changing their responses in the other modality. Consistent with the hypothesis that the commissural network encodes different sensory conditions in the combination of activated neurons, a new combination of excitation and inhibition was found when both pathways were activated simultaneously. The responses to this bimodal condition were distinct from either unimodal condition, and for 30% of the neurons, they were not predictive from the individual unimodal responses. Thus, in a sensorimotor network, different sensory modalities are encoded using a combinatorial code of neurons that are activated or inhibited. This provides motor networks with the ability to differentially respond to categorically different sensory conditions and may serve as a model to understand higher-level processing of multimodal information.

Dataset Information

Coherent Multimodal Sensory Information Allows Switching between Gravitoinertial Contexts.

Publications

Coherent Multimodal Sensory Information Allows Switching between Gravitoinertial Contexts.

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