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

Abstract

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.

Input–output organization of the mouse claustrum

“…To directly test this, we injected equal volumes of CTB conjugated with Alexa 647, 488, or 555 into the ACA, V1, and RSP, respectively, in the same animal to retrogradely label CLA neurons that project to each of these regions (Figure a, Table ). The ACA was selected since retrograde tracer injections here have been shown to strongly label CLA neurons throughout the entire length of the structure, and the distribution of these cells has been confirmed to fall within the boundaries of the CLA as defined by dense parvalbumin (PV) immunoreactivity and Gng2 expression (Mathur et al, ; White et al, , ). Similarly, V1 was selected as it has been shown to receive CLA input, however, some reports suggest that sensory cortical regions may receive segregated inputs from discrete parts of the CLA (Kitanishi & Matsuo, ; White et al, ).…”

Top‐down and bottom‐up control of stress‐coping

“…Topological distinctions can be made between prelimbic, infralimbic and anterior cingulate cortices, or even more generalised terms such as the ventromedial and dorsomedial prefrontal cortex. [211][212][213] In general, it appears that, although the mPFC exhibits a number of generalised core processes, such as having its neural ensembles exert top-down influence on lower brain regions, the part that is activated depends on the type of behaviour. 206 Previous work indicates that both the prelimbic and infralimbic cortex are important for anticipatory behaviour.…”

The relationship between the claustrum and endopiriform nucleus: A perspective towards consensus on cross‐species homology

“…The CLA-En boundary in primate brains is somewhat loosely defined. Using only the marmoset as an example, there are substantial regions of uncertainty which could lead to confusion and may hamper experimental progress by making it difficult to selectively target CLA versus En for injection of viral constructs, as have been employed in rodent studies (White et al, 2018). In the marmoset stereotaxic atlas of Paxinos, Charles, et al (2012a) and Paxinos, Watson, et al (2012b), the En is identified on the basis of increased cell density in the Nissl- In both New World (Reser et al, 2014(Reser et al, , 2017 and Old World monkey species (Baizer, 2014), the CLA complex is particularly well resolved by staining for myelin, which is present at much lower levels in the CLA than in the adjacent white matter tracts.…”