Trigeminal and telencephalic projections to jaw and other upper vocal tract premotor neurons in songbirds: Sensorimotor circuitry for beak movements during singing

Abstract

During singing in songbirds, the extent of beak opening, like the extent of mouth opening in human singers, is partially correlated with the fundamental frequency of the sounds emitted. Since song in songbirds is under the control of “the song system” (a collection of interconnected forebrain nuclei dedicated to the learning and production of song), it might be expected that beak movements during singing would also be controlled by this system. However, direct neural connections between the telencephalic output of the song system and beak muscle motor neurons in the brainstem are conspicuous by their absence, leaving unresolved the question of how beak movements are affected during singing. By using standard tract tracing methods, we sought to answer this question by defining beak premotor neurons and examining their afferent projections. In the caudal medulla, jaw premotor cell bodies were located adjacent to the terminal field of the output of the song system, into which many premotor neurons extended their dendrites. The premotor neurons also received a novel input from the trigeminal ganglion and an overlapping input from a lateral arcopallial component of a trigeminal sensorimotor circuit that traverses the forebrain. The ganglionic input in songbirds, which is not present in doves and pigeons that vocalize with a closed beak, may modulate the activity of beak premotor neurons in concert with the output of the song system. These inputs to jaw premotor neurons could, together, affect beak movements as a means of modulating filter properties of the upper vocal tract during singing.

The acoustic effect of vocal tract adjustments in zebra finches

“…Little is known about the motor coordination of the various upper vocal tract movements, in regard to functional connections, while the neural substrate for such coordination could be the ventromedial part of the parvocellular part of reticular formation (RPvcm), which is the pre-motor nucleus for upper vocal tract structures (Wild and Krützfeldt 2011). It is not clear whether movements of the different components, such as beak and OEC, are functionally linked during either their activity in ensuring airway patency during silent breathing or during vocal behavior.…”

The respiratory-vocal system of songbirds

“…Beak gape, and even tongue and laryngeal movements, may be more related to the control of the size and shape of the oropharyngeal-esophageal cavity, the volume of which in cardinals has been shown to be inversely related to sound frequency (Goller and Cooper, 2008; Riede et al, 2006, 2013; Suthers and Zollinger, 2008). The close relationship of the neural control of upper vocal tract structures to that of the syrinx and expiration has been studied anatomically by Wild and Krützfeldt (2012).…”

Afferents from Vocal Motor and Respiratory Effectors Are Recruited during Vocal Production in Juvenile Songbirds

“…Trigeminal brainstem regions are potentially key loci for coordinating various sensory inputs with vocal effectors, since they also receive afferent inputs from upper vocal tract structures such as the beak, jaw, and oral cavity (Wild et al, 1984; Arends and Zeigler, 1986; Wild and Farabaugh, 1996; Wild, 2004, 2008; Wild and Krutzfeldt, 2012). One possible route between trigeminal regions and circuits for song-control involves a projection from PrV and nuclei of the lateral lemniscus (nLL) to telencephalic somatosensory/auditory regions (basorostral nucleus, Bas, and frontal nidopallium,NF) that project in turn to regions of dorsal caudo-lateral cortex (dNCL) and motor cortex (intermediate arcopallium, Ai; Fig.…”

“…6). Although this circuit was originally discovered in pigeons (which do not learn their vocalizations), much of it has also been demonstrated in zebra finches (Wild et al, 1985; Wild and Farabaugh, 1996; Wild and Krutzfeldt, 2012). Furthermore, both Ai and dNCL in zebra finches are part of a circuit including a subregion of the song-control nucleus LMAN (shell region of the lateral magnocellular nucleus of the anterior nidopallium) which is essential for vocal learning in juvenile birds (Bottjer et al, 2000)(Bottjer and Altenau, 2009).…”

“…Thus, Ai is a song-control region in zebra finches, but it is not known whether the same region of Ai receives inputs from both LMAN SHELL and auditory/trigeminal regions; hence both Ai and dNCL are shown in white here, see Discussion. Based on (Wild, 1981; Bottjer and Arnold, 1982; Arends et al, 1984; Wild et al, 1985; Arends et al, 1988; Wild, 1990; Wild et al, 1990; Wild, 1993a, b; Wild and Farabaugh, 1996; Reinke and Wild, 1997; Wild et al, 1997; Reinke and Wild, 1998; Striedter and Vu, 1998; Sturdy et al, 2003; Ashmore et al, 2008; Wild and Krutzfeldt, 2012). Abbreviations: Ai, intermediate arcopallium; Bas, basorostral nucleus; dNCL, dorsal caudolateral nidopallium; DM, dorsomedial nucleus of the inferior colliculus; HVC, higher vocal center; LMAN SHELL , shell region of the lateral magnocellular nucleus of the anterior nidopallium; NIf, interfacial nucleus; NF, frontal nidopallium; nLL, nuclei of the lateral lemniscus; nTS, nucleus of the solitary tract; nTTD, nucleus of the descending trigeminal tract; nXII ts , tracheo-syringeal hypoglossal nucleus; PBvl, ventrolateral portion of the parabrachial nucleus; PAm, nucleus parambigualis; PBvl, ventrolateral parabrachial nucleus; PrV, principal sensory nucleus of the trigeminal tract; RA, robust nucleus of the arcopallium; RAm, nucleus retroambigualis; Uva, uvaeform nucleus of the thalamus.…”