Abstract

Vagal and spinal sensory endings in the wall of the hepatic portal and superior mesenteric veins (PMV) provide the brain with chemosensory information important for energy balance and other functions. To determine their medullary neuronal targets, we injected the transsynaptic anterograde viral tracer HSV-1 H129-772 (H129) into the PMV wall or left nodose ganglion (LNG) of male rats, followed by immunohistochemistry (IHC) and high-resolution imaging. We also determined the chemical phenotype of H129-infected neurons, and potential vagal and spinal axon terminal appositions in the dorsal motor nucleus of the vagus (DMX) and the nucleus of the solitary tract (NTS). PMV wall injections generated H129-infected neurons in both nodose ganglia and in thoracic dorsal root ganglia (DRGs). In the medulla, cholinergic preganglionic parasympathetic neurons in the DMX were virtually the only targets of chemosensory information from the PMV wall. H129-infected terminal appositions were identified on H129-infected somata and dendrites in the DMX, and on H129-infected DMX dendrites that extend into the NTS. Sensory transmission via vagal and possibly spinal routes from the PMV wall therefore reaches DMX neurons via axo-somatic appositions in the DMX and axo-dendritic appositions in the NTS. However, the dearth of H129-infected NTS neurons indicates that sensory information from the PMV wall terminates on DMX neurons without engaging NTS neurons. These previously underappreciated direct sensory routes into the DMX enable a vago-vagal and possibly spino-vagal reflexes that can directly influence visceral function.

Highlights

  • The superior mesenteric vein (SMV), gastric vein (GV), and splenic vein (SV) form the venous system that provides the liver with nutrient-rich blood from the intestines, together with blood from the gallbladder, spleen, and parts of the pancreas and stomach

  • Saberi et al (2008) have shown that hepatic portal vein (HPV) wall sensory endings extend into the SMV, thereby revealing that a key peripheral glucosensor is present in the walls of the hepatic portal and superior mesenteric veins (PMV) and transmits its information to the brain

  • Summary and conclusions Our results show that the vast majority of medullary neurons that are the first to receive chemosensory information from the PMV wall are preganglionic parasympathetic neurons in the DMX

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Summary

Introduction

The superior mesenteric vein (SMV), gastric vein (GV), and splenic vein (SV) form the venous system that provides the liver with nutrient-rich blood from the intestines, together with blood from the gallbladder, spleen, and parts of the pancreas and stomach. Hormones, and ions have been infused into the HPV and their subsequent effects ascribed to spinal and vagal sensory nerve endings in the HPV wall, which transmits this information to the brain This mixture of sensory information includes: glucose (Niijima, 1969, 1989; Donovan et al, 1991a,b, 1994; Hamilton-Wessler et al, 1994; Niijima, 1996; Hevener et al, 1997), lipids (Randich et al, 2001; Cox et al, 2004), proteins (Mithieux et al, 2005; Duraffourd et al, 2012), amino acids (Niijima and Meguid, 1995), and ions (Morita et al, 1990; Bourque, 2008; Morita and Abe, 2011), leptin (Shiraishi et al, 1999), GLP-1 (Nakabayashi et al, 1996; Vahl et al, 2007), and CCK (Horn and Friedman, 2004). Saberi et al (2008) have shown that HPV wall sensory endings extend into the SMV, thereby revealing that a key peripheral glucosensor is present in the walls of the hepatic portal and superior mesenteric veins (PMV) and transmits its information to the brain

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