Gastric distension modulates hypothalamic neurons via a sympathetic afferent path through the mesencephalic periaqueductal gray

Abstract

The effects of gastric distension on extracellulary recorded single neuronal activity in the lateral hypothalamuslateral preoptic area-medial forebrain bundle (LPA-LH-MFB), other areas of the hypothalamus, mesencephalic periaqueductal gray (PAG), and other areas associated with the mesencephalic reticular formation were determined in the anesthetized rat Gastric distension was produced by filling a gastric balloon with water using a calibrated infusion pump. Experimental conditions were based on previous studies that simulated gastric distension during fluid consumption In the rat. The effects of stomach distension using water at body temperature and room temperature were compared. Neurons in both the hypothalamus and mesencephalon were modulated by gastric distension. Hypothalamic neurone exhibited responses associated with gastric distension and exhibited interactions between distension and temperature stimulation of the stomach. Neurons in the mesencephalic periaqueductal gray (PAG) and associated reticular formation also were modulated by these gastric stimuli. When the PAG was electrically stimulated, similar responses to gastric distension and PAG stimulation were observed for hypothalamic neurons. The effects of gastric distension on hypothalamic neurons were reduced or eliminated when the PAG stimulating electrode site was destroyed by electrocoagulation. In addition, the microiontophoretic application of horseradish peroxidase at hypothalamic neuronal recording sites where gastric distension effects were observed resulted in the retrograde labeling of neurons in the PAG. These gastric stimulation-induced effects on hypothalamic and mesencephallc neuronal activity were attenuated but were not permanently eliminated by bilateral cervical vagotomy. However, these effects were significantly reduced or eliminated by bilateral transection of the cervical sympathetic chain or spinal transection at the first cervical level. Because the filling of balloons placed into the abdominal cavity close to the stomach had no similar effects on neural activity, these results can be attributed primarily to the activation of gastric mechano- and temperature-sensitive receptors. These results indicate that the effects of gastric temperature/distension stimulation under these conditions are mediated to a large degree by sympathetic afferents. The PAG is clearly involved as one of the mesencephalic relays for gastric afferent input to the hypothalamus.