In situ hybridization analyses of claustrum‐enriched genes in marmosets

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Application of molecular biological techniques to neuroanatomy has greatly expanded our notion of what “structure” is. Quite often, anatomical structures or cell types, which are difficult to identify accurately using morphology alone, exhibit discrete gene expression profiles. Whereas gene expression during development is directly associated with cell fate determination (Greig et al., 2013; Kepecs and Fishell, 2014), adult gene expression reflects the need of certain gene products for proper functioning of that cell. For example, the glutamate decarboxylase 67 (GAD67) gene is specifically expressed in the inhibitory neurons because it is required for producing γ‐aminobutyric acid (GABA). The diversity of gene expression revealed by genome‐wide screening (Gong et al., 2003; Lein et al., 2007) thus illustrates the complexity of the molecular machinery that lays the basis for the functioning of the various cell types that constitute the adult brain.
The claustrum and the adjacent endopiriform nucleus sit between the basal ganglia and the cerebral cortex. Their developmental origin and function has been a matter of debate and still remains enigmatic (Crick and Koch, 2005). Interestingly, a panel of genes is specifically enriched in the claustrum in adult rodent and macaque monkeys (Arimatsu et al., 1992; Miyashita et al., 2005; Mathur et al., 2009; Watakabe et al., 2014). The Allen Mouse Brain Atlas (Gong et al., 2003; Lein et al., 2007) now lists 44 genes categorized into “claustrum” by the “Fine Structure Search.” The existence of such “claustrum‐enriched genes” strongly suggests that the cell type that constitutes this enigmatic structure performs some unique functions that are quite different from the adjacent striatal or cortical cells.
I studied the expression patterns of seven “claustrum‐enriched genes” by in situ histochemistry (ISH) analyses using marmosets. This small‐bodied primate has many attractive features as an experimental animal and is a promising primate model for neuroscience research (Tokuno et al., 2015). In an evolutionary context, the marmoset is a New World monkey that separated from Old World monkeys, such as macaques, about 35–40 million years ago (Mitchell and Leopold, 2015). Considering the divergence of gene expression profiles among mouse, macaque, and marmoset (Watakabe, 2009; Bernard et al., 2012; Shukla et al., 2014), it is of interest whether the claustrum‐enriched genes in macaques and mice are also enriched in the claustrum in the marmoset. I show here that the nurr1, latexin, cux2, netrinG2, and GNG2 genes are enriched in the claustrum and endopiriform nucleus of the marmoset brain as in mice and macaques (Watakabe et al., 2014). In addition, I demonstrate for the first time that GNB4 and Tmem163, which were selected based on the Allen Brain atlas, are also enriched in the marmoset claustrum. Finally, gene expression profiling of the claustrum/endopiriform nucleus areas across the entire rostrocaudal axis provided insight into its inside structure.
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