Dataset Information

Neural activity in the mouse claustrum in a cross-modal sensory selection task.

ABSTRACT: The claustrum, a subcortical nucleus forming extensive connections with the neocortex, has been implicated in sensory selection. Sensory-evoked claustrum activity is thought to modulate the neocortex's context-dependent response to sensory input. Recording from claustrum neurons while mice performed a tactile-visual sensory-selection task, we found that neurons in the anterior claustrum, including putative optotagged claustrocortical neurons projecting to the primary somatosensory cortex (S1), were rarely modulated by sensory input. Rather, they exhibited different types of direction-tuned motor responses. Furthermore, we found that claustrum neurons encoded upcoming movement during intertrial intervals and that pairs of claustrum neurons exhibiting synchronous firing were enriched for pairs preferring contralateral lick directions, suggesting that the activity of specific ensembles of similarly tuned claustrum neurons may modulate cortical activity. Chemogenetic inhibition of claustrocortical neurons decreased lick responses to inappropriate sensory stimuli. Altogether, our data indicate that the claustrum is integrated into higher-order premotor circuits recently implicated in decision-making.

SUBMITTER: Chevee M

PROVIDER: S-EPMC8829966 | biostudies-literature | 2022 Feb

REPOSITORIES: biostudies-literature

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Neural activity in the mouse claustrum in a cross-modal sensory selection task.

Chevée Maxime M Finkel Eric A EA Kim Su-Jeong SJ O'Connor Daniel H DH Brown Solange P SP

Neuron 20211203 3

The claustrum, a subcortical nucleus forming extensive connections with the neocortex, has been implicated in sensory selection. Sensory-evoked claustrum activity is thought to modulate the neocortex's context-dependent response to sensory input. Recording from claustrum neurons while mice performed a tactile-visual sensory-selection task, we found that neurons in the anterior claustrum, including putative optotagged claustrocortical neurons projecting to the primary somatosensory cortex (S1), w ...[more]

PMID: 34863367

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Project description:Sensory loss induces cross-modal plasticity, often resulting in altered performance in remaining sensory modalities. Whereas much is known about the macroscopic mechanisms underlying cross-modal plasticity, only scant information exists about its cellular and molecular underpinnings. We found that Caenorhabditis elegans nematodes deprived of a sense of body touch exhibit various changes in behavior, associated with other unimpaired senses. We focused on one such behavioral alteration, enhanced odor sensation, and sought to reveal the neuronal and molecular mechanisms that translate mechanosensory loss into improved olfactory acuity. To this end, we analyzed in mechanosensory mutants food-dependent locomotion patterns that are associated with olfactory responses and found changes that are consistent with enhanced olfaction. The altered locomotion could be reversed in adults by optogenetic stimulation of the touch receptor (mechanosensory) neurons. Furthermore, we revealed that the enhanced odor response is related to a strengthening of inhibitory AWC→AIY synaptic transmission in the olfactory circuit. Consistently, inserting in this circuit an engineered electrical synapse that diminishes AWC inhibition of AIY counteracted the locomotion changes in touch-deficient mutants. We found that this cross-modal signaling between the mechanosensory and olfactory circuits is mediated by neuropeptides, one of which we identified as FLP-20. Our results indicate that under normal function, ongoing touch receptor neuron activation evokes FLP-20 release, suppressing synaptic communication and thus dampening odor sensation. In contrast, in the absence of mechanosensory input, FLP-20 signaling is reduced, synaptic suppression is released, and this enables enhanced olfactory acuity; these changes are long lasting and do not represent ongoing modulation, as revealed by optogenetic experiments. Our work adds to a growing literature on the roles of neuropeptides in cross-modal signaling, by showing how activity-dependent neuropeptide signaling leads to specific cross-modal plastic changes in neural circuit connectivity, enhancing sensory performance.

Project description:Joint attention refers to the coordinated attention between social partners to an object of shared interest, usually involving shared gaze toward the object. In the laboratory, however, joint attention is often investigated using computerized gaze cueing tasks that do not allow shared gaze. Instead, these computerized tasks require the participant to maintain fixation on the virtual partner's face, while the partner gazes to the left or right. Here we designed a modified gaze cueing task that better simulates a natural joint attention episode by allowing shared gaze, while still maintaining tight experimental control. In our computerized task the participant's gaze and the gaze of a virtual partner were manipulated independently, resulting in shared or unshared gaze. Following each gaze shift of the virtual partner a touch stimulus was delivered on one of the cheeks of the participant. We analyzed behavioral and neural (electro-encephalography) responses to the touch. Faster reaction-times and stronger lateralization of alpha power were observed when the touched cheek was in a jointly attended hemispace compared with a singly attended or unattended hemispace. Importantly, these effects were unique to joint attention and could not be explained as the additive effects of own gaze and gaze cue direction. Underlining its social nature, we found that the behavioral effect was absent when we repeated our experiment with nonsocial cues (arrows) instead of gaze cues. Furthermore, when we compared trustworthy with untrustworthy virtual partners (trustworthiness judgements based on facial appearance) we found the effect only for trustworthy and not for untrustworthy virtual partners. We conclude that joint attention based on shared gaze influences attentional orienting such that cross-modal sensory processing at the jointly attended location is facilitated, particularly when the partner is trustworthy. This indicates that social interactions and trustworthiness judgements affect cortical and behavioral responses to sensory information.

Dataset Information

Neural activity in the mouse claustrum in a cross-modal sensory selection task.

Publications

Neural activity in the mouse claustrum in a cross-modal sensory selection task.

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