scholarly journals Bursting by taste-responsive cells in the rodent brain stem

2015 ◽  
Vol 113 (7) ◽  
pp. 2434-2446
Author(s):  
John-Paul Baird ◽  
Michael G. Tordoff ◽  
Stuart A. McCaughey

Neurons that fire in bursts have been well-characterized in vision and other neural systems, but not in taste systems. We therefore examined whether brain stem gustatory neurons fire in bursts during spontaneous activity and, if so, whether such cells differ from nonbursting cells in other characteristics. We looked at neurons in the nucleus of the solitary tract (NST) of C57BL/6ByJ (B6) and 129P3/J (129) mice, and in the NST and parabrachial nucleus (PBN) of Sprague-Dawley rats. Many NST cells fired frequently with short intervals characteristic of bursting, and such neurons differed from others in their responsiveness to taste compounds. In B6 mice and rats, there was a significant positive correlation between the prevalence of short-interval firing and the net spikes evoked by application of NaCl. In contrast, in 129 mice the prevalence of short intervals was positively correlated with the size of sucrose responses. We also compared breadth-of-tuning measures based on counting either all spikes or only those following short intervals, and we found narrower tuning for the latter in the NST of B6 mice and rats. There was little evidence of spontaneous bursting in the rat PBN, and firing patterns in this nucleus were not related to the size of taste-evoked responses. We suggest that bursting may be a strategy employed by the NST to amplify the postsynaptic impact of particular taste stimuli, depending on an animal's needs. Another function may be to sharpen breadth-of-tuning and thus enhance the contrast between stimuli of different taste qualities.

Author(s):  
Shams M. Ghoneim ◽  
Frank M. Faraci ◽  
Gary L. Baumbach

The area postrema is a circumventricular organ in the brain stem and is one of the regions in the brain that lacks a fully functional blood-brain barrier. Recently, we found that disruption of the microcirculation during acute hypertension is greater in area postrema than in the adjacent brain stem. In contrast, hyperosmolar disruption of the microcirculation is greater in brain stem. The objective of this study was to compare ultrastructural characteristics of the microcirculation in area postrema and adjacent brain stem.We studied 5 Sprague-Dawley rats. Horseradish peroxidase was injected intravenously and allowed to circulate for 1, 5 or 15 minutes. Following perfusion of the upper body with 2.25% glutaraldehyde in 0.1 M sodium cacodylate, the brain stem was removed, embedded in agar, and chopped into 50-70 μm sections with a TC-Sorvall tissue chopper. Sections of brain stem were incubated for 1 hour in a solution of 3,3' diaminobenzidine tetrahydrochloride (0.05%) in 0.05M Tris buffer with 1% H2O2.


2000 ◽  
Vol 278 (2) ◽  
pp. R499-R503 ◽  
Author(s):  
C. M. Kotz ◽  
M. J. Glass ◽  
A. S. Levine ◽  
C. J. Billington

Naltrexone (NLTX) in the nucleus of the solitary tract (NTS) decreases feeding induced by neuropeptide Y (NPY) in the paraventricular nucleus (PVN). We sought to determine the NTS region most sensitive to NLTX blockade of PVN NPY-induced feeding. Male Sprague-Dawley rats were fitted with two cannulas; one in the PVN and one in a hindbrain region: caudal, medial, or rostral NTS or 1 mm outside the NTS. Animals received NLTX (0, 1, 3, 10, and 30 μg in 0.3 μl) into the hindbrain region just prior to PVN NPY (0.5 μg, 0.3 μl) or artificial cerebrospinal fluid (0.3 μl). Food intake was measured at 2 h following injection. PVN NPY stimulated feeding, and NLTX in the medial NTS significantly decreased NPY-induced feeding at 2 h, whereas administration of NLTX in the other hindbrain regions did not significantly influence PVN NPY induced feeding. These data suggest that opioid receptors in the medial NTS are most responsive to feeding signals originating in the PVN after NPY stimulation.


2005 ◽  
Vol 288 (1) ◽  
pp. H256-H262 ◽  
Author(s):  
Ana Carolina Rodrigues Dias ◽  
Melissa Vitela ◽  
Eduardo Colombari ◽  
Steven W. Mifflin

The neuromodulatory effect of NO on glutamatergic transmission has been studied in several brain areas. Our previous single-cell studies suggested that NO facilitates glutamatergic transmission in the nucleus of the solitary tract (NTS). In this study, we examined the effect of the nitric oxide synthase (NOS) inhibitor NG-nitro-l-arginine methyl ester (l-NAME) on glutamatergic and reflex transmission in the NTS. We measured mean arterial pressure (MAP), heart rate (HR), and renal sympathetic nerve activity (RSNA) from Inactin-anesthetized Sprague-Dawley rats. Bilateral microinjections of l-NAME (10 nmol/100 nl) into the NTS did not cause significant changes in basal MAP, HR, or RSNA. Unilateral microinjection of ( RS)-α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA, 1 pmol/100 nl) into the NTS decreased MAP and RSNA. Fifteen minutes after l-NAME microinjections, AMPA-evoked cardiovascular changes were significantly reduced. N-methyl-d-aspartate (NMDA, 0.5 pmol/100 nl) microinjection into the NTS decreased MAP, HR, and RSNA. NMDA-evoked falls in MAP, HR, and RSNA were significantly reduced 30 min after l-NAME. To examine baroreceptor and cardiopulmonary reflex function, l-NAME was microinjected at multiple sites within the rostro-caudal extent of the NTS. Baroreflex function was tested with phenylephrine (PE, 25 μg iv) before and after l-NAME. Five minutes after l-NAME the decrease in RSNA caused by PE was significantly reduced. To examine cardiopulmonary reflex function, phenylbiguanide (PBG, 8 μg/kg) was injected into the right atrium. PBG-evoked hypotension, bradycardia, and RSNA reduction were significantly attenuated 5 min after l-NAME. Our results indicate that inhibition of NOS within the NTS attenuates baro- and cardiopulmonary reflexes, suggesting that NO plays a physiologically significant neuromodulatory role in cardiovascular regulation.


2003 ◽  
Vol 285 (6) ◽  
pp. R1276-R1286 ◽  
Author(s):  
Lin Mei ◽  
Jing Zhang ◽  
Steve Mifflin

Previous studies have demonstrated that microinjection of baclofen, a GABAB receptor agonist, into the nucleus of the solitary tract (NTS) results in an enhanced pressor response in hypertensive (HT) rats compared with normotensive (NT) rats, suggesting a possible alteration in the responses of neurons in this area to activation of GABAB receptors. The following studies were designed to determine whether HT alters the sensitivity of neurons in the NTS to GABA receptor agonists. Sham-operated NT and unilateral nephrectomized, renal-wrap HT Sprague-Dawley rats were anesthetized, and the responses of NTS neurons receiving aortic nerve (AN) afferent inputs to iontophoretic application of GABA, the GABAA receptor agonist muscimol, and the GABAB agonist baclofen were examined. The AN input was classified as monosynaptic (MSN) if the cell responded to each of two stimuli separated by 5 ms with an action potential. If the cell did not respond, the input was considered polysynaptic (PSN). In MSNs, inhibition of AN-evoked discharge by GABA was not altered in 1 wk of HT but was reduced in 4 wk of HT, whereas in PSNs, sensitivity to GABA was reduced at 1 and 4 wk of HT. In HT rats, inhibition of AN-evoked discharge by baclofen was enhanced in MSNs, but not in PSNs, after 1 and 4 wk of HT, whereas inhibition by muscimol was reduced in MSNs and PSNs at 1 and 4 wk of HT. Changes in sensitivity to muscimol and baclofen within MSNs were the same whether the MSN received a slowly or a rapidly conducted AN afferent input. The results demonstrate that early in HT the sensitivity of NTS neurons to inhibitory amino acids is altered and that these changes are maintained for ≥4 wk. The alterations are dependent on the subtype of GABA receptor being activated and whether the neuron receives a mono- or polysynaptic baroreceptor afferent input.


1994 ◽  
Vol 641 (1) ◽  
pp. 171-175 ◽  
Author(s):  
Akira Monji ◽  
Nobumitsu Morimoto ◽  
Iwao Okuyama ◽  
Kazuo Umeno ◽  
Ikuko Nagatsu ◽  
...  

2009 ◽  
Vol 296 (3) ◽  
pp. G621-G631 ◽  
Author(s):  
Gregory M. Holmes ◽  
Melissa Tong ◽  
R. Alberto Travagli

The actions of cholecystokinin (CCK) on gastrointestinal functions occur mainly via paracrine effects on peripheral sensory vagal fibers, which engage vago-vagal brain stem circuits to convey effector responses back to the gastrointestinal tract. Recent evidence suggests, however, that CCK also affects brain stem structures directly. Many electrophysiological studies, including our own, have shown that brain stem vagal circuits are excited by sulfated CCK (CCK-8s) directly, and we have further demonstrated that CCK-8s induces a remarkable degree of plasticity in GABAergic brain stem synapses. In the present study, we used fasted, anesthetized Sprague-Dawley rats to investigate the effects of brain stem administration of CCK-8s on gastric tone before and after activation of the esophageal-gastric reflex. CCK-8s microinjected in the dorsal vagal complex (DVC) or applied on the floor of the fourth ventricle induced an immediate and transient decrease in gastric tone. Upon recovery of gastric tone to baseline values, the gastric relaxation induced by esophageal distension was attenuated or even reversed. The effects of CCK-8s were antagonized by vagotomy or fourth ventricular, but not intravenous, administration of the CCK-A antagonist lorglumide, suggesting a central, not peripheral, site of action. The gastric relaxation induced by DVC microinjection of CCK-8s was unaffected by pretreatment with systemic bethanecol but was completely blocked by NG-nitro-l-arginine methyl ester, suggesting a nitrergic mechanism of action. These data suggest that 1) brain stem application of CCK-8s induces a vagally mediated gastric relaxation; 2) the CCK-8s-induced gastric relaxation is mediated via activation of nonadrenergic, noncholinergic pathways; and 3) CCK-8s reverses the esophageal-gastric reflex transiently.


2014 ◽  
Vol 307 (11) ◽  
pp. H1539-H1546 ◽  
Author(s):  
Amy C. Arnold ◽  
Debra I. Diz

The decline in cardiovagal baroreflex function that occurs with aging is accompanied by an increase in circulating leptin levels. Our previous studies showed that exogenous leptin impairs the baroreflex sensitivity for control of heart rate in younger rats, but the contribution of this hormone to baroreflex dysfunction during aging is unknown. Thus we assessed the effect of bilateral leptin microinjection (500 fmol/60 nl) within the solitary tract nucleus (NTS) on the baroreflex sensitivity in older (66 ± 2 wk of age) urethane/chloralose anesthetized Sprague-Dawley rats with elevated circulating leptin levels. In contrast to the 63% reduction observed in younger rats, leptin did not alter the baroreflex sensitivity for bradycardia evoked by phenylephrine in older rats (0.76 ± 0.19 baseline vs. 0.71 ± 0.15 ms/mmHg after leptin; P = 0.806). We hypothesized that this loss of sensitivity reflected endogenous suppression of the baroreflex by elevated leptin, rather than cardiovascular resistance to the peptide. Indeed, NTS administration of a leptin receptor antagonist (75 pmol/120 nl) improved the baroreflex sensitivity for bradycardia in older rats (0.73 ± 0.13 baseline vs. 1.19 ± 0.26 at 10 min vs. 1.87 ± 0.32 at 60 min vs. 1.22 ± 0.54 ms/mmHg at 120 min; P = 0.002), with no effect in younger rats. There was no effect of the leptin antagonist on the baroreflex sensitivity for tachycardia, responses to cardiac vagal chemosensitive fiber activation, or resting hemodynamics in older rats. These findings suggest that the actions of endogenous leptin within the NTS, either produced locally or derived from the circulation, contribute to baroreflex suppression during aging.


2005 ◽  
Vol 288 (3) ◽  
pp. R678-R684 ◽  
Author(s):  
Manuel Ángeles-Castellanos ◽  
Jorge Mendoza ◽  
Mauricio Díaz-Muñoz ◽  
Carolina Escobar

When food is restricted to a few hours daily, animals increase their locomotor activity 2–3 h before food access, which has been termed food anticipatory activity. Food entrainment has been linked to the expression of a circadian food-entrained oscillator (FEO) and the anatomic substrate of this oscillator seems to depend on diverse neural systems and peripheral organs. Previously, we have described a differential involvement of hypothalamic nuclei in the food-entrained process. For the food entrainment pathway, the communication between the gastrointestinal system and central nervous system is essential. The visceral synaptic input to the brain stem arrives at the dorsal vagal complex and is transmitted directly from the nucleus of the solitary tract (NST) or via the parabrachial nucleus (PBN) to hypothalamic nuclei and other areas of the forebrain. The present study aims to characterize the response of brain stem structures in food entrainment. The expression of c-Fos immunoreactivity (c-Fos-IR) was used to identify neuronal activation. Present data show an increased c-Fos-IR following meal time in all brain stem nuclei studied. Food-entrained temporal patterns did not persist under fasting conditions, indicating a direct dependence on feeding-elicited signals for this activation. Because NST and PBN exhibited a different and increased response from that expected after a regular meal, we suggest that food entrainment promotes ingestive adaptations that lead to a modified activation in these brain stem nuclei, e.g., stomach distension. Neural information provided by these nuclei to the brain may provide the essential entraining signal for FEO.


2009 ◽  
Vol 297 (3) ◽  
pp. R622-R631 ◽  
Author(s):  
Nicholas T. Bello ◽  
Angela S. Guarda ◽  
Chantelle E. Terrillion ◽  
Graham W. Redgrave ◽  
Janelle W. Coughlin ◽  
...  

Repetitive cycles of palatable food access and chronic calorie restriction alter feeding behaviors and forebrain neural systems. The purpose of this study was to determine the behavioral, endocrine, and meal-related hindbrain neural activation in adult male Sprague-Dawley rats exposed to a binge-access feeding schedule. The binge-access schedule consisted of repeated twice-per-week episodes of acute calorie restriction (to one-third of the previous day's intake) followed by 2 h of concurrent access to high-calorie palatable food (sweetened fat: 90% vegetable shortening-10% sucrose) and chow. The binge-access rats consumed more calories during the “binge” period than rats with continuous access to sweetened fat (continuous-access group) or subjected to repeated acute calorie restriction only (chow-restricted group). The binge-access group also exhibited a ∼25% increase in sweetened fat intake from week 1 to week 6. Persistence of the binge phenotype in the binge-access animals was demonstrated 2 wk, but not 4 wk, after ad libitum chow. The binge-access and chow-restricted groups maintained a similar normal body composition and hormonal profiles, whereas the continuous-access animals developed an obese phenotype. Terminal ghrelin levels were significantly higher in the binge-access group than in the continuous-access group. Consumption of a standardized meal resulted in more c-Fos-positive cells along the anterior-posterior nucleus of the solitary tract regions in the binge-access group than in naive controls. These results suggest that repeated cycles of acute calorie restriction followed by palatable food produce physiological alterations that may facilitate overconsumption of a highly palatable food during limited-access periods.


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