Orthogonal topography in the parallel input architecture of songbird HVC

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The learned songs of adult male zebra finches are encoded within HVC, a premotor region of avian cortex. Numerous studies using a variety of experimental manipulations to target HVC—ablative, electrophysiological, pharmacological, thermal, and optogenetic—have shown remarkably specific effects on the learning and/or production of song (Andalman, Foerster, & Fee, 2011; Aronov, Andalman, & Fee, 2008; Aronov, Veit, Goldberg, & Fee, 2011; Basista et al., 2014; Hamaguchi & Mooney, 2012; Long & Fee, 2008; Nottebohm, Stokes, & Leonard, 1976; Poole, Markowitz, & Gardner, 2012; Roberts, Gobes, Murugan, Ölveczky, & Mooney, 2012; Scharff, Kirn, Grossman, Macklis, & Nottebohm, 2000; Simpson & Vicario, 1990; Stauffer et al., 2012; Thompson & Johnson, 2007; Thompson, Wu, Bertram, & Johnson, 2007; Williams, Crane, Hale, Esposito, & Nottebohm, 1992; Vu, Mazurek, & Kuo, 1994). Moreover, HVC neural activity is tightly correlated with the learning and production of song (Amador, Perl, Mindlin, & Margoliash, 2013; Jarvis & Nottebohm, 1997; Jarvis, Scharff, Grossman, Ramos, & Nottebohm, 1998; Jin & Clayton, 1997; Hahnloser, Kozhevnikov, & Fee, 2002; Hamaguchi, Tschida, Yoon, Donald, & Mooney, 2014; Kosche, Vallentin, & Long, 2015; Kozhevnikov & Fee, 2007; Long & Fee, 2008; Long, Jin, & Fee, 2010; Lynch, Okubo, Hanuschkin, Hahnloser, & Fee, 2016; Markowitz et al., 2015; Okubo, Mackevicius, Payne, Lynch, & Fee, 2015; Picardo et al., 2016; Vallentin & Long, 2015; Yu & Margoliash, 1996). Given this abundance of evidence, which clearly demonstrates the importance of HVC for the learning and production of song, surprisingly little is known about the pattern of afferent input connectivity that drives and/or modulates HVC neural activity.
Until recently all tract‐tracing evidence from adult birds indicated a uniformly distributed, nontopographic pattern of input from each of HVC's five afferent nuclei (MMAN, NIf, Uva, Av, RA, see Figure 1). The absence of topography was interpreted as evidence of a pattern of convergent afferent input, with widely branched axon terminals from each afferent nucleus overlapping one another with no specific pattern throughout the volume of HVC (Akutagawa & Konishi, 2010; Bauer et al., 2008; Bottjer, Halsema, Brown, & Miesner, 1989; Foster & Bottjer, 1998; Fortune & Margoliash, 1995; Nottebohm, Kelley, & Paton, 1982; Roberts, Klein, Kubke, Wild, & Mooney, 2008). However, using a new surgical approach to target HVC and paired injections of two different tracers, we have found that afferent projections onto medial and lateral HVC are in fact organized in parallel, where distinct subpopulations of cells within each HVC afferent nucleus project exclusively to medial or lateral HVC (Basista et al., 2014). This parallel input architecture complements recent evidence that adult HVC neurons are interconnected primarily along the rostral‐caudal axis (Day, Terleski, Nykamp, & Nick, 2013; Nottebohm et al., 1982; Stauffer et al., 2012) and that medial and lateral HVC can function independently in the production of adult song (Basista et al., 2014; Poole et al., 2012).
Here, we varied both the distance between and the axial orientation of paired tracer injections into HVC to further characterize the input architecture of HVC in adult birds. Like paired tracer injections into medial and lateral HVC (Basista et al., 2014), we find distinct single‐labeled subpopulations of cells within all HVC afferent nuclei when paired tracer injections target rostral and caudal HVC. The overall pattern of labeling suggests that the terminals from each afferent neuron address only one rostral or caudal location within medial or lateral HVC, and that each HVC location receives convergent input from each afferent nucleus in parallel.
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