Cortical hierarchy governs rat claustrocortical circuit organization

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The claustrum is a prominent telencephalic structure lying medial to the insula and lateral to the striatum. It is reciprocally connected with many cortical areas (Riche and Lanoir, 1978; Sherk, 1986; Park et al., 2012; Torgerson et al., 2015), and this anatomical configuration has inspired two major functional hypotheses. The first hypothesis is that the claustrum functions as a multisensory integrator (Ettlinger and Wilson, 1990; Hadjikhani and Roland, 1998; Crick and Koch, 2005), whereas the second hypothesis states that the claustrum is a relay for cortical information subserving attentional allocation (Mathur, 2008; Goll et al., 2015). These two hypotheses predict two different patterns of claustrocortical connectivity. For instance, the sensory integration hypothesis, which proposes that the claustrum integrates sensory information to form conscious percepts, predicts strong connectivity between sensory and motor cortices and the claustrum. In contrast, the attentional allocation hypothesis, which proposes that the claustrum transmits salient information to/from sensory association and executive cortices necessary for attention allocation, predicts that areas important for attention, such as the cingulate cortices, would be preferentially connected with the claustrum.
Our current understanding of claustrocortical circuits is based on an accumulation of evidence from studies that were conducted in different species and that targeted only one of a few cortical sites in nonhuman primates, cats, or rats (Sanides and Buchholtz, 1979; Olson and Graybiel, 1980; Irvine and Brugge, 1980; Levay and Sherk, 1981; Macchi et al., 1981; Pearson et al., 1982; Macchi et al., 1983; Shameem et al., 1984; Carey and Neal, 1985; Minciacchi et al., 1985; Adinolfi and Levine, 1986; Sloniewski et al., 1986; Druga et al. 1990; Baizer et al., 1997; Sadowski et al., 1997; Reser et al., 2014). Thus, an assessment of how the claustrum differentially connects with various cortical areas in a single species is required. Moreover, previous studies of claustral efferents have used overly inclusive definitions of the borders of the claustrum that led to the false assignment of retrogradely labeled cells that actually originate from insular cortex to the claustrum, thus limiting the interpretation of these studies (see Van de Werd and Uylings, 2008; Mathur et al., 2009). To address these issues, we have systematically examined the intraclaustral localization of cells projecting to cortical areas spanning the entire cortical hierarchy from primary sensory subdivisions to frontal cortical sites in the rat and defined claustral borders based on parvalbumin (PV) immunoreactivity, which is isomorphic with the expression pattern of the rodent claustral marker GNG2 (Mathur et al., 2009). The GNG2‐based definition of the claustrum is corroborated by publicly available mouse gene expression data from the Allen Institute for Brain Science and human GNG2 protein expression (Lein et al., 2007; Pirone et al., 2012; Allen Mouse Brain Atlas,
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