Cheng-Shu Li

GABA-mediated corticofugal inhibition of taste-responsive neurons in the nucleus of the solitary tract.

The nucleus of the solitary tract (NST) receives descending connections from several forebrain targets of the gustatory system, including the insular cortex. Many taste-responsive cells in the NST are inhibited by gamma-aminobutyric acid (GABA). In the present study, we investigated the effects of cortical stimulation on the activity of gustatory neurons in the NST. Multibarrel glass micropipettes were used to record the activity of NST neurons extracellularly and to apply the GABA(A) antagonist bicuculline methiodide (BICM) into the vicinity of the cell. Taste stimuli were 0.032 M sucrose (S), 0.032 M NaCl (N), 0.00032 M citric acid (H), and 0.032 M quinine hydrochloride (Q), presented to the anterior tongue. Each of 50 NST cells was classified as S-, N-, H-, or Q-best on the basis of its response to chemical stimulation of the tongue. The ipsilateral insular cortex was stimulated both electrically (0.5 mA, 100 Hz, 0.2 ms) and chemically (10 mM DL-homocysteic acid, DLH), while the spontaneous activity of each NST cell was recorded. The baseline activity of 34% of the cells (n=17) was modulated by cortical stimulation: eight cells were inhibited and nine were excited. BICM microinjected into the NST blocked the cortical-induced inhibition but had no effect on the excitatory response. Although the excitatory effects were distributed across S-, N-, and H-best neurons, the inhibitory effects of cortical stimulation were significantly more common in N-best cells. These data suggest that corticofugal input to the NST may differentially inhibit gustatory afferent activity through GABAergic mechanisms.

Opioid modulation of taste responses in the nucleus of the solitary tract.

Gustatory processing within the medulla is modulated by a number of physiologic and experiential factors. Several neurotransmitters, including excitatory amino acids, GABA, and substance P, are involved in synaptic processing within the rostral portion of the nucleus of the solitary tract (NST). Endogenous opiates have been implicated in the regulation of feeding behavior and in taste palatability and gustatory responses in the parabrachial nuclei are reduced by systemic morphine. In the present experiments, extracellular recording of neuronal activity within the NST in response to taste input was combined with local microinjection of met-enkephalin (Met-ENK) and naltrexone (NLTX) to determine the effect of these agents on gustatory activity. The anterior tongue was stimulated with anodal current pulses to determine the time course of drug action (n=85 cells) and with prototypical taste stimuli (0.032 M sucrose, NaCl, and quinine hydrochloride, and 0.0032 M citric acid) to investigate the effects of these opioid compounds on taste-evoked responses (n=80 cells). Among these 165 taste-responsive neurons in the NST, the activity of 39 (23.6%) was suppressed by Met-ENK. These effects were dose-dependent and blockable by NLTX, which alone was without effect, suggesting that opiates do not maintain a tonic inhibitory influence. Immunohistochemical experiments demonstrated both micro - and delta-opioid receptors within the gustatory portion of the NST; previous studies had shown numerous fiber terminals containing Met-ENK. These data suggest that endogenous opiates play an inhibitory role in gustatory processing within the medulla.

Gustatory Neural Circuitry in the Hamster Brain Stem

The nucleus of the solitary tract (NST) and the parabrachial nuclei (PbN) are the first and second central relays for the taste pathway, respectively. Taste neurons in the NST project to the PbN, which further transmits taste information to the rostral taste centers. Nevertheless, details of the neural connections among the brain stem gustatory nuclei are obscure. Here, we investigated these relationships in the hamster brain stem. Three electrode assemblies were used to record the activity of taste neurons extracellularly and then to electrically stimulate these same areas in the order: left PbN, right PbN, and right NST. A fourth electrode, a glass micropipette, was used to record from gustatory cells in the left NST. Results showed extensive bilateral communication between brain stem nuclei at the same level: 1) 10% of 96 NST neurons projected to the contralateral NST and 58% received synaptic input from the contralateral NST; and 2) 12% of 43 PbN neurons projected to the contralateral PbN and 21% received synaptic input from the contralateral PbN. Results also showed extensive communication between levels: 1) as expected, the majority of 119 NST neurons, 82%, projected to the ipsilateral PbN, but 85% of the 20 NST neurons tested received synaptic input from the ipsilateral PbN, as did 59% of 22 NST neurons that did not project to the PbN; and 2) although few, 3%, of 119 NST cells projected to the contralateral PbN and 38% received synaptic input from the contralateral PbN. These results demonstrated that taste neurons in the NST not only project to, but also receive descending input from the bilateral PbN and that gustatory neurons in the NST and PbN also communicate with the corresponding nucleus on the contralateral side.

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

The parvicellular part of the ventroposteromedial nucleus of the thalamus (VPMpc) is positioned at the key site between the gustatory parabrachial nuclei (PbN) and the gustatory cortex for relaying and processing gustatory information via the thalamocortical pathway. Although neuroanatomical and electrophysiological studies have provided information regarding the gustatory projection from PbN to VPMpc, the exact relationship between PbN and VPMpc, especially the efferent projection involving VPMpc to PbN, is obscure. Here we investigated the reciprocal connection between these two gustatory relays in urethane-anesthetized hamsters. We recorded from 114 taste-responsive neurons in the PbN and examined their responsiveness to electrical stimulation of the VPMpc bilaterally. Stimulation of either or both of the ipsilateral or contralateral VPMpc antidromically activated 109 gustatory PbN neurons. Seventy-two PbN neurons were antidromically activated after stimulation of both sides of the VPMpc, indicating that taste neurons in the PbN project heavily to the bilateral VPMpc. Stimulation of VPMpc also orthodromically activated 110 of PbN neurons, including 106 VPMpc projection neurons. Seventy-eight neurons were orthodromically activated bilaterally. Among orthodromic activations of the PbN cells, the inhibitory response was the dominant response; 106 cells were inhibited, including 10 neurons that were also excited contralaterally, indicating that taste neurons in the PbN are subject to strong inhibitory control from VPMpc. Moreover, stimulation of VPMpc altered taste responses of the neurons in the PbN, indicating that VPMpc modulates taste responses of PbN neurons. These results may provide functional insight of neural circuitry for taste processing and modulation involving these two nuclei.