Regional and cell-type-specific afferent and efferent projections of the mouse claustrum

Wang, Quanxin; Wang, Yun; Kuo, Hsien-Chi; Xie, Peng; Kuang, Xiuli; Hirokawa, Karla E.; Naeemi, Maitham; Yao, Shenqin; Mallory, Matt; Ouellette, Ben; Lesnar, Phil; Li, Yaoyao; Ye, Min; Chen, Chao; Xiong, Wei; Ahmadinia, Leila; El-Hifnawi, Laila; Çetin, Ali; Sorensen, Staci A.; Harris, Julie A.; Zeng, Hongkui; Koch, Christof

doi:10.1016/j.celrep.2023.112118

Cited by 26 publications

(35 citation statements)

References 97 publications

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“…While the latter is not easily identified with classical histological stains in the mouse brain, it has been reported that the claustrum is surrounded by densely myelinated fibers ( Wang et al. 2017 , 2022 ; Grimstvedt et al. 2022 ).…”

Section: Introductionmentioning

confidence: 98%

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Temporal origin of mouse claustrum and development of its cortical projections

et al. 2022

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The claustrum is known for its extensive connectivity with many other forebrain regions, but its elongated shape and deep location have made further study difficult. We have sought to understand when mouse claustrum neurons are born, where they are located in developing brains, and when they develop their widespread connections to the cortex. We established that a well-characterized parvalbumin plexus, which identifies the claustrum in adults, is only present from postnatal day (P) 21. A myeloarchitectonic outline of the claustrum can be derived from a triangular fiber arrangement from P15. A dense patch of Nurr1+ cells is present at its core and is already evident at birth. Bromodeoxyuridine birth dating of forebrain progenitors reveals that the majority of claustrum neurons are born during a narrow time window centered on embryonic day 12.5, which is later than the adjacent subplate and endopiriform nucleus. Retrograde tracing revealed that claustrum projections to anterior cingulate (ACA) and retrosplenial cortex (RSP) follow distinct developmental trajectories. Claustrum–ACA connectivity matures rapidly and reaches adult-like innervation density by P10, whereas claustrum–RSP innervation emerges later over a protracted time window. This work establishes the timeline of claustrum development and provides a framework for understanding how the claustrum is built and develops its unique connectivity.

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Section: Introductionmentioning

confidence: 98%

“…2018 ), targeting different laminae in different areas ( Wang et al. 2017 , 2022 ). It has strong reciprocal connections with prefrontal and cingulate cortex as well as temporal and retrohippocampal areas ( Carman et al.…”

Section: Introductionmentioning

confidence: 99%

Temporal origin of mouse claustrum and development of its cortical projections

et al. 2022

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“…Borders for the rodent CLCX are difficult to define, and the use of various methods to do so has resulted in substantial variation among current delineation schemes (Bruguier et al, 2020;Dillingham et al, 2019;Fang et al, 2021;Smith et al, 2019;Wang et al, 2023). We (Alcantara et al, 1993;Hof et al, 1999;Tremblay et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

A multifaceted architectural framework of the mouse claustrum complex

Grimstvedt,

Shelton,

Hoerder‐Suabedissen

et al. 2023

J of Comparative Neurology

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Accurate anatomical characterizations are necessary to investigate neural circuitry on a fine scale, but for the rodent claustrum complex (CLCX), this has yet to be fully accomplished. The CLCX is generally considered to comprise two major subdivisions, the claustrum (CL) and the dorsal endopiriform nucleus (DEn), but regional boundaries to these areas are debated. To address this, we conducted a multifaceted analysis of fiber‐ and cytoarchitecture, genetic marker expression, and connectivity using mice of both sexes, to create a comprehensive guide for identifying and delineating borders to CLCX, including an online reference atlas. Our data indicated four distinct subregions within CLCX, subdividing both CL and DEn into two. Additionally, we conducted brain‐wide tracing of inputs to CLCX using a transgenic mouse line. Immunohistochemical staining against myelin basic protein (MBP), parvalbumin (PV), and calbindin (CB) revealed intricate fiber‐architectural patterns enabling precise delineations of CLCX and its subregions. Myelinated fibers were abundant dorsally in CL but absent ventrally, whereas PV expressing fibers occupied the entire CL. CB staining revealed a central gap within CL, also visible anterior to the striatum. The Nr2f2, Npsr1, and Cplx3 genes expressed specifically within different subregions of the CLCX, and Rprm helped delineate the CL‐insular border. Furthermore, cells in CL projecting to the retrosplenial cortex were located within the myelin sparse area. By combining own experimental data with digitally available datasets of gene expression and input connectivity, we could demonstrate that the proposed delineation scheme allows anchoring of datasets from different origins to a common reference framework.

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“…Both female and male mice (3 to 6 months old) were used in experiments. B6;129S- Slc17a8 tm1.1(cre)Hze /J (stock number: 028534, Jackson Laboratories) mice were used for studying the effect of optogenetic and chemogenetic activation ( 26 , 67 , 68 ). B6;129S- Slc17a8 tm1.1(cre)Hze /J mice were crossed with C57BL/6J (stock number: 000664, Jackson Laboratories) for breeding.…”

Section: Methodsmentioning

confidence: 99%

Sex-specific modulation of the medial prefrontal cortex by glutamatergic median raphe neurons

Collins,

Stinson,

Himes

et al. 2023

Sci. Adv.

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A substantial proportion of raphe neurons are glutamatergic. However, little is known about how these glutamatergic neurons modulate the forebrain. We investigated how glutamatergic median raphe nucleus (MRN) input modulates the medial prefrontal cortex (mPFC), a critical component of fear circuitry. We show that vesicular glutamate transporter 3 (VGLUT3)–expressing MRN neurons activate VGLUT3- and somatostatin-expressing neurons in the mPFC. Consistent with this modulation of mPFC GABAergic neurons, activation of MRN (VGLUT3) neurons enhances GABAergic transmission in mPFC pyramidal neurons and attenuates fear memory in female but not male mice. Serotonin plays a key role in MRN (VGLUT3) neuron–mediated GABAergic plasticity in the mPFC. In agreement with these female-specific effects, we observed sex differences in glutamatergic transmission onto MRN (VGLUT3) neurons and in mPFC (VGLUT3) neuron–mediated dual release of glutamate and GABA. Our results demonstrate a cell type–specific modulation of the mPFC by MRN (VGLUT3) neurons and reveal a sex-specific role of this neuromodulation in mPFC synaptic plasticity.

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Regional and cell-type-specific afferent and efferent projections of the mouse claustrum

Cited by 26 publications

References 97 publications

Temporal origin of mouse claustrum and development of its cortical projections

Temporal origin of mouse claustrum and development of its cortical projections

A multifaceted architectural framework of the mouse claustrum complex

Sex-specific modulation of the medial prefrontal cortex by glutamatergic median raphe neurons

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