Low-dose furosemide modulates taste responses in the nucleus of the solitary tract of the rat

2004 ◽  
Vol 287 (4) ◽  
pp. R706-R714 ◽  
Author(s):  
Young K. Cho ◽  
Michael E. Smith ◽  
Ralph Norgren

Taste-evoked neural responses in the nucleus of the solitary tract (NST) are subject to both excitatory and inhibitory modulation by physiological conditions that influence ingestion. Treatments that induce sodium appetite predominantly reduce NST gustatory responsiveness to sapid stimuli. When sodium appetite is aroused with 10 mg of the diuretic furosemide (Furo), however, NST gustatory neurons exhibit an enhanced responsiveness to NaCl. In addition to inducing a sodium appetite, 10 mg Furo supports a conditioned taste aversion (CTA). A lower, 2-mg dose of Furo induces an equivalent sodium appetite, but not a CTA. To determine whether the anomalous electrophysiological results reflected the adverse effects of the 10-mg dose, we replicated the original experiment but instead used 2 mg of Furo. In chronically prepared, lightly anesthetized rats, the responses of 49 single NST neurons to 12 taste stimuli were recorded after subcutaneous injections of either 2 mg Furo or saline. There was no effect of treatment on NST neural responses to the four standard taste stimuli. In the NaCl concentration series, however, 2 mg Furo evoked significantly higher responses to the two highest concentrations of NaCl. There was no effect of treatment in the sucrose concentration series. Thus, unlike other methods that induce a sodium appetite, Furo increases NST neural responsiveness to NaCl. At least as far as the first central relay, sodium appetite apparently does not depend on specific changes in the sensory neural code for taste.

1997 ◽  
Vol 273 (4) ◽  
pp. R1381-R1391 ◽  
Author(s):  
Ryoi Tamura ◽  
Ralph Norgren

Furosemide sodium depletions were induced repeatedly to determine the effects on gustatory neural responses in the nucleus of the solitary tract (NST) of chronically prepared, but lightly anesthetized, rats. Sodium-replete and sodium-deplete conditions were alternated four times in each rat. When rats were under depleted conditions, the responses to NaCl were significantly greater than in sodium-replete conditions. This effect was attributable primarily to an increase in the magnitude of response of those neurons that responded better to NaCl than to the other standard stimuli (sucrose, citric acid, and quinine hydrochloride). In addition, the largest change in responsiveness of the NaCl-best neurons occurred during the third and fourth sodium depletions. These results are essentially opposite to those reported for NST neurons when sodium appetite is induced by dietary sodium restriction. This suggests that the coding of intensity in the gustatory system is dependent not only on the animal’s deprivation condition, but also the method through which the deprivation is produced.


2003 ◽  
Vol 284 (4) ◽  
pp. R1108-R1118 ◽  
Author(s):  
R. Tamura ◽  
R. Norgren

Activation of the renin-angiotensin system in the brain is considered important in the arousal and expression of sodium appetite. To clarify the effects of directly activating this hormonal cascade, taste neurons in the nucleus of the solitary tract of rats were tested with a battery of sapid stimuli after intracerebroventricular injection of renin or its vehicle. The rats were chronically prepared but lightly anesthetized during the recording procedure. Eighty-five taste neurons were tested: 46 after renin injections and 39 after vehicle. Neural activity was counted for 5.0-s periods without stimulation (spontaneous) and during stimulation with water and sapid chemicals. The averaged responses to each of the standard stimuli (0.1 M NaCl, 0.3 M sucrose, 0.01 M citric acid, and 0.01 M quinine hydrochloride) did not differ significantly between the two conditions. When the rats were tested with a concentration range of NaCl, however, after renin the average responses to the hypertonic 0.3 and 1.0 M stimuli were reduced to 74 and 70%, respectively, compared with those after vehicle injections. A similar tendency was evident for the subsample of neurons that responded best to NaCl, but the effect was smaller. These data are consistent with, but not as dramatic as, those reported after dietary-induced sodium appetite.


1979 ◽  
Vol 73 (5) ◽  
pp. 569-594 ◽  
Author(s):  
R J Contreras ◽  
M Frank

The effects of sodium deprivation for 10 d, a period sufficient to induce sodium appetite, on gustatory nerve discharges in rats were determined. Chorda tympani responses to concentration series of sodium chloride, sucrose, hydrochloric acid, and quinine hydrochloride were recorded and analyzed without the experimenter knowing the animal's deprivation condition. After deprivation, both whole nerve and single nerve fiber responses to sodium chloride were smaller; NaCl-best fibers, those more responsive to sodium chloride than to sucrose, hydrochloric acid, or quinine, were most affected. Thresholds had not changed; however, slopes of the stimulus-response functions for sodium chloride were lowered. Comparable changes in responses to the other stimuli did not occur. These results were discussed with respect to a possible relationship between changes in sodium chloride responsivity and changes in sodium intake, differences between methods of inducing sodium appetite, coding of taste quality and intensity, and mechanisms which might effect the responsivity change.


2003 ◽  
Vol 90 (2) ◽  
pp. 911-923 ◽  
Author(s):  
Christian H. Lemon ◽  
Toshiaki Imoto ◽  
David V. Smith

We examined the effect of the sweet transduction blocker gurmarin on taste responses recorded from neurons in the rat solitary nucleus (NST) to determine how gurmarin sensitivity is distributed across neuronal type. Initially, responses evoked by washing the anterior tongue and palate with 0.5 M sucrose, 0.1 M NaCl, 0.01 M HCl, and 0.01 M quinine-HCl were recorded from 35 neurons. For some cells, responses to a sucrose concentration series (0.01–1.0 M) or an array of sweet-tasting compounds were also measured. Gurmarin (10 μg/ml, 2–4 ml) was then applied to the tongue and palate. Stimuli were reapplied after 10–15 min. Neurons were segregated into groups based on similarities among their initial response profiles using hierarchical cluster analysis (HCA). Results indicated that sucrose responses recorded from neurons representative of each HCA-defined class were suppressed by gurmarin. However, a disproportionate percentage of cells in each group displayed sucrose responses that were substantially attenuated after gurmarin treatment. Postgurmarin sucrose responses recorded from neurons that composed 57% of class S, 40% of class N, and 33% of class H were suppressed by ≥50% relative to control. On average, attenuation was statistically significant only in class S and N neurons. Although the magnitude of gurmarin-induced response suppression did not differ across sucrose concentration, responses to different sweet-tasting compounds were differentially affected. Responses to NaCl, HCl, or quinine were not suppressed by gurmarin. Results suggest that information from gurmarin-sensitive and -insensitive receptor processes converges onto single NST neurons.


1995 ◽  
Vol 269 (3) ◽  
pp. R647-R661 ◽  
Author(s):  
K. Nakamura ◽  
R. Norgren

The activity of single taste neurons was recorded from the nucleus of the solitary tract before (n = 41) and after (n = 58) awake, behaving rats were switched to a sodium-free diet. During sodium deprivation, the spontaneous activity of the neurons increased (142%), but responses to water and sapid stimuli decreased. For all neurons in the sample, the mean response to water decreased to 72% of its predeprivation level, NaCl dropped to 53%, sucrose to 41%, citric acid to 68%, and quinine HCl to 84%. Despite the drop in magnitude, the response profiles of the taste neurons were not changed by the dietary condition. In the Na-replete state, 61% of the activity elicited by NaCl occurred in NaCl-best cells and 33% in sucrose-best neurons. In the depleted state, these values were 60 and 26%, respectively. Nevertheless, at the highest concentrations tested, deprivation did alter the relative responsiveness of the gustatory neurons to sucrose and NaCl in specific categories of neurons. Compared with acute preparations, dietary sodium deprivation in awake, behaving rats produced a more general reduction in the gustatory responses of neurons in the nucleus of the solitary tract. The largest reductions in elicited activity occurred for the "best stimulus" of a particular neuron, thus leading to smaller differences in response magnitude across stimuli, particularly at the highest concentrations tested.


2006 ◽  
Vol 96 (4) ◽  
pp. 1877-1886 ◽  
Author(s):  
Christopher T. Simons ◽  
Yves Boucher ◽  
Mirela Iodi Carstens ◽  
E. Carstens

This study investigated effects of nicotine applied to the tongue surface on responses of gustatory neurons in the nucleus of the solitary tract (NTS) in rats. In pentobarbital-anesthetized rats, single-unit recordings were made from NTS units responsive to one or more tastants (sucrose, NaCl, citric acid, monosodium glutamate, quinine). Application of nicotine (0.87, 8.7, or 600 mM) excited gustatory NTS units and significantly attenuated NTS unit responses to their preferred tastant in a dose-dependent manner. The depressant effect of nicotine was equivalent regardless of which tastant best excited the NTS unit. Nicotinic excitation of NTS units and depression of their tastant-evoked responses were both significantly attenuated by the nicotinic antagonist mecamylamine, which itself did not excite NTS units. In rats with bilateral trigeminal ganglionectomy, nicotine still excited nearly all NTS units but no longer depressed tastant-evoked responses. Nicotine did not elicit plasma extravasation when applied to the tongue. The results indicate that nicotine directly excites NTS units by gustatory nerves and inhibits their tastant-evoked responses by a nicotinic acetylcholine receptor-mediated excitation of trigeminal afferents that inhibit NTS units centrally.


1991 ◽  
Vol 66 (4) ◽  
pp. 1232-1248 ◽  
Author(s):  
K. Nakamura ◽  
R. Norgren

1. The activity of 117 single neurons was recorded in the rostral nucleus of the solitary tract (NST) and tested with each of four standard chemical stimuli [sucrose, NaCl, citric acid, and quinine HCl (QHCl)] and distilled water in awake, behaving rats. In 101 of these neurons, at least one sapid stimulus elicited a significant taste response. The mean spontaneous rate of the taste neurons was 4.1 +/- 5.8 (SD) spike/s. The mean response magnitudes were as follows: sucrose, 10.6 +/- 11.7; NaCl, 8.6 +/- 14.6; citric acid, 6.2 +/- 7.8; and QHCl, 2.4 +/- 6.6 spikes/s. 2. On the basis of their largest response, 42 taste neurons were classified as sucrose-best, 25 as NaCl-best, 30 as citric acid-best, and 4 as QHCl-best. The mean spontaneous rates for these categories were 4.9 +/- 6.2 for sucrose-best cells, 5.8 +/- 7.4 for NaCl-best, 1.6 +/- 2.0 for citric acid-best, and 5.8 +/- 6.0 spikes/s for QHCl-best. The spontaneous rate of the citric acid-best neurons was significantly lower than that of the other categories. 3. At the standard concentrations, 45 taste cells (44.6%) responded significantly to only one of the gustatory stimuli. Of the 30 acid-best neurons, 23 (76.7%) responded only to citric acid. For sucrose-best cells, specific sensitivity was less common (18/42, 42.9%), and for NaCl-best neurons, it was relatively uncommon (3/25, 12%). One of the 4 QHCl-best neurons was specific. In a concentration series, more than one-half of the 19 specific neurons tested responded to only one chemical at any strength. 4. The mean entropy for the excitatory responses of all gustatory neurons was 0.60. Citric acid-best cells showed the least breadth of responsiveness (0.49), sucrose-best cells were somewhat broader (0.56), but NaCl-best and QHCl-best cells were considerably less selective (0.77 and 0.79, respectively). Inhibition was observed infrequently and never reached the criterion for significance. 5. In the hierarchical cluster analysis, the four largest clusters segregated neurons primarily by best-stimulus category. The major exception to this was a group of sucrose-best neurons that also responded to NaCl and were grouped with the NaCl-best neurons. In a two-dimensional space, the specific taste neurons, those that responded to only one of the four standard sapid stimuli, remained in well-separated groups. These specific groups, however, were joined in a ring-like formation by other neurons that responded to more than one of the sapid stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)


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