Distribution and connections of inspiratory premotor neurons in the brainstem of the pigeon (Columba livia)

Abstract

We have recorded extracellular, inspiratory-related (IR) unit activity in the medulla at locations corresponding to those of neurons retrogradely labeled by injections of retrograde tracers in the lower brachial and upper thoracic spinal cord, injections that covered cell bodies and dendrites of motoneurons innervating inspiratory muscles. Bulbospinal neurons were distributed throughout the dorsomedial and ventrolateral medulla, from the spinomedullary junction through about 0.8 mm rostral to the obex. Almost all of the 104 IR units recorded were located in corresponding parts of the ventrolateral medulla, rostral to nucleus retroambigualis, where expiratory related units are found. Injections of biotinylated dextran amine at the recording sites labeled projections both to the spinal cord and to the brainstem. In the lower brachial and upper thoracic spinal cord, bulbospinal axons traveled predominantly in the contralateral dorsolateral funiculus and terminated in close relation to the dendrites of inspiratory motoneurons retrogradely labeled with cholera toxin B-chain. In the brainstem, there were predominantly ipsilateral projections to the nucleus retroambigualis, tracheosyringeal motor nucleus (XIIts), ventrolateral nucleus of the rostral medulla, infraolivary superior nucleus, ventrolateral parabrachial nucleus, and dorsomedial nucleus of the intercollicular complex. In all these nuclei, except XIIts, retrogradely labeled neurons were also found, indicating reciprocity of the connections. These results suggest the possibility of monosynaptic connections between inspiratory premotor neurons and inspiratory motoneurons, which, together with connections of IR neurons with other brainstem respiratory-vocal nuclei, seem likely to mediate the close coordination that exists in birds between the vocal and respiratory systems. The distribution of IR neurons in birds is similar to that of the rostral ventral respiratory group (rVRG) in mammals.

Avian nucleus retroambigualis: Cell types and projections to other respiratory‐vocal nuclei in the brain of the zebra finch (Taeniopygia guttata)

“…obs. ), and the inspiratory-related nucleus parambigualis (PAm) is a rostral continuation of RAm at levels straddling the obex (Reinke and Wild, 1997, 1998). …”

“…In birds PAm neurons generally fire in phase with inspiration and likewise project to thoracic spinal motoneurons innervating inspiratory muscles (Reinke and Wild, 1997, 1998). Whether PAm bulbospinal neurons have collaterals to RAm is unknown, as is the function of the reciprocal connections between them.…”

“…RVL has been postulated to be equivalent to the mammalian Bötzinger complex (BötC) and IOS to the retrofacial nucleus (Reinke and Wild, 1997). However, a strict comparison of RVL with BötC is complicated by the fact that birds do not possess a functional diaphragm, a phrenic nucleus, or a dorsal respiratory group that projects upon a phrenic nucleus.…”

Neural pathways for bilateral vocal control in songbirds

“… Abstract Ipsilateral and contralateral projections of nucleus robustus archistriatalis (RA), a telencephalic vocal premotor nucleus, to respiratory‐vocal nuclei in the brainstem were defined in adult male Wasserschlager canaries, grey catbirds, and zebra finches, three songbird species that appear to differ in the degree of lateralized syringeal dominance. In all three species, ipsilateral projections of RA to the medulla included the tracheosyringeal part of the hypoglossal nucleus (XIIts), that innervates the syrinx, the bird's vocal organ, the suprahypoglossal area (SH), and two respiratory‐related nuclei, retroambigualis (RAm) and parambigualis (PAm; Reinke and Wild [1998] J Comp Neurol 391:147–163). Projections of RA to the contralateral XIIts, SH and RAm, were substantial in canaries, which use the left side of the syrinx predominantly during singing; less pronounced in catbirds, which have no lateral dominance for song control; and least pronounced in zebra finches, in which there is a right‐sided dominance for song control.…”

Neural pathways mediating control of reproductive behavior in male Japanese quail

“…This is explained by the fact that DM projects upon a suite of vocal‐respiratory brainstem nuclei that includes the vocal motor nucleus (n. tracheosyringealis, or XIIts) and nucleus retroambigualis (RAm; Wild et al, 1997). RAm projects upon lower thoracic and upper lumbar motor neurons that innervate expiratory muscles, and also projects upon XIIts, a projection thought to underlie the coordination of expiration and vocalization in the production of species‐typical calls or songs (Wild, 1993, 1994; Reinke and Wild, 1997, 1998; Sturdy et al, 2003; Kubke et al, 2005). Although the resemblance of the projections of DM and RAm in birds to those of the lateral PAG and NRA in mammals has been noted in the context of vocalization and respiration (Wild et al, 1997, 2009), it has not hitherto been asked whether RAm also has projections to the sacral spinal cord that, like those of NRA, may be involved in reproductive behavior.…”