Tangential migration of corridor guidepost neurons contributes to anxiety circuits

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Brain functioning relies on exquisite circuits that begin to be established during embryogenesis by the coordinated migration of specific neuronal types and their wiring via long‐range axonal connections. Crucially, cell migration and axon guidance occur concomitantly, influencing each other in a complex developmental choreography that is not yet fully understood. In particular, the mammalian neocortex forms connections with the rest of the brain via the internal capsule, a large fascicle of axons that comprises corticofugal efferent and reciprocal thalamocortical afferent projections (TCAs), which convey sensory and motor information to the neocortex (Grant, Hoerder‐Suabedissen, & Molnár, 2012; Lemon, 2008; Molnár, Garel, López‐Bendito, Maness, & Price, 2012; Sherman, 2016). The guidance of TCAs along an internal trajectory relies on a population of tangentially migrating neurons called corridor (Co) cells, which form a permissive “bridge” for axons en route to the neocortex (Bielle, Marcos‐Mondejar, Keita, et al., 2011; Bielle, Marcos‐Mondéjar, Leyva‐Díaz, et al., 2011; Feng et al., 2016; Lokmane et al., 2013; Lokmane & Garel, 2014; Squarzoni, Thion, & Garel, 2015; Zhou, Qu, Tissir, & Goffinet, 2009). Co cells are located in the subpallium, which is a major site of neuronal proliferation and migration. The subpallium includes the lateral, medial and caudal ganglionic eminences (LGE, MGE, and CGE, respectively) and the preoptic area (POA); these structures generate projection neurons of the striatum, the pallidum and the amygdala (Dodson et al., 2015; Eisenstat et al., 1999; Hagimoto, Takami, Murakami, & Tanabe, 2017; Hamasaki, Goto, Nishikawa, & Ushio, 2003; Long, Cobos, Potter, & Rubenstein, 2009; Marín & Rubenstein, 2003; Nóbrega‐Pereira et al., 2010; Waclaw, Ehrman, Pierani, & Campbell, 2010; Wichterle, Turnbull, Nery, Fishell, & Alvarez‐Buylla, 2001). In addition, the MGE, the LGE/CGE and POA produce interneurons that migrate tangentially to contribute to cortical and subcortical circuits (Corbin, Nery, & Fishell, 2001; Corbin & Butt, 2011; Elshatory & Gan, 2008; Gelman, Marín, & Rubenstein, 2012; Hirata et al., 2009; Marin, Anderson, & Rubenstein, 2000; Marín & Rubenstein, 2001; Nóbrega‐Pereira et al., 2008; Torigoe, Yamauchi, Kimura, Uemura, & Murakami, 2016; Touzot, Ruiz‐Reig, Vitalis, & Studer, 2016; Xu, Tam, & Anderson, 2008). Co cells express transcription factors Islet1 and Ebf1 (López‐Bendito et al., 2006), similarly to LGE‐derived striatal projection neurons of the direct pathway (dSPN; Ehrman et al., 2013; Garel, Marín, Grosschedl, & Charnay, 1999; Lu, Evans, Hirano, & Liu, 2014). However, unlike the latter, which migrate radially to form the striatum (Halliday & Cepko, 1992; Hamasaki et al., 2003; Wichterle et al., 2001), Co neurons migrate tangentially from the LGE into the MGE from E11.5 to E14, where they create a permissive corridor for TCAs in the otherwise non‐permissive MGE (López‐Bendito et al., 2006). It has been shown that defects in corridor positioning led to abnormal TCAs pathfinding (Bielle, Marcos‐Mondejar, Keita et al., 2011; Bielle, Marcos‐Mondéjar, Leyva‐Díaz et al., 2011; Feng et al., 2016; Morello et al., 2015; Zhou et al., 2009). In addition, Co cells not only control TCA internal navigation but also their topographic organization. Indeed, Co cells express gradients of guidance cues that organize TCAs along the rostro‐caudal axis and allow them to target specific cortical areas (Bielle, Marcos‐Mondejar, Keita, et al., 2011; Bielle, Marcos‐Mondéjar, Leyva‐Díaz, et al., 2011; Garel & López‐Bendito, 2014; Lokmane et al., 2013; Lokmane & Garel, 2014; Squarzoni et al., 2015). Therefore, Co cells play essential and diverse roles in TCA pathfinding (Lokmane & Garel, 2014; López‐Bendito et al., 2006; Molnár et al., 2012; Squarzoni et al., 2015). Despite their importance, we have little information on this neuronal population and whether it contributes to adult brain circuits.
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