Anatomical characterization of subcortical descending projections to the inferior colliculus in mouse

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The inferior colliculus (IC) is a major integration site in the auditory system, and the filter properties of IC neurons are modifiable by manipulations of descending inputs and behavioral context (Yan and Suga, 1998; Ma and Suga, 2001; Malone and Semple, 2001; Yan and Ehret, 2001; Yan et al., 2005; Metzger et al., 2006; Malmierca et al., 2009). Most previous work on descending control of the IC has been focused on the massive set of projections from the auditory cortex (AC) to the IC (reviewed in Suga, 2008; Bajo and King, 2011; Stebbings et al., 2014). However, additional descending projections to the IC also arise from subcortical structures. For example, several anatomical studies have described projections to the IC that originate in the auditory thalamus, paralaminar thalamic nuclei, and brachium of the IC of mice, rats, cats, gerbils, and monkeys (Adams, 1980; Kuwabara and Zook, 2000; Senatorov and Hu, 2002; Winer et al., 2002; Kuwabara, 2012). These projections target nonprimary parts of the IC (the lateral cortex [LC] and dorsal cortex [DC]), emanate from nonprimary auditory thalamic regions (the medial division of medial geniculate body, suprageniculate nucleus, peripeduncular nucleus, and paralaminar nuclei) and branch to lower brainstem structures. It is not yet known whether these subcortically derived projections to the IC contribute to previously described modifications of IC tuning properties after AC stimulation, although it should be noted that the sources of thalamotectal projections are heavily innervated by the AC (Llano and Sherman, 2008; Mellott et al., 2014).
Previous work in the auditory system of nonmammalian species as well as work from the visual system suggests that the thalamotectal pathway is highly conserved. The dominant descending projection to the frog auditory midbrain is from the posterior thalamus (Feng and Lin, 1991), which may play a role in motivational aspects of phonotaxis (Endepols et al., 2003). The frog thalamotectal pathway may also have an inhibitory component, based on intra‐ and extracellular recordings in the frog midbrain after thalamic stimulation (Endepols and Walkowiak, 1999; Ponnath and Farris, 2014). The visual tectum also receives subcortical descending input from the thalamus in turtles (Kenigfest and Belekhova, 2009), pretectal and thalamic areas in frog (Ingle, 1973; Trachtenberg and Ingle, 1974; Chapman and Debski, 1995; Li et al., 2005) and rat, at least part of which in all three species is inhibitory (Ingle, 1973; Born and Schmidt, 2004; Li et al., 2005; Kenigfest and Belekhova, 2009).
Little is known about the mammalian auditory thalamotectal pathway. The regions of the thalamus containing cells that project to the IC comprise a heterogeneous population of cells with a range of soma sizes, and have neurons with both stellate and elongated morphologies (Senatorov and Hu, 2002; Winer et al., 2002; Smith et al., 2006). These regions of the thalamus generally stain positively for the calcium‐binding proteins calbindin or calretinin (Cruikshank et al., 2001; Lu et al., 2009), although it is not yet known which, if any, of these calcium‐binding proteins are found in thalamotectal cells. The presence or absence of such calcium‐binding proteins has been an integral part of schemes to parse thalamic nuclei (Jones, 2001), and therefore may have functional implications. In addition, the regions of the thalamus populated by thalamotectal cells project to regions outside of the auditory system, such as the basal ganglia and amygdala (Takada et al., 1985; Clugnet et al., 1990; Bordi and LeDoux, 1994). It is not currently known if the same populations of thalamic cells that project to the IC also project to the basal ganglia or amygdala.
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