Search

Gustatory responses in the brain stem are modifiable by several physiological factors, including blood insulin and glucose, intraduodenal lipids, gastric distension, and learning, although the neural substrates for these modulatory effects are not known. Stimulation of the lateral hypothalamus (LH) produces increases in food intake and alterations in taste preference behavior, whereas damage to this area has opposite effects. In the present study, we investigated the effects of LH stimulation on the neural activity of taste-responsive cells in the nucleus of the solitary tract (NST) of the hamster. Bipolar stimulating electrodes were bilaterally implanted in the LH, and the responses of 99 neurons in the NST, which were first characterized for their taste sensitivities, were tested for their response to both ipsilateral and contralateral LH stimulation. Half of the taste-responsive cells in the NST (49/99) were modulated by LH stimulation. Contralateral stimulation was more often effective (41 cells) than ipsilateral (13 cells) and always excitatory; 10 cells were excited bilaterally. Six cells were inhibited by ipsilateral stimulation. A subset of these cells ( n = 13) was examined for the effects of microinjection of dl-homocysteic acid (DLH), a glutamate receptor agonist, into the LH. The effects of electrical stimulation were completely mimicked by DLH, indicating that cell somata in and around the LH are responsible for these effects. Other cells ( n = 14) were tested for the effects of electrical stimulation of the LH on the responses to stimulation of the tongue with 0.032 M sucrose, NaCl, and quinine hydrochloride, and 0.0032 M citric acid. Responses to taste stimuli were more than doubled by the excitatory influence of the LH. These data show that the LH, in addition to its role in feeding and metabolism, exerts descending control over the processing of gustatory information through the brain stem.

The parabrachial nuclei (PbN), the second central relay for the gustatory pathway, transfers taste information to various forebrain gustatory nuclei and to the gustatory cortex. The nucleus accumbens is one of the critical neural substrates of the reward system, and the nucleus accumbens shell region (NAcSh) is associated with feeding behavior. Taste-evoked neuronal responses of PbN neurons are modulated by descending projections from the gustatory nuclei in the forebrain. In the present study, we investigated whether taste-responsive neurons in the PbN project to the NAcSh and whether pontine gustatory neurons are subject to modulatory influence from the NAcSh in urethane-anesthetized hamsters. Extracellular single-unit activity was recorded in the PbN, and taste responses were confirmed by the delivery of 32 mM sucrose, NaCl, quinine hydrochloride, and 3.2 mM citric acid to the anterior tongue. The NAcSh was then stimulated (0.5 ms, ≤100 μA) bilaterally using concentric bipolar stimulating electrodes. A total of 98 taste neurons were recorded from the PbN. Eighteen neurons were antidromically invaded from the NAcSh, mostly the ipsilateral NAcSh ( n = 16). Stimulation of the ipsilateral and contralateral NAcSh suppressed the neuronal activity of 88 and 55 neurons, respectively; 52 cells were affected bilaterally. In a subset of pontine neurons tested, electrical stimulation of the NAcSh during taste stimulation also suppressed taste-evoked neuronal firing. These results demonstrated that taste-responsive neurons in the PbN not only project to the NAcSh but also are under substantial descending inhibitory influence from the bilateral NAcSh.

The lateral hypothalamus (LH) and the central nucleus of the amygdala (CeA) exert an influence on ingestive behavior and are reciprocally connected to gustatory and viscerosensory areas, including the nucleus of the solitary tract (NST) and the parabrachial nuclei (PbN). We investigated the effects of LH and CeA stimulation on the activity of 101 taste-responsive neurons in the hamster PbN. Eighty three of these neurons were antidromically activated by stimulation of these sites; 57 were antidromically driven by both. Of these 83 neurons, 21 were also orthodromically activated—8 by the CeA and 3 by the LH. Additional neurons were excited ( n = 5) or inhibited ( n = 8) by these forebrain nuclei but not antidromically activated. Taste stimuli were: 0.032 M sucrose, 0.032 M sodium chloride (NaCl), 0.032 M quinine hydrochloride (QHCl), and 0.0032 M citric acid. Among the 34 orthodromically activated neurons, more sucrose-best neurons were excited than inhibited, whereas the opposite occurred for citric-acid- and QHCl-best cells. Neurons inhibited by the forebrain responded significantly more strongly to citric acid and QHCl than cells excited by these sites. The effects of electrical stimulation were mimicked by microinjection of dl-homocysteic acid, indicating that cells at these forebrain sites were responsible for these effects. These data demonstrate that many individual PbN gustatory neurons project to both the LH and CeA and that these areas modulate the gustatory activity of a subset of PbN neurons. This neural substrate is likely involved in the modulation of taste activity by physiological and experiential factors.

Previous studies have shown a modulatory influence of forebrain gustatory areas, such as the gustatory cortex and lateral hypothalamus, on the activity of taste-responsive cells in the nucleus of the solitary tract (NST). The central nucleus of the amygdala (CeA), which receives gustatory afferent information, also exerts descending control over taste neurons in the parabrachial nuclei (PbN) of the pons. The present studies were designed to investigate the role of descending amgydaloid projections to the NST in the modulation of gustatory activity. Extracellular action potentials were recorded from 109 taste-responsive cells in the NST of urethan-anesthetized hamsters and analyzed for a change in excitability following electrical and chemical stimulation of the CeA. Electrical stimulation of the CeA orthodromically modulated 36 of 109 (33.0%) taste-responsive NST cells. An excitatory response was observed in 33 (30.28%) cells. An initial decrease in excitability to electrical stimulation of the CeA, suggestive of postsynaptic inhibition, was observed in three (2.75%) NST taste cells. NST cells modulated by the CeA were significantly less responsive to taste stimuli than cells that were not. Many of these cells were under the modulatory influence of the contralateral CeA (28/36 = 77.8%) as well as the ipsilateral (22/36 = 61.1%); 14 (38.9%) were excited bilaterally. Latencies for excitation were longer after ipsilateral than after contralateral CeA stimulation. Microinjection of dl-homocysteic acid (DLH) into the CeA mimicked the effect of electrical stimulation on each of the nine cells tested: DLH excited eight and inhibited one of these electrically activated NST cells. Application of subthreshold electrical stimulation to the CeA during taste trials increased the taste responses of every CeA-responsive NST cell ( n = 7) tested with this protocol. These effects would enhance taste discriminability by increasing the signal-to-noise ratio of taste-evoked activity.

Li, Cheng-Shu and David V. Smith. Glutamate receptor antagonists block gustatory afferent input to the nucleus of the solitary tract. J. Neurophysiol. 77: 1514–1525, 1997. The effects of excitatory amino acid (EAA) receptor antagonists in blocking the synaptic transmission between gustatory fibers of the chorda tympani (CT) nerve and taste-responsive neurons within the nucleus of the solitary tract (NST) were examined electrophysiologically in urethan-anesthetized hamsters. Single neurons in the NST were recorded extracellularly and drugs were microinjected into the vicinity of the cell with the use of a multibarrel pipette assembly. The activity of each cell was recorded in response to lingual stimulation with 0.032 M NaCl, 0.032 M sucrose, 0.0032 M citric acid, 0.032 M quinine hydrochloride, and/or 25-μA anodal current pulses. Once a cell was identified as a taste-responsive neuron, one or more EAA receptor antagonists were administered by microinjection. Approximately 27 nl of 50 mM kynurenic acid (KYN), a broad-spectrum EAA receptor antagonist; 0.5 or 2.0 mM dl-2-amino-5-phosphonovalerate (APV), an N-methyl-d-aspartate (NMDA) receptor antagonist; 0.05 or 0.5 mM 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), an α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)/kainate receptor antagonist; or phosphate-buffered physiological saline was applied to the neuron. Responses to chemical stimulation of the anterior tongue were obtained before and after drug administration and again after recovery; responses to anodal current stimulation (0.1 Hz) were obtained continually throughout the drug administration protocol. Microinjection of KYN completely and reversibly abolished responses elicited by both anodal current and chemical stimulation of the anterior tongue. The excitatory responses of cells in the NST to chemical and electrical stimulation of the anterior tongue were also completely and reversibly blocked by CNQX, implicating the involvement of an AMPA/kainate receptor. Microinjection of APV was generally less effective and partially reduced the responses of some taste-responsive NST cells to chemical stimulation of the anterior tongue. There were no effects following microinjection of a 27-nl bolus of phosphate-buffered saline. None of these EAA receptor antagonists had a differential effect on responses to different taste stimuli. The responses to all tastants were completely blocked by both KYN and CNQX; there was no apparent relationship between the response to any particular tastant and the limited effects of APV. These data implicate glutamate as an excitatory neurotransmitter between CT gustatory fibers and taste-responsive NST cells and suggest that it acts primarily on AMPA/kainate receptors, with some contribution from NMDA receptors. This conclusion is strengthened by other data obtained from in vitro slice preparations, which show that responses of cells in the rostral NST to solitary tract stimulation are blocked by both NMDA and AMPA/kainate receptor antagonists.