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The mouse claustrum synaptically connects cortical network motifs.

ABSTRACT: Spatially distant areas of the cerebral cortex coordinate their activity into networks that are integral to cognitive processing. A common structural motif of cortical networks is co-activation of frontal and posterior cortical regions. The neural circuit mechanisms underlying such widespread inter-areal cortical coordination are unclear. Using a discovery based functional magnetic resonance imaging (fMRI) approach in mouse, we observe frontal and posterior cortical regions that demonstrate significant functional connectivity with the subcortical nucleus, the claustrum. Examining whether the claustrum synaptically supports such frontoposterior cortical network architecture, we observe cortico-claustro-cortical circuits reflecting the fMRI data: significant trans-claustral synaptic connectivity from frontal cortices to posteriorly lying sensory and sensory association cortices contralaterally. These data reveal discrete cortical pathways through the claustrum that are positioned to support cortical network motifs central to cognitive control functions and add to the canon of major extended cortico-subcortico-cortical systems in the mammalian brain.

SUBMITTER: Qadir H

PROVIDER: S-EPMC9838879 | biostudies-literature | 2022 Dec

REPOSITORIES: biostudies-literature

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The mouse claustrum synaptically connects cortical network motifs.

Qadir Houman H Stewart Brent W BW VanRyzin Jonathan W JW Wu Qiong Q Chen Shuo S Seminowicz David A DA Mathur Brian N BN

Cell reports 20221201 12

Spatially distant areas of the cerebral cortex coordinate their activity into networks that are integral to cognitive processing. A common structural motif of cortical networks is co-activation of frontal and posterior cortical regions. The neural circuit mechanisms underlying such widespread inter-areal cortical coordination are unclear. Using a discovery based functional magnetic resonance imaging (fMRI) approach in mouse, we observe frontal and posterior cortical regions that demonstrate sign ...[more]

PMID: 36543121

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Project description:The claustrum, a subcortical structure situated between the insular cortex and striatum, is reciprocally connected with almost all neocortical regions. Based on this connectivity, the claustrum has been postulated to integrate multisensory information and, in turn, coordinate widespread cortical activity. Although studies have identified how sensory information is mapped onto the claustrum, the function of individual topographically arranged claustro-cortical pathways has been little explored. Here, we investigated the organization and function of identified claustro-cortical pathways in mice using multiple anatomical and optogenetic techniques. Retrograde and anterograde tracing demonstrated that the density of anterior claustrum-to-cortical projection differs substantially depending on the target cortical areas. One of the major targets was the medial entorhinal cortex (MEC) and the MEC-projecting claustral neurons were largely segregated from the neurons projecting to primary cortices M1, S1, or V1. Exposure to a novel environment induced c-Fos expression in a substantial number of MEC-projecting claustral neurons and some M1/S1/V1-projecting claustral neurons. Optogenetic silencing of the MEC-projecting claustral neurons during contextual fear conditioning impaired later memory retrieval without affecting basal locomotor activity or anxiety-related behavior. These results suggest that the dense, anterior claustro-MEC pathway that is largely separated from other claustro-cortical pathways is activated by novel context and modulates the MEC function in contextual memory.Significance statementThe claustrum is a poorly understood subcortical structure reciprocally connected with widespread neocortical regions. We investigated the organization and function of identified claustro-cortical projections in mice using pathway-specific approaches. Anatomical tracing showed that the density of anterior claustrum-to-cortical projection is dependent on the target cortical areas and that the medial entorhinal cortex (MEC) is one of the major projection targets. Novel context exposure activated multiple claustro-cortical pathways and a large fraction of the activated neurons projected to the MEC. Optogenetic silencing of the claustro-MEC pathway during contextual fear learning suppressed subsequent memory retrieval. These results suggest that the dense claustro-MEC pathway is activated by novel context and modulates MEC function in contextual memory.

Dataset Information

The mouse claustrum synaptically connects cortical network motifs.

Publications

The mouse claustrum synaptically connects cortical network motifs.

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