In songbirds, neural vocal control is achieved by a chain of interconnected brain areas in the fore-, mid-, and hindbrain (Nottebohm et al., 1976; Vates et al., 1997; Vu et al., 1994; Wild, 1997; Yu et al., 1996). Vocal learning of songbirds correlates with the differentiation of forebrain vocal control areas, the robust nucleus of the arcopallium (RA), lateral magnocellular nucleus of the anterior nidopallium (lMAN), HVC (used as proper name), medial magnocellular nucleus of the anterior nidopallium (mMAN), Area X, and nucleus interface of the nidopallium (NIF) (Fig. 3.1). Albeit under intense study, the specific role of any forebrain nucleus for learning and production of vocal pattern is unclear. Hummingbirds and parrots, too, evolved forebrain networks, which are composed of multiple areas (for review: Gahr, 2003). In parakeets, some of these areas do not seem homologous to the forebrain vocal control nuclei of oscines, while the hodologic and molecular properties of others suggest similarities in the neural organization of forebrain vocal control pathways of budgerigars and songbirds (Durand et al., 1997; Jarvis and Mello, 2000; Striedter, 1994). Similarly, the singing hummingbird species such as Anna's hummingbird (Calypte anna) and Amazilia hummingbird (Amazilia amazi-lia) differentiate an lMAN-like, an HVC-like, and an RA-like area (Gahr, 2000). Areas similar to these reported by Gahr (2000) were found in the Sombre hummingbirds (Aphantochroa cirrhochloris) and Rufous-breasted hermit (Glaucis hirsuta) to be active during vocalizing as indicated by the expression of immediate early genes, a molecular activity marker (Jarvis et al., 2000). The HVC-, RA-, and lMAN-like areas are rudimentary in adult male Ruby-throated hummingbirds (Archilochus colubris) and Allen's hummingbirds (Selasphorus sasin) that do not sing (Gahr, 2000). Areas comparable to vocal areas of songbirds, parrots, and hummingbirds are not found in vocal nonlearning swifts and suboscines, the taxonomic sister groups of hummingbirds and songbirds, respectively (Gahr, 2000). These areas are further missing in owls, doves, gulls, and gallinaceous species, avian taxa that do not learn vocalizations (Gahr, 2000). Common to all three vocal-learning avian taxa is a projection of archistriatal neurons on brain stem nuclei, in particular to the medullary syringeal motonucleus (nucleus hypoglossus pars tracheosyringealis, nXIIts) and the respiratory pre-motonucleus RAm (nucleus retroambigualis) (Gahr, 2000; Striedter, 1994; Wild, 1997)(Fig.3.1).
The nucleus hypoglossus appears to be the common motonucleus of the syrinx in all bird taxa. Similarly, the vocal-respiratory areas of the brain stem and parts of the midbrain nucleus intercollicularis innervating the brain stem areas are common to all birds (Wild, 1997; Wild et al., 1997).
Figure 3.1. The vocal control system of songbirds and degrees of sexual dimorphisms. This schematic diagram of a composite view of parasagittal sections of a songbird brain gives approximate positions of vocal nuclei and brain regions and their content of androgen receptors (red, rose) and estrogen receptors (green). All structures are bilateral—for reasons of clarity, only those in one-half of the brain are depicted. Further, some thalamic brain areas that appear important for coordination of the left and right vocal control network are omitted. The volumes of vocal control areas of adult zebra finches are highly sexually dimorphic, while those of canaries are to a lesser extent, indicated in the relative size of the areas. Despite these sex differences, all areas and connections as well as the sex hormone receptors are present in the female vocal control system and syrinx. The HVC of canaries contains higher amounts of estrogen receptors compared to the zebra finch. Area X and NC (rose) contains androgen receptors in only some animals. Androgen receptors are found in the caudal nidopallium including the caudo-medial nidopallium. Abbreviations: DLM, nucleus dorsolateralis anterior, pars medialis; DM, dorsomedial nucleus of the midbrain nucleus intercollicularis; HVC, acronym used as a proper name; formerly known as high vocal center; Field L; lMAN, lateral magno-cellular nucleus of the anterior nidopallium; mMAN, medial magnocellular nucleus of the anterior nidopallium; NC, caudal nidopallium; NIF, nucleus interface of the nido-pallium; nXIIts, tracheosyringeal portion of the nucleus hypoglossus; RA, robust nucleus of the arcopallium; RAm, nucleus retroambigualis; rVRG, rostroventral respiratory group; Area X.
Auditory input to the forebrain vocal areas is likely provided by the forebrain field L, which represents the auditory cortex of birds and adjacent areas of the caudal nidopallium including the caudomedial nidopallium (NCM) representing secondary auditory cortices (for review see Bolhuis and Gahr, 2006). There is, however, no strong direct synaptic input of the primary or secondary auditory cortex to the vocal areas (Fortune and Margoliash, 1995).
Next to this indirect connection with the auditory system of songbirds, forebrain vocal areas obtain input of catecholaminergic neurons located mainly in the midbrain central gray (HVC) and area ventralis of Tsai (HVC, RA, Area X) (Appeltants et al., 2001, 2002) and cholinergic input of the ventral paleostriatum (Sakaguchi et al., 2000) or via uvaeform nucleus of the thalamus (Akutagawa and Konishi, 2005).
In songbirds, all areas of the vocal control circuit are found in males and females, although there are considerable sex differences in various species (Fig. 3.1; see below, Table 3.1). In particular, forebrain nuclei are degenerated or cannot be delineated anatomically in adult females of those songbird species in which females do not utter learned sounds such as the zebra finch and the Orange bishop (Arai et al., 1989; Nottebohm and Arnold, 1976). Nevertheless, although some areas in the zebra finch such as Area X are not visible in histological stainings, neurons in the potential region of Area X are connected with HVC, as in the case of males (Fig. 3.1 and Fig. 3.2). This suggests that even in case of species with nonsinging sexes, the general vocal control network of songbirds develops. Similarly, in non-singing female hummingbirds, forebrain vocal areas are rudimentary (Gahr, 2000). In the budgerigar, the only parrot studied in detail, vocal areas are present in females with some sexually dimorphic features (Brauth et al., 2005). In avian taxa that do not learn their vocalizations, sex differences in vocal areas are not studied in much detail. It appears that sex differences in vocalizations of these species are mainly due to steroid-dependent sexually dimorphic differentiation of the syrinx (Ballintijn and Ten Cate, 1997; Beani et al., 1995; Takahashi and Noumura, 1987) but might involve as well sex differences in subareas of the midbrain nucleus intercollicularis (for review see Beani et al., 1995).
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