Morphological and electrophysiological features of motor neurons and putative interneurons in the dorsal vagal complex of rats and mice

Abstract

The dorsal motor nucleus of the vagus (DMV) contains preganglionic motor neurons that control viscera along the subdiaphragmatic digestive tract, but may also contain neurons that do not project to the viscera. Neurons that expressed EGFP 60-72 h subsequent to PRV-152 inoculation of vagal terminals in the stomach wall were targeted for whole-cell patch-clamp recording and biocytin filling in transverse brainstem slices from rats and their quantitative morphological and electrophysiological characteristics were compared with uninfected cells. Over 90% of PRV-152 labeled neurons were also labeled subsequent to intraperitoneal injection of FluoroGold, indicating most were preganglionic motor neurons. In reconstructed neurons with an identifiable axon trajectory, two cellular subtypes were distinguished. The axon projected ventrolaterally from the DMV in 44 of 49 cells and these were likely to be vagal motor neurons. Axons of other neurons ramified within the nucleus tractus solitarius (NTS) or DMV. These cells were smaller and otherwise morphologically distinct from putative motor neurons. Transgenic mice with GFP-expressing inhibitory neurons (i.e., GIN mice) were used to identify a GABAergic subset vagal neurons. These neurons had locallyramifying axons and formed a morphologically distinct subset of DMV cells, which were similar in size and axon trajectory to GABAergic neurons in the NTS. Most neurons in the DMV therefore possess morphological features of motor neurons, but locally projecting cells and inhibitory neurons with distinct morphological features are also found within the DMV. These cells likely contribute to regulation of vagal function.

Mechanisms of facilitation of synaptic glutamate release by nicotinic agonists in the nucleus of the solitary tract

“…The NTS plays a key role in the maintenance of autonomic homeostasis and projects within the brainstem [e.g., to the dorsal motor nucleus of the vagus (DMV) and the ventrolateral medulla] that support parasympathetic and sympathetic visceral reflexes (e.g., gastrointestinal and baroreflex), as well as to higher brain regions (e.g., the thalamus and the hypothalamus) that support behavioral and endocrine functions (2, 46). Therefore, modulation of neuronal activity and synaptic transmission in the NTS by biologically active compounds such as nicotinic agonists can have potent effects on basic autonomic functions and visceral reflexes.The NTS contains a highly heterogeneous population of neurons characterized by a broad spectrum of morphological, electrophysiological, and cytochemical properties and multiple projection targets (3,6,12,17,20,23,44,55). Expression of nicotinic and muscarinic acetylcholine receptors (nAChRs and mAChRs, respectively) also varies across the NTS region (44, 55).…”

“…The NTS contains a highly heterogeneous population of neurons characterized by a broad spectrum of morphological, electrophysiological, and cytochemical properties and multiple projection targets (3,6,12,17,20,23,44,55). Expression of nicotinic and muscarinic acetylcholine receptors (nAChRs and mAChRs, respectively) also varies across the NTS region (44, 55).…”

Nicotine enhances inhibition of mouse vagal motor neurons by modulating excitability of premotor GABAergic neurons in the nucleus tractus solitarii

“…GABAergic neurons are densely distributed throughout the NTS (Blessing 1990;Fong et al 2005;Gao et al 2009;Glatzer et al 2007), and most can be activated after stimulation of primary visceral afferents (Bailey et al 2008;Glatzer et al 2007). Here we used a transgenic mouse that expresses EGFP in the somatostatinergic subset of GABA neurons in the NTS.…”

“…Useful labeling of DMV and NTS neurons occurs after 60 -72 h, a time well before onset of cellular or functional degradation (Card et al 1993;Glatzer et al 2003;Smith et al 2000). This method allows preganglionic DMV motor neurons and synaptically connected, premotor NTS neurons that are specifically related to gastric motor output to be identified and targeted for electrophysiological recording in the in vitro brain stem slice preparation (Blake and Smith 2012;Davis et al 2003;Derbenev et al 2004;Gao et al 2009;Gao and Smith 2010;Glatzer et al 2003Glatzer et al , 2007Glatzer and Smith 2005;Smith et al 2000;Williams et al 2007). Neurons expressing EGFP or mRFP1 were visualized in living tissue under epifluorescence by using fluorescein isothiocyanate (FITC) or tetramethylrhodamine isothiocyanate (TRITC) filter sets.…”

μ-Opioid receptor stimulation in the medial subnucleus of the tractus solitarius inhibits gastric tone and motility by reducing local GABA activity

“…An excitatory effect of MOR stimulation in the DMV on gastric tone and motility was not unexpected. It is well documented that DMV neurons receive local GABAergic input, even from interneurons (12,47), and MOR-mediated reduction of this local inhibition would result in disinhibition of gastric-projecting DMV neurons and excitation at the level of the stomach.…”