Modular‐extramodular organization in developing multisensory shell regions of the mouse inferior colliculus

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Neuroanatomical approaches often provide valuable insights concerning the fine structure organization or microarchitecture of brain regions that appear nondescript in classical stains or Golgi preparations. Histochemical and immunocytochemical methods are particularly useful for highlighting specific neuronal subsets against seemingly homogeneous backgrounds. Studies comparing various neurochemical markers within a given structure and their relative degree of overlap have proved important for defining functional zones or compartments, thereby providing a more comprehensive understanding of network complexities (Burwell, 2001; Gerfen, 1992; Ma, 1993; Mana & Chevalier, 2001; Soares et al., 2001; Wallace 1986a).
The inferior colliculus (IC) is typically portrayed as a midbrain relay hub in the ascending auditory system. This depiction, while fitting for its tonotopically‐arranged central nucleus (CNIC), does not aptly describe its surrounding shell nuclei (the lateral cortex of the IC, LCIC, and the dorsal cortex of the IC, DCIC), that receive a rich array of multimodal inputs (Coleman & Clerici, 1987; Gruters & Groh, 2012; Lesicko, Hristova, Maigler, & Llano, 2016). Many of these projections specifically target the LCIC and exhibit highly compartmentalized terminal distributions in a variety of species (Stebbings, Lesicko, & Llano, 2014). Somatosensory and auditory afferents, in particular, appear largely segregated in the adult mouse LCIC (Lesicko et al., 2016). Somatosensory inputs ascending from the spinal trigeminal and dorsal column nuclei in the brainstem, along with descending projections from somatosensory cortex, terminate within a discontinuous patchy or modular LCIC layer 2 lattice. In contrast, auditory inputs from the CNIC and auditory cortex exhibit seemingly complementary terminal fields, preferentially targeting surrounding presumptive LCIC extramodular zones.
This recently described LCIC connectional modularity appears to correlate with previous reports of an underlying neurochemical framework. A distinct set of LCIC modules that span layer 2 have been most thoroughly described in the adult rat (Chernock, Larue, & Winer, 2004) and mouse (Lesicko et al., 2016; Stebbings et al., 2014) for a variety of markers, including acetylcholinesterase (AChE), nicotinamide adenine dinucleotide phosphate‐diaphorase (NADPH‐d), cytochrome oxidase (CO), glutamic acid decarboxylase (GAD), and parvalbumin (PV). Analogous markers that emphasize surrounding LCIC extramodular zones, however, have yet to be identified. Although not explicitly stated, data from a single study in rat suggests calretinin (CR) may be such a marker (Lohmann & Friauf, 1996).
Understanding how circuit arrangements interface with defined neurochemical and metabolic markers should provide insights concerning the functional significance of the patch‐matrix‐like LCIC configuration. Currently lacking is an appreciation for the development of its micro‐organization and the mechanisms that shape early LCIC target zones and their multimodal connections. This study describes the emergence of neurochemically‐defined LCIC modular fields, focusing exclusively on AChE, NADPH‐d, CO, and GAD, as preliminary findings for PV suggest it is a weak modular marker in neonatal mice. CR is identified as a novel, highly specific extramodular marker and is compared with LCIC modular patterns. Experiments pairing modular staining with CR‐labeling in the same tissue reveal complementary LCIC zones that are clearly delineated early in development. The described developing neurochemical framework is discussed in light of previous findings from our lab that show similar modular‐extramodular patterns revealed by Eph‐ephrin guidance molecule expression (Cramer & Gabriele, 2014; Gabriele et al., 2011; Wallace, Harris, Brubaker, Klotz, & Gabriele, 2016). Implications regarding potential signaling mechanisms that may influence the specificity of early multimodal LCIC inputs are addressed.
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