Medullary visceral reflex circuits: Local afferents to nucleus tractus solitarii synthesize catecholamines and project to thoracic spinal cord

Abstract

Visceral feedback circuits in lower brainstem were elucidated with retrograde tracers by mapping neurons that issue local projections to the general visceral afferent division of the nucleus tractus solitarii (NTS) and dorsomotor vagal nucleus (DMX) in adult male rats. In study 1, spinal and intramedullary afferents to the visceral-sensorimotor complex (NTS-X) were traced to contiguous populations of cell bodies arranged in cylindrical segmental organization. NTS-X afferents derive from curvilinear arrays of neurons that parallel the efferent radiations of the solitariotegmental tract. Newly discovered afferents arise from circumscribed cell groups in the dorsal reticular formation and periventricular zone. Another source was traced to a paraambigual cell column in the apex of the rostral ventrolateral reticular nucleus (n.RVL). In study 2, catecholaminergic afferents were initially defined with combined retrograde transport-immunocytochemical methods. Deposits of retrograde tracers into NTS-X transported to neurons containing tyrosine hydroxylase (TH) in the A1, C1, and C3 areas or phenylethanolamine N-methyltransferase (PNMT) in the C1 area of the n.RVL and C3 area. In study 3, it was revealed that NTS-X afferents arise, in part, as collaterals of thoracic reticulospinal neurons. Deposits of the retrograde fluorescent tracer Fluorogold into the upper thoracic cord and rhodamine-labeled microbeads into NTS-X transported to the same neurons within a subambigual locus in n.RVL and parts of nucleus raphe magnus. In study 4, dual retrograde tracer-immunocytochemical analysis demonstrated that catecholamines are synthesized by a subset of neurons in the n.RVL that issue collaterals to the NTS-X and thoracic cord. Double retrogradely labeled TH- or PNMT-immunoreactive cell bodies were restricted to the C1 area within a 450-microns column bordered rostrally by the facial nucleus and ventrally by the medullary subpial surface. We conclude that visceral reflex arcs are reciprocally organized. Targets of NTS projection are also sources of local NTS-X afferent innervation. Catecholaminergic and other local afferents from reticular formation, periventricular, and spinal gray may, via collaterals, simultaneously modulate visceral reflex excitability at the level of NTS and the outflow of autonomic and respiratory motoneurons.

Visceral Afferents Directly Activate Catecholamine Neurons in the Solitary Tract Nucleus

“…The location of CA neurons amid the terminal fields of visceral afferents led to a general assumption that NTS CA neurons broadly integrate afferent information and relay it to multiple brain regions via their extensive projections (Chiba and Kato, 1978;Takahashi et al, 1979;Kalia et al, 1985a,b;Mtui et al, 1995). Activation of afferents from gastrointestinal, cardiovascular, and respiratory targets supported widespread stimulation of CA NTS neurons in various behaviors including sleep and stress (Murphy et al, 1994;Chan and Sawchenko, 1998;Dayas et al, 2004;Kubin et al, 2006).…”

Divergent projections of catecholaminergic neurons in the nucleus of the solitary tract to limbic forebrain and medullary autonomic brain regions

“…Likewise, using the same retrograde tracer, a projection from the nucleus paragigantocellularis (PGi) to the NTS was established (Ross et al, 1985;Hancock, 1988;Van Bockstaele et al, 1989;Mtui et al, 1995;Aicher et al, 1996). The term PGi has been used in a myriad of anatomical and physiological studies (Satoh et al, 1979;Punnen et al, 1984;Van Bockstaele et al, 1989;Van Bockstaele et al, 1998a).…”

cGMP/Protein Kinase G-Dependent Potentiation of Glutamatergic Transmission Induced by Nitric Oxide in Immature Rat Rostral Ventrolateral Medulla Neurons in Vitro

“…Both electrophysiological and anatomical studies showed that a subset of RVLM neurons directly innervates preganglionic vasomotor neurons in the intermediolateral cell columns of the spinal cord, which are involved in the regulation of vasomotor and cardiac tone (Morrison et al, 1991;Deuchars et al, 1995). In addition, the RVLM neurons are tonically active in vivo and receive convergent excitatory and inhibitory inputs from multiple sources (Mtui et al, 1995;Guyenet et al, 1996). However, little is known regarding the physiological regulation of the tonic excitation of these neurons.…”