As opposed to the six-layered cortical structure of the mammalian brain, the songbird brain is organized into different functional nuclei (Fernando Nottebohm, Stokes, and Leonard 1976). The nuclei involved in song learning and song production have been intensively studied in recent decades (Akutagawa and Konishi
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1998; Aronov, Andalman, and Fee 2008; Bottjer, Miesner, and Arnold 1984; F Nottebohm, Stokes, and Leonard 1976). The neural circuits linking these song-related nuclei relay the sensory input and the motor output of the song. These nuclei and their interconnections are crucial for the learning, production, and memory of birdsong (Scharff and Nottebohm 1991), and together they form the song system (Anton Reiner, David J.Perkel, Claudio V. Mello et al. 2004) (Figure 1.
3).
Figure 1. 3: A schematic of the song system emphasizing HVC and its connections. This parasagittal view of the songbird brain shows the major brain pathways involved in song production and song learning. Adapted from (Mooney 2014).
* Note that in this figure, the HVC is colored as if it has distinctive subregions along rostrocaudal axis, that correspond to the red and blue brain pathways, respectively. This is not the case. For a more accurate review of the HVC local architecture, please see section 1.3.
The song system of zebra finches comprises two major brain pathways that are actively involved in song production and song learning. The song motor pathway (SMP, shown in blue in Figure 1. 3), drives the production of the crystallized song in adult birds, and the anterior forebrain pathway (AFP, shown in red in Figure 1. 3), drives song learning and the production of the subsong (vocal babbling) in juveniles (M. S. Brainard and Doupe 2000).
The SMP starts with nucleus HVC and projects to the robust nucleus of the arcopallium (RA), with some reciprocal connections from the RA back to HVC (Roberts et al. 2008; Yip, Miller-Sims, and Bottjer 2012). RA neurons in turn
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project to the dorsal medial nucleus (DM) (not shown in Figure 1. 3) and the tracheosyringeal part of the hypoglossal nucleus (nXIIts) (Wild 1993). The motor neurons in the nXIIts then directly innervate the syringeal muscles of the vocal organ, the syrinx, in order to produce the learned songs in adult male zebra finches (Vicario and Nottebohm 1988). Alternatively, the DM nucleus projects to brainstem respiratory areas, the nucleus paraambiguus (PAm) and nucleus retroambiguus (RAm) (not shown in Figure 1. 3) (Vates, Vicario, and Nottebohm 1997), to coordinate breathing during singing. Single-unit recording of the RA-projecting neurons in HVC, denoted as HVCRA neurons, revealed that the neurons fire sparsely to drive RA activity during song production (Hahnloser, Kozhevnikov, and Fee 2002). In contrast, premotor neurons in RA fire relatively dense and short bursts of spikes, with less precision but still reliably associated with the song features during singing (Yu and Margoliash 1996). The motor neurons in the descending target of RA, the nucleus nXIIts, are somewhat somatotopically organized to project to and control different muscles of the syrinx (Vicario and Nottebohm 1988). Thus, these interconnected brain nuclei, HVC, RA, and nXIIts, structurally and functionally form the neural pathway underlying song production in adult male zebra finches (McCasland 1987).
The other brain pathway, the AFP, also connects HVC to RA through various nuclei.
It starts with another class of HVC projection neurons, the HVCX neurons that project to area X. Unlike the late-developing projections from HVC to RA, the pathway that links HVC to area X is generated early in development (Mooney and Rao 1994). Songbird area X, which is the homolog of mammalian basal ganglia, in turn projects to the dorsal lateral nucleus of the medial thalamus (DLM). From DLM, the AFP continues projecting back to the lateral magnocellular nucleus of the anterior nidopallium (LMAN) in the forebrain, which then projects back to the motor circuitry at RA and merges again (after HVC) with the SMP pathway. In addition, LMAN sends collateral projections back to area X and forms the recurrent connections of the basal ganglia-thalamocortical loop (Doupe et al. 2005; Goldberg and Fee 2011). Lesions in any component of the AFP pathway disrupt song development in juvenile birds, but do not affect the maintenance or production of song in adults (Bottjer et al. 1984; Goldberg and Fee 2011; Scharff and Nottebohm 1991). The AFP actively drives vocal babbling in juvenile birds, but does not require HVC as shown by a lesion experiment (Aronov et al. 2008).
As highlighted in green and white in Figure 1. 3, auditory information reaches the song system through different afferent pathways (Mooney 2014). The auditory information of the tutor song reaches and is stored in the song system, and actively shapes the song learning related neural circuit in juveniles (Keller and Hahnloser 2009; Roberts et al. 2010; Yanagihara and Yazaki-Sugiyama 2016). Tutor song deprivation in juvenile leads to significant long-lasting structural and physiological changes in HVC, even into adulthood, as observed from a closely related songbird species (Peng et al. 2012). In addition to learning, auditory feedback is also shown to be important for song maintenance in adult zebra finches (M. S. Brainard and Doupe 2000; Tschida and Mooney 2012).
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Many brain nuclei in the zebra finch song system show song-selective electrophysiological responses to auditory stimuli (Vicario and Yohay 1993), even in the nuclei that are mainly involved in song motor functions, which suggests that these nuclei have mixed sensorimotor characteristics (Doupe and Solis 1997). HVC, as one of such nuclei located at the origin of the SMP and AFP pathways, shows selective response to the bird’s own song (BOS). Intracellular recordings have shown that all three major neuron types of HVC, HVCRA neuron, HVCX neuron, as well as inhibitory interneurons (HVCI neurons), are BOS selective (Rosen and Mooney 2000, 2003). This selectivity most likely arises within HVC because BOS-selective responses are absent or less selective in the known afferents to HVC (Coleman et al. 2007; Doupe and Konishi 1991; Janata and Margoliash 1999).
The zebra finch HVC is important in both song production and song learning, and it plays an active role in the auditory processing of the tutor song during song development. Therefore, I focused on HVC in the present study.