Functional properties, topological organization and sexual dimorphism of claustrum neurons projecting to anterior cingulate cortex

Abstract

Objective: To define the physiological properties of neurons projecting from the claustrum to the anterior cingulate cortex (ACC). Design: To identify the claustrum in live slices, we used a transgenic mouse line that expresses yellow fluorescent protein (YFP)-tagged Volvox channelrhodopsin-1 at high levels within the claustrum. Claustrum cells projecting to the ACC were identified by retrograde labelling. Whole-cell patch-clamp recordings from labelled claustrum neurons were used to characterize the intrinsic electrical properties of these neurons. Cells were classified according to their intrinsic electrical properties, based on a previous classification scheme. Results: Labelled neurons were found in the claustrum but not the insular cortex. Four types of ACC-projecting neurons were identified based on action potential adaptation and waveform: strongly adapting (SA) cell types 2, 3 and 4, and moderately adapting (MA) cell type 2. Labelled cells were predominantly SA4 in the anterior (44%) and posterior (63%) claustrum, while MA2 predominated (77%) in the central claustrum. The male anterior claustrum showed a bias toward SA3 cells (53%) while the female anterior claustrum showed a bias toward SA3 cells (76%). Conclusions: There is ipsilateral dominance for ACC-projecting claustrum neurons, with the intrinsic properties of these neurons varying along the anterior-posterior axis. Sexual dimorphism was observed in ACC-projecting claustrum cells. Our results are consistent with the hypothesis that the claustrum serves as a link between the insular cortex and the ACC. ARTICLE HISTORY

The Claustrum is Involved in Cognitive Processes Related to the Classical Conditioning of Eyelid Responses in Behaving Rabbits

“…Even though rabbit CL is far easier to access, due to its significantly larger size (compared with mouse CL), its differential and dense connectivity (anti- and ortho-dromic) with MC, mPFC, and CC ( Carman et al. 1964 ; Crick and Koch 2005 ; Mathur 2014 ; Chia et al. 2017 ; Atlan et al.…”

A Role for the Claustrum in Salience Processing?

“…Beyond these classic neuroanatomical tracing approaches, more sophisticated viral tracing from CLA-specific transgenic mice and other approaches have confirmed all of these connections (Chia et al, 2017; Wang et al, 2017; Atlan et al, 2018; Zingg et al, 2018). Furthermore, these studies indicate that there is some reciprocal connectivity between CLA and agranular insular cortex, making it more difficult to interpret differences in functional connectivity between CLA and insula given that these structures appear to have direct connections.…”

“…Though the function of the CLA remains largely unknown, recent studies indicate that the CLA plays a role in salience detection, attentional processing, and possibly cognition (Remedios et al, 2010, 2014; Goll et al, 2015; Atlan et al, 2018; Jackson et al, 2018), particularly via its connections with Cg cortex (Chia et al, 2017; White and Mathur, 2018; White et al, 2018). Most notably, electrophysiology recordings in the CLA of non-human primates lead the investigators to propose that “the claustrum detects the occurrence of novel or salient sensory events” (Remedios et al, 2014).…”

Changing the Cortical Conductor’s Tempo: Neuromodulation of the Claustrum

“…The claustrum is thought to participate primarily in two ICNs: the salience network (SAN) and the default mode network (DMN; Figure 3 ; Smith et al, 2019b ). Specifically, the claustrum serves as a link between the anterior insula and the ACC (Wang et al, 2017 ; Chia et al, 2017 , 2020 ; Qadir et al, 2018 ; Zingg et al, 2018 ; Krimmel et al, 2019 ; Rodríguez-Vidal et al, 2019 ; Smith et al, 2019a ), two very prominent components of the SAN (Menon and Uddin, 2010 ). As the claustrum also is connected within the DMN, it is ideally positioned to process sensory-limbic information and use this information to toggle in and out of the DMN like a switch; the claustrum is linked to the recruitment of the SAN and disengagement of the DMN (Krimmel et al, 2019 ; Rodríguez-Vidal et al, 2019 ; Smith et al, 2019b ).…”

“…Current evidence points to the claustrum being involved in higher cognition. Hypothesized functions of the claustrum revolve around four main themes: consciousness (Crick and Koch, 2005 ; Koubeissi et al, 2014 ; Chau et al, 2015 ; Yin et al, 2016 ; Bickel and Parvizi, 2019 ), attention and salience (Mathur, 2014 ; Chia et al, 2017 ; Atlan et al, 2018 ; Smith et al, 2019b ), learning and memory (Grasby and Talk, 2013 ; Jankowski and O’Mara, 2015 ; Renouard et al, 2015 ; Liu et al, 2019 ; O’Mara and Aggleton, 2019 ; Reus-García et al, 2020 ), and sleep (Renouard et al, 2015 ; Narikiyo et al, 2020 ; Norimoto et al, 2020 ).…”