Distribution of tachykinin- and opioid-expressing neurons in the hamster solitary nucleus: an immuno- and in situ hybridization histochemical study

Davis, Barry J.; Kream, Richard M.

doi:10.1016/0006-8993(93)90185-p

Cited by 37 publications

(12 citation statements)

References 46 publications

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“…The activation of this channel has been shown to produce inhibition by shunting current across the membrane. Endogenous opioids may also mediate inhibitory control of taste processing in the rostral NTS (Li et al, 2003; Davis and Kream, 1993). Li et al (2003) showed that microinjection of met-enkephalin into the gustatory NTS suppresses taste responsivity.…”

Section: Discussionmentioning

confidence: 99%

Two types of inhibitory influences target different groups of taste-responsive cells in the nucleus of the solitary tract of the rat

Rosen

Lorenzo

2009

Brain Research

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Electrical stimulation of the chorda tympani nerve (CT; innervating taste buds on the rostral tongue) is known to initiate recurrent inhibition in cells in the nucleus of the solitary tract (NTS, the first central relay in the gustatory system). Here, we explored the relationship between inhibitory circuits and the breadth of tuning of taste-responsive NTS neurons. Initially, NTS cells with evoked responses to electrical stimulation of the CT (0.1 ms pulses; 1 Hz) were tested with each of four tastants (0.1 M NaCl, 0.01 M HCl, 0.01 M quinine and 0.5 M sucrose) in separate trials. Next, the CT was electrically stimulated using a paired-pulse (10-2000 ms interpulse interval; blocks of 100 trials) paradigm. Forty-five (30 taste-responsive) of 51 cells with CT-evoked responses (36 tasteresponsive) were tested with paired pulses. The majority (34; 75.6%) showed paired-pulse attenuation, defined as fewer evoked spikes in response to the second (test) pulse compared with the first (conditioning) pulse. A bimodal distribution of the peak of paired-pulse attenuation was found with modes at 10 ms and 50 ms in separate groups of cells. Cells with early peak attenuation showed short CT-evoked response latencies and large responses to relatively few taste stimuli. Conversely, cells with late peak attenuation showed long CT-evoked response latencies and small taste responses with less selectivity. Results suggest that the breadth of tuning of an NTS cell may result from the combination of the sensitivities of peripheral nerve inputs and the recurrent influences generated by the circuitry of the NTS.

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Section: Discussionmentioning

confidence: 99%

Two types of inhibitory influences target different groups of taste-responsive cells in the nucleus of the solitary tract of the rat

Rosen

Lorenzo

2009

Brain Research

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“…Opioids modulate a wide range of visceral and autonomic processes in the brain stem. In the rNST, varicose fibers containing endogenous ligands for MORs are plentiful, including the enkephalins, which activate ␦-opioid receptors as well as MORs (Raynor et al 1994), and the endomorphins, which are specific MOR agonists (Zadina et al 1997 (Davis and Kream 1993;Fallon and Leslie 1986;Murakami et al 1987;Stornetta et al 2001), but endomorphinergic soma are located only in the cNST at the level of area postrema and the hypothalamus near and in the dorsomedial and arcuate nuclei (Martin-Schild et al 1999;Pierce and Wessendorf 2000).…”

Section: Damgo (Presynaptically) Suppresses St-evoked Responses In Thmentioning

confidence: 99%

The μ-opioid receptor agonist DAMGO presynaptically suppresses solitary tract-evoked input to neurons in the rostral solitary nucleus

Boxwell

Yanagawa

Travers

et al. 2013

Journal of Neurophysiology

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Boxwell AJ, Yanagawa Y, Travers SP, Travers JB. The -opioid receptor agonist DAMGO presynaptically suppresses solitary tract-evoked input to neurons in the rostral solitary nucleus. J Neurophysiol 109: 2815-2826, 2013. First published March 13, 2013 doi:10.1152/jn.00711.2012.-Taste processing in the rostral nucleus of the solitary tract (rNST) is subject to modulatory influences including opioid peptides. Behavioral pharmacological studies suggest an influence of -opioid receptors in rNST, but the underlying mechanism is unknown. To determine the cellular site of action, we tested the effects of the -opioid receptor agonist DAMGO in vitro. Whole cell patch-clamp recordings were made in brain stem slices from GAD67-GFP knockin mice expressing enhanced green fluorescent protein (EGFP) under the control of the endogenous promoter for GAD67, a synthetic enzyme for GABA. Neuron counts showed that ϳ36% of rNST neurons express GABA. We recorded monosynaptic solitary tract (ST)-evoked currents (jitter Յ 300 s) in both GAD67-EGFP-positive (GAD67ϩ) and GAD67-EGFP-negative (GAD67Ϫ) neurons with equal frequency (25/31; 22/28), but the inputs to the GAD67ϩ neurons had significantly smaller paired-pulse ratios compared with GAD67Ϫ neurons. DAMGO (0.3 M) significantly suppressed ST-evoked currents in both cell types (mean suppression ϭ 46 Ϯ 3.3% SE), significantly increased the paired-pulse ratio of these currents, and reduced the frequency of spontaneous miniature excitatory postsynaptic currents but did not diminish their amplitude, indicating a presynaptic site of action. Under inhibitory amino acid receptor blockade, DAMGO was significantly more suppressive in GAD67ϩ neurons (59% reduction) compared with GAD67Ϫ neurons (35% reduction), while the reverse was true in normal artificial cerebrospinal fluid (GAD67ϩ: 35% reduction; GAD67Ϫ: 57% reduction). These findings suggest that DAMGO suppresses activity in rNST neurons predominantly via a presynaptic mechanism, and that this effect may interact significantly with tonic or evoked inhibitory activity.

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“…However, the source(s) of the endogenous ligand for rNST/RF MORs is unclear. Cell bodies immunoreactive for enkephalin and endomorphin are present in the NST (9,44,48,56), suggesting that one of the major inputs to rNST/RF MORs may be from NST interneurons. Additionally, previous studies have provided evidence for a multisynaptic opioid connection between the rNST and limbic and homeostatic feeding centers, such as the central nucleus of the amygdala and hypothalamic nuclei (16,36).…”

Section: Discussionmentioning

confidence: 99%

“…The rNST and RF are anatomically connected and together exert a major influence on taste processing and oromotor integration (5, 6). Both the rNST and RF contain MORs (40, 47), and their endogenous ligands, the enkephalins and endomorphins (9,28,44,48,56). Indeed, experiments examining the consequences of manipulating MORs near the rNST/RF have demonstrated increases in chow intake (16,33,35,36).…”

mentioning

confidence: 99%

μ-Opioid modulation in the rostral solitary nucleus and reticular formation alters taste reactivity: evidence for a suppressive effect on consummatory behavior

Kinzeler

Travers

2011

American Journal of Physiology-Regulatory, Integrative and Comp

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Kinzeler NR, Travers SP. -Opioid modulation in the rostral solitary nucleus and reticular formation alters taste reactivity: evidence for a suppressive effect on consummatory behavior. Am J Physiol Regul Integr Comp Physiol 301: R690 -R700, 2011. First published June 22, 2011; doi:10.1152/ajpregu.00142.2011.-The neural control of feeding involves many neuromodulators, including the endogenous opioids that bind -opioid receptors (MORs). Injections of the MOR agonist, Damgo, into limbic and hypothalamic forebrain sites increase intake, particularly of palatable foods. Indeed, forebrain Damgo injections increase sucrose-elicited licking but reduce aversive responding (gaping) to quinine, suggesting that MOR activation may enhance taste palatability. A -opioid influence on taste reactivity has not been assessed in the brain stem. However, MORs are present in the first-order taste relay, the rostral nucleus of the solitary tract (rNST), and in the immediately subjacent reticular formation (RF), a region known to be essential for consummatory responses. Thus, to evaluate the consequences of rNST/dorsal RF Damgo in this region, we implanted rats with intraoral cannulas, electromyographic electrodes, and brain cannulas aimed at the ventral border of the rNST. Licking and gaping elicited with sucrose, water, and quinine were assessed before and after intramedullary Damgo and saline infusions. Damgo slowed the rate, increased the amplitude, and decreased the size of fluid-induced lick and gape bouts. In addition, the neutral stimulus water, which typically elicits licks, began to evoke gapes. Thus, the current results demonstrate that -opioid activation in the rNST/dorsal RF exerts complex effects on oromotor responding that contrast with forebrain effects and are more indicative of a suppressive, rather than a facilitatory effect on ingestion.licking; gaping; feeding; nucleus of the solitary tract CONSIDERABLE EVIDENCE SUGGESTS that the endogenous opioid system modulates feeding and ingestive behavior. Until recently, the focus had been primarily on opioid effects at forebrain sites or after systemic injections. Systemic injections of morphine increase feeding, whereas the general opioid antagonist, naltrexone, attenuates intake (38, 39, 43). These effects are greatest when the animals are presented with a diet high in sugar or fat, suggesting that opioids can facilitate feeding by enhancing palatability. Experiments using the taste reactivity test support this conclusion. Morphine lengthens (11), and naltrexone shortens (52), the length of licking bouts elicited by sucrose, a measure positively correlated with stimulus palatability (15, 68), whereas systemic morphine reduces the number of aversive reactions (i.e., gapes) to the bitter stimulus, quinine (52).Experiments conducted using central injections have begun to establish which brain sites underlie these effects. Similar to systemic administration, infusions of the -opioid receptor (MOR) agonist D-Ala 2 , N-Me-Phe 4 , and Gly-ol 5 -enkephalin (Damgo) into various h...

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Distribution of tachykinin- and opioid-expressing neurons in the hamster solitary nucleus: an immuno- and in situ hybridization histochemical study

Cited by 37 publications

References 46 publications

Two types of inhibitory influences target different groups of taste-responsive cells in the nucleus of the solitary tract of the rat

Two types of inhibitory influences target different groups of taste-responsive cells in the nucleus of the solitary tract of the rat

The μ-opioid receptor agonist DAMGO presynaptically suppresses solitary tract-evoked input to neurons in the rostral solitary nucleus

μ-Opioid modulation in the rostral solitary nucleus and reticular formation alters taste reactivity: evidence for a suppressive effect on consummatory behavior

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