Cranial Afferent Glutamate Heterosynaptically Modulates GABA Release onto Second-Order Neurons via Distinctly Segregated Metabotropic Glutamate Receptors

Jin, Young Ho; Bailey, Timothy W.; Andresen, Michael

doi:10.1523/jneurosci.1991-04.2004

Cited by 54 publications

(79 citation statements)

References 40 publications

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“…Cranial visceral afferent excitation of second-order NTS neurons relies on non-NMDA receptor mediated glutamatergic transmission (Jin et al, 2004a;Jin et al, 2004b). Propofol did not alter the shape of EPSC events whether evoked or spontaneous, a result consistent with cortical neurons (Kitamura et al, 2003).…”

Section: Propofol Does Not Affect Glutamatergic Transmission In Seconsupporting

confidence: 62%

Propofol enhances both tonic and phasic inhibitory currents in second-order neurons of the solitary tract nucleus (NTS)

et al. 2008

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The anesthetic propofol is thought to induce rapid hypnotic sedation by facilitating a GABAergic tonic current in forebrain neurons. The depression of cardiovascular and respiratory regulation often observed during propofol suggests potential additional actions within the brainstem. Here we determined the impacts of propofol on both GABAergic and glutamatergic synaptic mechanisms in a class of solitary tract nucleus (NTS) neurons common to brainstem reflex pathways. In horizontal brainstem slices, we recorded from NTS neurons directly activated by solitary tract (ST) axons. We identified these second-order NTS neurons by time-invariant ("jitter" <200 µs), "all-or-none" glutamatergic excitatory postsynaptic currents (EPSCs) in response to shocks to the ST. In order to assess propofol actions, we measured ST-evoked, spontaneous and miniature EPSCs and inhibitory postsynaptic currents (IPSCs) during propofol exposure. Propofol prolonged miniature IPSC decay time constants by 50% above control at 1.8 µM. Low concentrations of gabazine (SR-95531) blocked phasic GABA currents. At higher concentrations, propofol (30 µM) induced a gabazine-insensitive tonic current that was blocked by picrotoxin or bicuculline. In contrast, total propofol concentrations up to 30 µM had no effect on EPSCs. Thus, propofol enhanced phasic GABA events in NTS at lower concentrations than tonic current induction, opposite to the relative sensitivity observed in forebrain regions. These data suggest that therapeutic levels of propofol facilitate phasic (synaptic) inhibitory transmission in second order NTS neurons which likely inhibits autonomic reflex pathways during anesthesia.

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Section: Propofol Does Not Affect Glutamatergic Transmission In Seconsupporting

confidence: 62%

Propofol enhances both tonic and phasic inhibitory currents in second-order neurons of the solitary tract nucleus (NTS)

et al. 2008

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“…Note that we examined only ionotropic receptors; the presence of GABA and glutamate metabotropic receptors in vagal brain stem circuits (17,21,35,38,47,48,60) adds another potentially larger level of complexity. Indeed, in the present study we did not examine the contribution of metabotropic receptors to the basal firing rate of DMV neurons and thus we cannot exclude their activation; however, we did not observe any significant effect on the DMV membrane induced by the GABA B antagonist saclofen (17) or Kynurenic acid was applied first, followed by bicuculline.…”

Section: Discussionmentioning

confidence: 99%

Differential organization of excitatory and inhibitory synapses within the rat dorsal vagal complex

Babic

Browning

Travagli

2011

American Journal of Physiology-Gastrointestinal and Liver Physi

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Babic T, Browning KN, Travagli RA. Differential organization of excitatory and inhibitory synapses within the rat dorsal vagal complex. Am J Physiol Gastrointest Liver Physiol 300: G21-G32, 2011. First published October 14, 2010 doi:10.1152/ajpgi.00363.2010.-The dorsal motor nucleus of the vagus (DMV) is pivotal in the regulation of upper gastrointestinal functions, including motility and both gastric and pancreatic secretion. DMV neurons receive robust GABA-and glutamatergic inputs. Microinjection of the GABAA antagonist bicuculline (BIC) into the DMV increases pancreatic secretion and gastric motility, whereas the glutamatergic antagonist kynurenic acid (KYN) is ineffective unless preceded by microinjection of BIC. We used whole cell patch-clamp recordings with the aim of unveiling the brain stem neurocircuitry that uses tonic GABA-and glutamatergic synapses to control the activity of DMV neurons in a brain stem slice preparation. Perfusion with BIC altered the firing frequency of 71% of DMV neurons, increasing firing frequency in 80% of the responsive neurons and decreasing firing frequency in 20%. Addition of KYN to the perfusate either decreased (52%) or increased (25%) the firing frequency of BIC-sensitive neurons. When KYN was applied first, the firing rate was decreased in 43% and increased in 21% of the neurons; further perfusion with BIC had no additional effect in the majority of neurons. Our results indicate that there are several permutations in the arrangements of GABA-and glutamatergic inputs controlling the activity of DMV neurons. Our data support the concept of brain stem neuronal circuitry that may be wired in a finely tuned organ-or function-specific manner that permits precise and discrete modulation of the vagal motor output to the gastrointestinal tract. electrophysiology; vagus; brain stem SENSORY INFORMATION FROM THE gastrointestinal (GI) tract is encoded by chemo-and mechanoreceptors with different modalities, responses, and properties (reviewed in Ref. 11). Regardless of their function(s) or modalities, however, primarily nonnoxious visceral sensory information is transmitted through the afferent vagus into the brain stem via a glutamatergic synapse at the level of the nucleus tractus solitarius (NTS) (2,3,8,54). The NTS comprises various subnuclei that appear to be organized viscerotopically (1, 9, 57), such that the vagal sensory input from each visceral organ is concentrated in a particular subnucleus. The subnucleus centralis, for example, receives inputs almost exclusively from the esophagus.The motor output to the GI tract is provided by the spontaneously firing neurons of the dorsal motor nucleus of the vagus (DMV), which, in contrast to NTS neurons, are organized in neuronal "columns" that project to the viscera through each of the five subdiaphragmatic vagal branches (reviewed in Ref. 57). DMV neurons within each column, however, are not identical but comprise heterogeneous neuronal populations that differ in their neurochemical, morphological, and electrophysiological prope...

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“…Increasing evidence from different laboratories, including our own, have shown that even within a relatively restricted group of nuclei, such as those comprised in the dorsal vagal complex, fundamental differences exists in the organization of synaptic circuits controlling GI, cardiovascular, and respiratory functions (1,3,6,14,15,17,18,24,29,45,51,52). This arrangement is quite logical, when considered from a physiological standpoint, since the requirements of each system vary greatly in the type, as well as the timing and duration, of responses.…”

Section: Discussionmentioning

confidence: 99%

Vanilloid, purinergic, and CCK receptors activate glutamate release on single neurons of the nucleus tractus solitarius centralis

Browning

Wan

Baptista

et al. 2011

American Journal of Physiology-Regulatory, Integrative and Comp

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Browning KN, Wan S, Baptista V, Travagli RA. Vanilloid, purinergic, and CCK receptors activate glutamate release on single neurons of the nucleus tractus solitarius centralis. Am J Physiol Regul Integr Comp Physiol 301: R394 -R401, 2011. First published May 4, 2011 doi:10.1152/ajpregu.00054.2011.-Baroreceptor inputs to nucleus of the tractus solitarius medialis (mNTS) neurons can be differentiated, among other features, by their response to vanilloid or purinergic agonists, active only on C-or A-fibers, respectively. A major aim of this study was to examine whether neurons of NTS centralis (cNTS), a subnucleus dominated by esophageal inputs, exhibit a similar dichotomy. Since it has been suggested that cholecystokinin (CCK), exerts its gastrointestinal (GI)-related effects via paracrine activation of vagal afferent C-fibers, we tested whether CCK-sensitive fibers impinging upon cNTS neurons are responsive to vanilloid but not purinergic agonists. Using whole cell patch-clamp recordings from cNTS, we recorded miniature excitatory postsynaptic currents (mEPSCs) to test the effects of the vanilloid agonist capsaicin, the purinergic agonist ␣,␤-methylene-ATP (␣,␤-Met-ATP), and/or CCK-octapeptide (CCK-8s). ␣,␤-Met-ATP, capsaicin; and CCK-8s increased EPSC frequency in 37, 71, and 46% of cNTS neurons, respectively. Approximately 30% of cNTS neurons were responsive to both CCK-8s and ␣,␤-Met-ATP, to CCK-8s and capsaicin, or to ␣,␤-Met-ATP and capsaicin, while 32% of neurons were responsive to all three agonists. All neurons responding to either ␣,␤-Met-ATP or CCK-8s were also responsive to capsaicin. Perivagal capsaicin, which is supposed to induce a selective degeneration of C-fibers, decreased the number of cNTS neurons responding to capsaicin or CCK-8s but not those responding to ␣,␤-Met-ATP. In summary, GI inputs to cNTS neurons cannot be distinguished on the basis of their selective responses to ␣,␤-Met-ATP or capsaicin. Our data also indicate that CCK-8s increases glutamate release from purinergic and vanilloid responsive fibers impinging on cNTS neurons. brainstem; vagus; electrophysiology VAGAL AFFERENT (SENSORY) FIBERS convey a vast amount of information about the physiological state of the thoracic and abdominal viscera to the central nervous system, specifically, to the nucleus of the tractus solitarius (NTS). Vagal afferent fibers are organized in the NTS in an overlapping topographical manner. Sensory afferents from the stomach and intestine, for example, terminate in the subnuclei commissuralis and medialis, inputs from the stomach terminate in the subnuclei medialis and gelatinosus, while inputs from the esophagus terminate in the subnucleus centralis (49). Vagal afferent fibers relay this visceral information by a mixture of myelinated (A-type) and unmyelinated (C-type) axons. These two types of afferent fibers display distinct physiological and functional characteristics, including different sensory modalities and conduction velocities and may regulate autonomic homeostatic and regulatory reflexes di...

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Cranial Afferent Glutamate Heterosynaptically Modulates GABA Release onto Second-Order Neurons via Distinctly Segregated Metabotropic Glutamate Receptors

Cited by 54 publications

References 40 publications

Propofol enhances both tonic and phasic inhibitory currents in second-order neurons of the solitary tract nucleus (NTS)

Propofol enhances both tonic and phasic inhibitory currents in second-order neurons of the solitary tract nucleus (NTS)

Differential organization of excitatory and inhibitory synapses within the rat dorsal vagal complex

Vanilloid, purinergic, and CCK receptors activate glutamate release on single neurons of the nucleus tractus solitarius centralis

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