Influence of claustrum on cortex varies by area, layer, and cell type

McBride, Ethan G; Gandhi, Saurabh R.; Kuyat, Jacqulyn R; Ollerenshaw, Douglas R.; Arkhipov, Anton; Koch, Christof; Olsen, Shawn R.

doi:10.1016/j.neuron.2022.10.026

Cited by 30 publications

(32 citation statements)

References 49 publications

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“…Our in vivo studies show broad activation with 5 ms light pulses of CLA neurons expressing ChR2 driven by the CaMKIIa promoter produce, in the LFP band, an overall small and brief excitation follow by a potent inhibition in the ACC. This type of response was observed both in layer 2/3 and layer 5/6 and suggested, as previously reported 13, 18, 50 that CLA provides a “blanket of inhibition” to the ACC. However, LFP responses while easy to record, have proven notoriously difficult to interpret 69–71 .…”

Section: Discussionsupporting

confidence: 84%

“…CLA has been reported to exert either excitatory or an inhibitory effect on different cortical regions 1, 18 . There is anatomical and functional evidence showing that CLA outputs target both excitatory and inhibitory cells within cortical circuits 2, 10, 13 .…”

Section: Discussionmentioning

confidence: 99%

“…This could be due to the different effects of CLA input on different cortical areas. A recent study showed that activation of Esr2 population, a subgroup of CLA neurons driven by the CaMKIIa promoter, showed moderate inhibitory effect albeit their preference for FS and little impact in RS 18 . This raises the possibility that Esr2-expressing neurons may express their own target selectivity in cortex.…”

Section: Discussionmentioning

confidence: 99%

“…Functions implicated have included: awareness 37 , consciousness 38 , salience reporting 10,11,[39][40][41] , memory consolidation 42 , pain mediation 35,36 , attention [43][44][45] , regulation of cortical sleep waves [46][47][48][49][50] and impulse control 51 . Central to the different functions assumed for CLA is the robust connectivity with various cortical regions 1,11,21 , in particular with prefrontal regions such as the anterior cingulate cortex (ACC) 11,18,20,21 . Several studies have shown that despite being a glutamatergic excitatory projection, the impact of CLA on targeted cortical regions is largely inhibitory, mediated by synchronized activation of cortical GABAergic interneurons 13,42,43,50,[52][53][54][55][56] .…”

Section: Introductionmentioning

confidence: 99%

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Presynaptic and Postsynaptic Determinants of the Functional Connectivity Between the Claustrum and Anterior Cingulate Cortex

Martínez

Chia

Tokarska

et al. 2023

Preprint

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The claustrum (CLA) is a brain nucleus located between the insula and lateral striatum, implicated in a wide range of behaviors. Underpinning the different behavioral phenotypes is the connectivity between the claustrum and various cortical regions, including the anterior cingulate cortex (ACC). CLA projection neurons are glutamatergic neurons, however, the impact of CLA on its cortical targets has been shown in some studies to be inhibitory. Such inhibition is likely to arise from claustral activation of cortical interneurons, however, the intricate synaptic connectivity between different CLA and cortical cell types is not known. Here, we combine in vivo and ex vivo electrophysiology and optogenetics to reveal the functional organization of the CLA-ACC pathway according to the identity of its pre- and postsynaptic populations. Optogenetic stimulation of CLA neurons in awake mice resulted in multiphasic excitatory and inhibitory responses in ACC cells, which depended on the layer, cell type, and stimulated CLA population. Using ex vivo paired recordings in ACC, monosynaptic responses were recorded in pyramidal cells and different types of interneurons following photostimulation of CLA-ACC synaptic terminals. CLA axons formed monosynaptic connections in all ACC cortical layers, but the probability and strength of synaptic responses depended on the type of CLA projection, target layer in ACC, and the type of postsynaptic neuron. This intricate organization of the CLA-ACC pathway may explain the complex impact of CLA on ACC and other cortical regions, thus resolving some of the discrepancies in the field and shedding light on the functional role CLA plays in cortical function.

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Section: Discussionsupporting

confidence: 84%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Presynaptic and Postsynaptic Determinants of the Functional Connectivity Between the Claustrum and Anterior Cingulate Cortex

Martínez

Chia

Tokarska

et al. 2023

Preprint

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“…Images of the 100 µm coronal sections were aligned to the Allen Institute Common Coordinate Framework (CCFv3) following the process detailed by McBride et al (2022) and images from serial twophoton tomography were aligned to the CCFv3 following the process detailed by Oh et al (2014).…”

Section: Ex Vivo Imaging and Localization Of Electrodesmentioning

confidence: 99%

Cortico-thalamo-cortical interactions modulate electrically evoked EEG responses in mice

Claar

Rembado

Kuyat

et al. 2022

Preprint

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Perturbational complexity analysis predicts the presence of consciousness in humans by stimulating the brain with a brief pulse, recording cortical responses with electroencephalography (EEG), and measuring their spatiotemporal complexity. Measures reflecting perturbational complexity are low when consciousness vanishes in deep sleep, general anesthesia, or after widespread brain damage, and are high during wake, dreaming sleep and after recovery from brain injury. Here we examine the neural circuits underlying perturbational complexity in a mouse model by directly stimulating the cortex and recording high-density EEG, as well as spiking activity throughout the cortico-thalamo-cortical system with up to three Neuropixels probes, while subjects are awake or anesthetized via isoflurane. We find that when the mouse is awake, stimulation of deep cortical layers reliably evokes locally a brief pulse of excitation, followed by a bi-phasic sequence of a 120 ms profound off period and a rebound excitation. A similar pattern of spiking activity, some of which can be attributed to burst spiking, is seen in the connected thalamic nuclei. These spiking patterns are associated with a pronounced late component in the evoked EEG. We infer that cortico-thalamo-cortical interactions drive the long-lasting evoked EEG signals elicited by deep cortical stimulation during the awake state. The cortical and thalamic off period and rebound excitation, as well as the late component in the EEG, are reduced in running mice and are absent in animals anesthetized with isoflurane. This is also mirrored in the perturbational complexity indices computed during quiet wakefulness, running, and anesthetized states. Taken together, these results suggest that cortico-thalamo-cortical interactions contribute to ongoing activity in the conscious state that leads to highly complex global responses.

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The Claustrum Controls Motor Activity Through Anterior Cingulate Cortex Input and Local Circuit Synchronization in a Preparatory Manner

Kou,

Chen,

Abdurahman

et al. 2023

Neurosci. Bull.

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Influence of claustrum on cortex varies by area, layer, and cell type

Cited by 30 publications

References 49 publications

Presynaptic and Postsynaptic Determinants of the Functional Connectivity Between the Claustrum and Anterior Cingulate Cortex

Presynaptic and Postsynaptic Determinants of the Functional Connectivity Between the Claustrum and Anterior Cingulate Cortex

Cortico-thalamo-cortical interactions modulate electrically evoked EEG responses in mice

The Claustrum Controls Motor Activity Through Anterior Cingulate Cortex Input and Local Circuit Synchronization in a Preparatory Manner

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