scholarly journals Comparison of baroreceptive to other afferent synaptic transmission to the medial solitary tract nucleus

2008 ◽  
Vol 295 (5) ◽  
pp. H2032-H2042 ◽  
Author(s):  
Michael C. Andresen ◽  
James H. Peters
Keyword(s):  
Synaptic Transmission ◽  
Brain Stem ◽  
Glutamate Release ◽  
Second Order ◽  
Visceral Afferents ◽  
Solitary Tract Nucleus ◽  
Failure Rates ◽  
Solitary Tract ◽  
Frequency Dependent ◽  
Aortic Depressor Nerve

Cranial nerve visceral afferents enter the brain stem to synapse on neurons within the solitary tract nucleus (NTS). The broad heterogeneity of both visceral afferents and NTS neurons makes understanding afferent synaptic transmission particularly challenging. To study a specific subgroup of second-order neurons in medial NTS, we anterogradely labeled arterial baroreceptor afferents of the aortic depressor nerve (ADN) with lipophilic fluorescent tracer (i.e., ADN+) and measured synaptic responses to solitary tract (ST) activation recorded from dye-identified neurons in medial NTS in horizontal brain stem slices. Every ADN+ NTS neuron received constant-latency ST-evoked excitatory postsynaptic currents (EPSCs) (jitter <192 μs, SD of latency). Stimulus-recruitment profiles showed single thresholds and no suprathreshold recruitment, findings consistent with EPSCs arising from a single, branched afferent axon. Frequency-dependent depression of ADN+ EPSCs averaged ∼70% for five shocks at 50 Hz, but single-shock failure rates did not exceed 4%. Whether adjacent ADN− or those from unlabeled animals, other second-order NTS neurons (jitters <200 μs) had ST transmission properties indistinguishable from ADN+. Capsaicin (CAP; 100 nM) blocked ST transmission in some neurons. CAP-sensitive ST-EPSCs were smaller and failed over five times more frequently than CAP-resistant responses, whether ADN+ or from unlabeled animals. Variance-mean analysis of ST-EPSCs suggested uniformly high probabilities for quantal glutamate release across second-order neurons. While amplitude differences may reflect different numbers of contacts, higher frequency-dependent failure rates in CAP-sensitive ST-EPSCs may arise from subtype-specific differences in afferent axon properties. Thus afferent transmission within medial NTS differed by axon class (e.g., CAP sensitive) but was indistinguishable by source of axon (e.g., baroreceptor vs. nonbaroreceptor).

scholarly journals Isoflurane Differentially Modulates Inhibitory and Excitatory Synaptic Transmission to the Solitary Tract Nucleus

2008 ◽  
Vol 108 (4) ◽  
pp. 675-683 ◽  
Author(s):  
James H. Peters ◽  
Stuart J. McDougall ◽  
David Mendelowitz ◽  
Dennis R. Koop ◽  
Michael C. Andresen
Keyword(s):  
Nucleus Tractus Solitarius ◽  
Second Order ◽  
Visceral Afferents ◽  
Gas Chromatography Mass Spectrometry ◽  
Gamma Aminobutyric Acid ◽  
Solitary Tract ◽  
Excitatory Postsynaptic Currents ◽  
Inhibitory Postsynaptic Currents ◽  
Postsynaptic Currents ◽  
Presynaptic Mechanisms

Background Isoflurane anesthesia produces cardiovascular and respiratory depression, although the specific mechanisms are not fully understood. Cranial visceral afferents, which innervate the heart and lungs, synapse centrally onto neurons within the medial portion of the nucleus tractus solitarius (NTS). Isoflurane modulation of afferent to NTS synaptic communication may underlie compromised cardiorespiratory reflex function. Methods Adult rat hindbrain slice preparations containing the solitary tract (ST) and NTS were used. Shocks to ST afferents evoked excitatory postsynaptic currents with low-variability (SEM &lt;200 mus) latencies identifying neurons as second order. ST-evoked and miniature excitatory postsynaptic currents as well as miniature inhibitory postsynaptic currents were measured during isoflurane exposure. Perfusion bath samples were taken in each experiment to measure isoflurane concentrations by gas chromatography-mass spectrometry. Results Isoflurane dose-dependently increased the decay-time constant of miniature inhibitory postsynaptic currents. At greater than 300 mum isoflurane, the amplitude of miniature inhibitory postsynaptic currents was decreased, but the frequency of events remained unaffected, whereas at equivalent isoflurane concentrations, the frequency of miniature excitatory postsynaptic currents was decreased. ST-evoked excitatory postsynaptic current amplitudes decreased without altering event kinetics. Isoflurane at greater than 300 mum increased the latency to onset and rate of synaptic failures of ST-evoked excitatory postsynaptic currents. Conclusions In second-order NTS neurons, isoflurane enhances phasic inhibitory transmission via postsynaptic gamma-aminobutyric acid type A receptors while suppressing excitatory transmission through presynaptic mechanisms. These results suggest that isoflurane acts through multiple distinct mechanisms to inhibit neurotransmission within the NTS, which would underlie suppression of homeostatic reflexes.

Allopregnanolone Effects on Transmission in the Brain Stem Solitary Tract Nucleus (NTS)

Neuroscience ◽  
2018 ◽  
Vol 379 ◽  
pp. 219-227 ◽  
Author(s):  
Sojin Kim ◽  
Sung-Moon Kim ◽  
Bermseok Oh ◽  
Jihoon Tak ◽  
Eunhee Yang ◽  
...  
Keyword(s):  
Brain Stem ◽  
Solitary Tract Nucleus ◽  
Solitary Tract ◽  
The Brain

scholarly journals Corticosterone inhibits vagal afferent glutamate release in the nucleus of the solitary tract via retrograde endocannabinoid signaling

2020 ◽  
Vol 319 (6) ◽  
pp. C1097-C1106
Author(s):  
Forrest J. Ragozzino ◽  
Rachel A. Arnold ◽  
Cody W. Kowalski ◽  
Marina I. Savenkova ◽  
Ilia N. Karatsoreos ◽  
...  
Keyword(s):  
Brain Stem ◽  
Autonomic Function ◽  
Glutamate Release ◽  
Vagal Afferents ◽  
Solitary Tract ◽  
Excitatory Neurotransmitter ◽  
Cannabinoid Type 1 Receptor ◽  
Glutamate Signaling ◽  
Vagal Afferent ◽  
Afferent Terminals

Circulating blood glucocorticoid levels are dynamic and responsive to stimuli that impact autonomic function. In the brain stem, vagal afferent terminals release the excitatory neurotransmitter glutamate to neurons in the nucleus of the solitary tract (NTS). Vagal afferents integrate direct visceral signals and circulating hormones with ongoing NTS activity to control autonomic function and behavior. Here, we investigated the effects of corticosterone (CORT) on glutamate signaling in the NTS using patch-clamp electrophysiology on brain stem slices containing the NTS and central afferent terminals from male C57BL/6 mice. We found that CORT rapidly decreased both action potential-evoked and spontaneous glutamate signaling. The effects of CORT were phenocopied by dexamethasone and blocked by mifepristone, consistent with glucocorticoid receptor (GR)-mediated signaling. While mRNA for GR was present in both the NTS and vagal afferent neurons, selective intracellular quenching of G protein signaling in postsynaptic NTS neurons eliminated the effects of CORT. We then investigated the contribution of retrograde endocannabinoid signaling, which has been reported to transduce nongenomic GR effects. Pharmacological or genetic elimination of the cannabinoid type 1 receptor signaling blocked CORT suppression of glutamate release. Together, our results detail a mechanism, whereby the NTS integrates endocrine CORT signals with fast neurotransmission to control autonomic reflex pathways.

Reliability of Monosynaptic Sensory Transmission in Brain Stem Neurons In Vitro

2001 ◽  
Vol 85 (5) ◽  
pp. 2213-2223 ◽  
Author(s):  
Mark W. Doyle ◽  
Michael C. Andresen
Keyword(s):  
Brain Stem ◽  
Nucleus Tractus Solitarius ◽  
Temporal Integration ◽  
Second Order ◽  
Failure Rates ◽  
Critical Feature ◽  
Medial Nucleus ◽  
Nmda Glutamate Receptors ◽  
Spatio Temporal

The timing of events within the nervous system is a critical feature of signal processing and integration. In neurotransmission, the synaptic latency, the time between stimulus delivery and appearance of the synaptic event, is generally thought to be directly related to the complexity of that pathway. In horizontal brain stem slices, we examined synaptic latency and its shock-to-shock variability (synaptic jitter) in medial nucleus tractus solitarius (NTS) neurons in response to solitary tract (ST) electrical activation. Using a visualized patch recording approach, we activated ST 1–3 mm from the recorded neuron with short trains (50–200 Hz) and measured synaptic currents under voltage clamp. Latencies ranged from 1.5 to 8.6 ms, and jitter values (SD of intraneuronal latency) ranged from 26 to 764 μs ( n = 49). Surprisingly, frequency of synaptic failure was not correlated with either latency or jitter ( P > 0.147; n = 49). Despite conventional expectations, no clear divisions in latency were found from the earliest arriving excitatory postsynaptic currents (EPSCs) to late pharmacologically polysynaptic responses. Shortest latency EPSCs (<3 ms) were mediated by non– N-methyl-d-aspartate (non-NMDA) glutamate receptors. Longer latency responses were a mix of excitatory and inhibitory currents including non-NMDA EPSCs and GABAa receptor–mediated currents (IPSC). All synaptic responses exhibited prominent frequency-dependent depression. In a subset of neurons, we labeled sensory boutons by the anterograde fluorescent tracer, DiA, from aortic nerve baroreceptors and then recorded from anatomically identified second-order neurons. In identified second-order NTS neurons, ST activation evoked EPSCs with short to moderate latency (1.9–4.8 ms) but uniformly minimal jitter (31 to 61 μs) that were mediated by non-NMDA receptors but had failure rates as high as 39%. These monosynaptic EPSCs in identified second-order neurons were significantly different in latency and jitter than GABAergic IPSCs (latency, 2.95 ± 0.71 vs. 5.56 ± 0.74 ms, mean ± SE, P = 0.027; jitter, 42.3 ± 6.5 vs. 416.3 ± 94.4 μs, P = 0.013, n = 4, 6, respectively), but failure rates were similar (27.8 ± 9.0 vs. 9.7 ± 4.4%, P = 0.08, respectively). Such results suggest that jitter and not absolute latency or failure rate is the most reliable discriminator of mono- versus polysynaptic pathways. The results suggest that brain stem sensory pathways may differ in their principles of integration compared with cortical models and that this importantly impacts synaptic performance. The unique performance properties of the sensory-NTS pathway may reflect stronger axosomatic synaptic processing in brain stem compared with dendritically weighted models typical in cortical structures and thus may reflect very different strategies of spatio-temporal integration in this NTS region and for autonomic regulation.

scholarly journals Independent transmission of convergent visceral primary afferents in the solitary tract nucleus

2013 ◽  
Vol 109 (2) ◽  
pp. 507-517 ◽  
Author(s):  
Stuart J. McDougall ◽  
Michael C. Andresen
Keyword(s):  
Potential Interaction ◽  
Primary Afferents ◽  
Second Order ◽  
Solitary Tract Nucleus ◽  
Solitary Tract ◽  
Multiple Contacts ◽  
Large Numbers ◽  
Response Profiles ◽  
Active Release ◽  
The Brain

Cranial primary afferents from the viscera enter the brain at the solitary tract nucleus (NTS), where their information is integrated for homeostatic reflexes. The organization of sensory inputs is poorly understood, despite its critical impact on overall reflex performance characteristics. Single afferents from the solitary tract (ST) branch within NTS and make multiple contacts onto individual neurons. Many neurons receive more than one ST input. To assess the potential interaction between converging afferents and proximal branching near to second-order neurons, we probed near the recorded soma in horizontal slices from rats with focal electrodes and minimal shocks. Remote ST shocks evoked monosynaptic excitatory postsynaptic currents (EPSCs), and nearby focal shocks also activated monosynaptic EPSCs. We tested the timing and order of stimulation to determine whether focal shocks influenced ST responses and vice versa in single neurons. Focal-evoked EPSC response profiles closely resembled ST-EPSC characteristics. Mean synaptic jitters, failure rates, depression, and phenotypic segregation by capsaicin responsiveness were indistinguishable between focal and ST-evoked EPSCs. ST-EPSCs failed to affect focal-EPSCs within neurons, indicating that release sites and synaptic terminals were functionally independent and isolated from cross talk or neurotransmitter overflow. In only one instance, focal shocks intercepted and depleted the ST axon generating evoked EPSCs. Despite large numbers of functional contacts, multiple afferents do not appear to interact, and ST axon branches may be limited to close to the soma. Thus single or multiple primary afferents and their presynaptic active release sites act independently when they contact single second-order NTS neurons.

scholarly journals pH modulation of glial glutamate transporters regulates synaptic transmission in the nucleus of the solitary tract

2013 ◽  
Vol 110 (2) ◽  
pp. 368-377 ◽  
Author(s):  
Rafiq Huda ◽  
Donald R. McCrimmon ◽  
Marco Martina
Keyword(s):  
Synaptic Transmission ◽  
Glutamate Uptake ◽  
Glutamate Release ◽  
Glutamate Transporters ◽  
Functional Expression ◽  
Repetitive Stimulation ◽  
Solitary Tract ◽  
Extracellular Acidification ◽  
Sensory Afferents ◽  
Selective Membrane

The nucleus of the solitary tract (NTS) is the major site for termination of visceral sensory afferents contributing to homeostatic regulation of, for example, arterial pressure, gastric motility, and breathing. Whereas much is known about how different neuronal populations influence these functions, information about the role of glia remains scant. In this article, we propose that glia may contribute to NTS functions by modulating excitatory neurotransmission. We found that acidification (pH 7.0) depolarizes NTS glia by inhibiting K+-selective membrane currents. NTS glia also showed functional expression of voltage-sensitive glutamate transporters, suggesting that extracellular acidification regulates synaptic transmission by compromising glial glutamate uptake. To test this hypothesis, we evoked glutamatergic slow excitatory potentials (SEPs) in NTS neurons with repetitive stimulation (20 pulses at 10 Hz) of the solitary tract. This SEP depends on accumulation of glutamate following repetitive stimulation, since it was potentiated by blocking glutamate uptake with dl- threo-β-benzyloxyaspartic acid (TBOA) or a glia-specific glutamate transport blocker, dihydrokainate (DHK). Importantly, extracellular acidification (pH 7.0) also potentiated the SEP. This effect appeared to be mediated through a depolarization-induced inhibition of glial transporter activity, because it was occluded by TBOA and DHK. In agreement, pH 7.0 did not directly alter d-aspartate-induced responses in NTS glia or properties of presynaptic glutamate release. Thus acidification-dependent regulation of glial function affects synaptic transmission within the NTS. These results suggest that glia play a modulatory role in the NTS by integrating local tissue signals (such as pH) with synaptic inputs from peripheral afferents.

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

2008 ◽  
Vol 54 (3) ◽  
pp. 552-563 ◽  
Author(s):  
Stuart J. McDougall ◽  
Timothy W. Bailey ◽  
David Mendelowitz ◽  
Michael C. Andresen
Keyword(s):  
Second Order ◽  
Solitary Tract Nucleus ◽  
Solitary Tract
Sign in / Sign up

Export Citation Format

Share Document