Physiological and anatomical properties of intramedullary projection neurons in rat rostral nucleus of the solitary tract

Abstract

The rostral nucleus of the solitary tract (rNTS), the first-order relay of gustatory information, not only transmits sensory information to more rostral brain areas but also connects to various brain stem sites responsible for orofacial reflex activities. While much is known regarding ascending projections to the parabrachial nucleus, intramedullary projections to the reticular formation (which regulate oromotor reflexive behaviors) remain relatively unstudied. The present study examined the intrinsic firing properties of these neurons as well as their morphological properties and synaptic connectivity with primary sensory afferents. Using in vitro whole cell patch-clamp recording, we found that intramedullary projection neurons respond to depolarizing current injection with either tonic or bursting action potential trains and subsets of these groups of neurons express A-type potassium, H-like, and postinhibitory rebound currents. Approximately half of the intramedullary projection neurons tested received monosynaptic innervation from primary afferents, while the rest received polysynaptic innervation, indicating that at least a subpopulation of these neurons can be directly activated by incoming sensory information. Neuron morphological reconstructions revealed that many of these neurons possessed numerous dendritic spines and that neurons receiving monosynaptic primary afferent input have a greater spine density than those receiving polysynaptic primary afferent input. These results reveal that intramedullary projection neurons represent a heterogeneous class of rNTS neurons and, through both intrinsic voltage-gated ion channels and local circuit interactions, transform incoming gustatory information into signals governing oromotor reflexive behaviors.

Inhibitory modulation of optogenetically identified neuron subtypes in the rostral solitary nucleus

“…Cells held in current clamp were injected with current steps (0.02 nA, 250 ms) ranging from Ϫ0.1 to 0.36 nA or until the number of action potentials began to decrease, to define a threshold, maximum firing frequency, and breakpoint (Table 1). Cells were classified as either "burst" or "tonic" based on the response to 0.1-nA depolarization (Corson and Bradley 2013;Wang and Bradley 2010a). Neurons that responded with action potentials that did not extend past 125 ms were deemed burst; those that persisted throughout the stimulation period were classified as tonic.…”

“…Thus it remains possible that other GABAergic neurons express I A . Similarly, I h was detected in subsets of both PBN-and RF-projecting neurons, but its prevalence in GABAergic neurons was not specified (Corson and Bradley 2013;Suwabe and Bradley 2009;Wang and Bradley 2010a).…”

“…In addition to the receptor-mediated inhibitory effects of GABA (Liu et al 1993;Wang andBradley 1993, 1995), inhibition can further influence the excitability of rNST neurons through ion channels activated or deinactivated by hyperpolarization. When hyperpolarized, rNST cells show evidence of both the nonspecific cation current I h and/or a transient outward K ϩ current, I A (Corson and Bradley 2013;Suwabe and Bradley 2009;Tell and Bradley 1994;Uteshev and Smith 2006;Wang and Bradley 2010a). These currents do not appear to be ubiquitous.…”

“…These currents do not appear to be ubiquitous. For example, I A was present in subsets of neurons that projected to the parabrachial nucleus (PBN) (Suwabe and Bradley 2009) or reticular formation (RF) (Corson and Bradley 2013) but absent in GABAergic neurons (Wang and Bradley 2010a). This latter conclusion, however, was based on identifying GABAergic neurons in the "GIN" mouse (Oliva et al 2000), in which EGFP in inhibitory rNST neurons was found principally in a circumscribed region, the ventral subdivision (Travers et al 2005;Wang and Bradley 2010a).…”

Neurons with diverse phenotypes project from the caudal to the rostral nucleus of the solitary tract

“…The ventral subdivision of rNST also receives a robust cNST projection. This region is subjacent to the dense primary afferent input located in the central subdivision but some taste responses have been noted there (Geran & Travers, 2006;Hu, Travers, & Travers, 1997;McPheeters et al, 1990), perhaps due to monosynaptic input onto dorsally extending dendrites (Corson & Bradley, 2013;Wang & Bradley, 2010). The ventral subdivision projects preferentially to the underlying reticular formation (Halsell et al, 1996), which houses circuitry implicated in the consummatory phase of feeding, including stereotyped taste-modulated acceptance and rejection behaviors, i.e.…”