Impact of antral mechanoreceptor activation on the vago-vagal reflex in the rat: functional zonation of responses

Abstract

1. Activation of gastric sensory afferents alters gastric motor and secretory function via the gastric vago-vagal reflex. In this report, we investigated in the rat the impact of gastric mechanoreceptor activation on the brain stem components of the reflex, which are located in the dorsal vagal complex (DVC), i.e. the nucleus of the solitary tract (NTS) and the subjacent dorsal motor nucleus (DMN). 2. In our extracellular recordings of single-cell activity in the DVC, we observed a relation between the response to antral distention and the location of the cell in the DVC. Specifically, cells that were excited by antral distention (ON cells) were located dorsal to those that were inhibited (OFF cells) by the same stimulus (mean depth = 536 +/- 15 and 627 +/- 14 microns for ON and OFF cells, respectively). 3. For a subset of DVC cells, the location was marked by ionophoretic ejection of Pontamine Blue from the recording barrel. Histological analysis indicated that ON cells were located in the NTS, and OFF cells were located in the ventral NTS or within the boundaries of the DMN. Together, these data led to the hypothesis that ON and OFF cells are functionally different groups of neurones, i.e. ON cells may be NTS neurones, and OFF cells may be DMN neurones. We tested this directly by employing both an intragastric balloon and a non-traumatic vagal stimulating electrode to determine whether inflation-related cells were NTS or DMN cells via orthodromic and antidromic activation, respectively. 4. Almost all ON cells (12/13) were orthodromically activated by vagal stimulation, i.e. they were NTS neurones. One ON cell was antidromically activated, and therefore was a DMN neurone. Of the twenty-eight OFF cells that were encountered, ten were classified as NTS neurones because they were orthodromically inhibited by vagal stimulation. The remaining eighteen OFF cells were orthodromically inhibited and antidromically activated (i.e. DMN neurones). Thus, our results support the hypothesis that ON and OFF cells can be functionally distinct populations of neurones, in that almost all ON cells are NTS cells and approximately 2/3 of the OFF cells are DMN neurones. 5. The response to mechanoreceptor activation was different for NTS and DMN neurones. NTS cells were activated (55%) or inhibited (45%) by balloon distention of the stomach, whereas DMN cells were almost exclusively inhibited (95%) by this stimulus. This information provides insight into the organization of excitatory and inhibitory connections of the brain stem components that mediate gastric vago-vagal reflexes.