Efferent projection from the bed nucleus of the stria terminalis suppresses activity of taste-responsive neurons in the hamster parabrachial nuclei

Abstract

Although the reciprocal projections between the bed nucleus of the stria terminalis (BNST) and the gustatory parabrachial nuclei (PbN) have been demonstrated neuroanatomically, there is no direct evidence showing that the projections from the PbN to the BNST carry taste information or that descending inputs from the BNST to the PbN modulate the activity of PbN gustatory neurons. A recent electrophysiological study has demonstrated that the BNST exerts modulatory influence on taste neurons in the nucleus of the solitary tract (NST), suggesting that the BNST may also modulate the activity of taste neurons in the PbN. In the present study, we recorded from 117 taste-responsive neurons in the PbN and examined their responsiveness to electrical stimulation of the BNST bilaterally. Thirteen neurons (11.1%) were antidromically invaded from the BNST, mostly from the ipsilateral side (12 cells), indicating that a subset of taste neurons in the PbN project their axons to the BNST. The BNST stimulation induced orthodromic responses on most of the PbN neurons: 115 out of 117 (98.3%), including all BNST projection units. This descending modulation on the PbN gustatory neurons was exclusively inhibitory. We also confirmed that activation of this efferent inhibitory projection from the BNST reduces taste responses of PbN neurons in all units tested. The BNST is part of the neural circuits that involve stress-associated feeding behavior. It is also known that brain stem gustatory nuclei, including the PbN, are associated with feeding behavior. Therefore, this neural substrate may be important in the stress-elicited alteration in ingestive behavior.

Modulation of activity of gustatory neurons in the hamster parabrachial nuclei by electrical stimulation of the ventroposteromedial nucleus of the thalamus

“…The overall baseline activity of the 114 taste-responsive PbN neurons recorded in the present study varied from 0 to 15.80 imp/s, with a mean of 3.58 Ϯ 0.34 imp/s. This mean firing rate was similar to that recorded previously in the PbN (e.g., 3.70 Ϯ 0.27 imp/s, t ϭ 0.266, df ϭ 229, P ϭ 0.791) (34) and was significantly higher than that recorded in the NST in our previous experiments (e.g., 2.12 Ϯ 0.27 imp/s, t ϭ 3.350, df ϭ 221, P Ͻ 0.001) (36).…”

“…The anterior-posterior distribution of the recording marks extended rostrally from the level at which LC is first apparent and caudally to the appearance of the accessory trigeminal nucleus. The locations of the recording sites in the PbN were similar to those of our laboratory's previous recordings (34,35).…”

“…The taste stimulation was repeated throughout the test period as follows: 2 s of taste solution delivery followed by a 20-s pause and then delivery of a 3-s distilled water rinse. This 25-s stimulus sequence was repeated at 10-s intervals until the end of the session to create a PSTH, as in our previous study (34). This procedure is especially useful for testing units that exhibit no or low spontaneous firing and that receive inhibitory input from the VPMpc, because this protocol lets us determine whether these neurons receive inhibitory input from the VPMpc.…”

“…From the NST, ascending gustatory fibers project to third-order taste cells within the PbN of the pons (7,22,42,46,(53)(54)(55)87). Two separate routes carry taste information from the PbN further to the forebrain taste areas and cortex: the ventral forebrain pathway that involves the central nucleus of the amygdala (CeA), the lateral hypothalamus (LH), the bed nucleus of the stria terminalis (BNST), the substantia innominata (3,12,16,21,31,33,34,41,47,63,64,71); and the thalamocortical pathway that is characterized by the involvement of the bilateral VPMpc, which, in turn, carries taste information to the gustatory cortex (GC) (5,25,45,48,51).The PbN is a critical neural substrate for a number of taste-guided behavioral or physiological responses, including conditioned taste aversion learning (CTA), gastric distension, and sodium appetite. It has been demonstrated that a subpopulation of neurons in the PbN can be coactivated by both gustatory and vagal (hepatic) stimulation (26) or gustatory and gastric distension (1), indicating that the PbN is the locus of integration for gustatory and other vagal afferent inputs.…”

“…The involvement of the forebrain gustatory nuclei in the ventral forebrain pathway, e.g., LH, CeA, BNST, and GC, on modulation of activity of PbN taste neurons has been well documented (10,11,34,35,39,40). However, the possibility of the involvement of the VPMpc in the thalamocortical pathway on modulation of activity of taste neurons in the PbN has never been investigated.…”