Cortical hierarchy governs rat claustrocortical circuit organization

White, Margaret A.; Cody, Patrick A.; Bubser, Michael; Wang, Huidong; Deutch, Ariel Y.; Mathur, Brian N.

doi:10.1002/cne.23970

Cited by 71 publications

(118 citation statements)

References 70 publications

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“…The output from the claustrum to the cortex has also been demonstrated to portray a dorsoventral organization in the rat (Sadowski et al, ), with a dorsal sensorimotor zone and a ventral visuoauditory zone. In contrast, a recent study in rats found that claustral neurons projecting to different sensory cortices localized to discrete zones, but a topographical organization could not be discerned (White et al, ).…”

mentioning

confidence: 90%

Mapping synaptic cortico‐claustral connectivity in the mouse

Atlan

Terem

Peretz-Rivlin

et al. 2016

J of Comparative Neurology

100

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The claustrum is an intriguing brain structure, featuring the highest connectivity per regional volume in the brain. It is a thin and elongated structure enclosed between the striatum and the insular cortex, with widespread reciprocal connections with the sensory modalities and prefrontal cortices. Retinotopic and somatotopic organizations have been described in the claustrum, and anatomical studies in cats, monkeys, and rats have demonstrated topographic organization of cortico-claustral connections. In this study we mapped the projections from cortical modalities (visual, auditory, somatosensory, motor, and olfactory), and prefrontal regions (anterior cingulate cortex and orbitofrontal cortex) to the claustrum in mice. Utilizing expression of a virally encoded synaptic anterograde tracer, AAV-SynaptoTag, followed by 3D reconstruction of the cortical projections, we performed a comprehensive study of the organization of these projections within the mouse claustrum. Our results clearly demonstrate a dorsoventral laminar organization of projections from the sensory cortices to the claustrum, whereas frontal inputs are more extensive and overlap with the inputs from the sensory cortices. In addition, we find evidence supporting a core/shell organization of the claustrum. We propose that the overlap between the frontal inputs and the inputs from the sensory modalities may underlie executive regulation of the communication between the claustrum and the cortical modalities. J. Comp. Neurol. 525:1381-1402, 2017. © 2016 Wiley Periodicals, Inc.

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mentioning

confidence: 90%

Mapping synaptic cortico‐claustral connectivity in the mouse

Atlan

Terem

Peretz-Rivlin

et al. 2016

J of Comparative Neurology

100

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“…It is known that the claustrum is highly interconnected with many areas of cortex (Mathur, 2014; Crick and Koch, 2005; Torgerson et al, 2015; Mathur et al, 2009), including prefrontal, parietal, and visual cortices in monkey (Druga et al, 1990; Pearson et al, 1982; Reser et al, 2014; Riche and Lanoir, 1978; Tanné-Gariépy et al, 2002; Gattass et al, 2014; Ungerleider et al, 1984), as well as prelimbic and cingulate cortices of the rat (White et al, 2017; Wang et al, 2017; Atlan et al, 2017; Smith and Alloway, 2010; Smith et al, 2012). However, it is unknown whether claustrum mediates top-down or bottom-up information flow (Mathur, 2014), sits atop the information processing hierarchy to bind sensory information for conscious perception (Crick and Koch, 2005), or exists solely as a satellite processer for cortices (Olson and Graybiel, 1980).…”

Section: Introductionmentioning

confidence: 99%

“…However, it is unknown whether claustrum mediates top-down or bottom-up information flow (Mathur, 2014), sits atop the information processing hierarchy to bind sensory information for conscious perception (Crick and Koch, 2005), or exists solely as a satellite processer for cortices (Olson and Graybiel, 1980). Based on recent work showing that the rat claustrum receives a dense innervation from the anterior cingulate cortex (ACC; White et al, 2017), an area implicated in top-down attention (Zhang et al, 2014, 2016), we hypothesize that the claustrum is positioned to receive top-down input for cognitive control (Mathur, 2014). Testing this, we found that ACC input to the mouse claustrum encodes an anticipatory top-down signal that is proportional to task load and required for optimal performance accuracy.…”

Section: Introductionmentioning

confidence: 99%

Anterior Cingulate Cortex Input to the Claustrum Is Required for Top-Down Action Control

et al. 2018

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SUMMARY Cognitive abilities, such as volitional attention, operate under top-down, executive frontal cortical control of hierarchically lower structures. The circuit mechanisms underlying this process are unresolved. The claustrum possesses interconnectivity with many cortical areas and, thus, is hypothesized to orchestrate the cortical mantle for top-down control. Whether the claustrum receives top-down input and how this input may be processed by the claustrum have yet to be formally tested, however. We reveal that a rich anterior cingulate cortex (ACC) input to the claustrum encodes a preparatory top-down information signal on a five-choice response assay that is necessary for optimal task performance. We further show that ACC input monosynaptically targets claustrum inhibitory interneurons and spiny glutamatergic projection neurons, the latter of which amplify ACC input in a manner that is powerfully constrained by claustrum inhibitory microcircuitry. These results demonstrate ACC input to the claustrum is critical for top-down control guiding action.

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“…The claustrum is anatomically characterized by widespread connectivity with cortex (Crick and Koch 2005; Mathur 2014). Executive cortices such as the anterior cingulate cortex (ACC) are heavily interconnected with claustrum (Smith and Alloway 2010; White et al 2017; Wang et al 2017; Atlan et al 2017). In addition, activation of afferents from ACC, but not sensory cortices, drives action potential firing of claustrum spiny projection neurons (White et al 2018).…”

Section: Introductionmentioning

confidence: 99%

Frontal cortical control of posterior sensory and association cortices through the claustrum

White

Mathur

2018

Brain Struct Funct

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The claustrum is a telencephalic gray matter nucleus that is richly interconnected with the neocortex. This structure subserves top-down executive functions that require frontal cortical control of posterior cortical regions. However, functional anatomical support for the claustrum allowing for long-range intercortical communication is lacking. To test this, we performed a channelrhodopsin-assisted long-circuit mapping strategy in mouse brain slices. We find that anterior cingulate cortex input to the claustrum is transiently amplified by claustrum neurons that, in turn, project to parietal association cortex or to primary and secondary visual cortices. Additionally, we observe that claustrum drive of cortical neurons in parietal association cortex is layer-specific, eliciting action potential generation briefly in layers II/III, IV, and VI but not V. These data are the first to provide a functional anatomical substrate through claustrum that may underlie top-down functions, such as executive attention or working memory, providing critical insight to this most interconnected and enigmatic nucleus.

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Cortical hierarchy governs rat claustrocortical circuit organization

Cited by 71 publications

References 70 publications

Mapping synaptic cortico‐claustral connectivity in the mouse

Mapping synaptic cortico‐claustral connectivity in the mouse

Anterior Cingulate Cortex Input to the Claustrum Is Required for Top-Down Action Control

Frontal cortical control of posterior sensory and association cortices through the claustrum

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