Ketamine Differentially Blocks Sensory Afferent Synaptic Transmission in Medial Nucleus Tractus Solitarius (mNTS)

Jin, Young Ho; Bailey, Timothy W.; Doyle, Mark; Li, Bai Yan; Chang, Kyoung S. K.; Schild, John H.; Mendelowitz, David; Andresen, Michael

doi:10.1097/00000542-200301000-00021

Cited by 36 publications

(46 citation statements)

References 46 publications

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“…Activation of NMDARs in glial cells seems unlikely because calcium rises in glial cells induced by visceral fibers stimulation are insensitive to NMDAR blockade (McDougal et al, 2011). Although part of excitatory synapses between visceral fibers and NTS neurons do not express synaptic NMDARs (Doyle and Andresen, 2001; Jin et al, 2003), they are present extrasynaptically. In addition, EC may diffuse over micrometric distances (Chevaleyre and Castillo, 2004).…”

Section: Discussionmentioning

confidence: 99%

“…Although, the PPR and CV changes demonstrate that the LTD is expressed presynaptically, NMDARs could be located in the presynaptic or postsynaptic compartment. Monosynaptic responses elicited by solitary tract stimulation often lack an NMDA component, thereby suggesting that at least some NTS glutamatergic synapses are devoid of NMDARs (Doyle and Andresen, 2001;Jin et al, 2003). To determine whether NMDARs were located presynaptically or postsynaptically, we used a specific postsynaptic blockade of NMDARs.…”

Section: Ltd Induced By Lfs Requires Nmdars Not Located In the Postsymentioning

confidence: 99%

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Anandamide, Cannabinoid Type 1 Receptor, and NMDA Receptor Activation Mediate Non-Hebbian Presynaptically Expressed Long-Term Depression at the First Central Synapse for Visceral Afferent Fibers

Khlaifia¹,

Farah²,

Gackière³

et al. 2013

Journal of Neuroscience

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Presynaptic long-term depression (LTD) of synapse efficacy generally requires coordinated activity between presynaptic and postsynaptic neurons and a retrograde signal synthesized by the postsynaptic cell in an activity-dependent manner. In this study, we examined LTD in the rat nucleus tractus solitarii (NTS), a brainstem nucleus that relays homeostatic information from the internal body to the brain. We found that coactivation of N-methyl-D-aspartate receptors (NMDARs) and type 1 cannabinoid receptors (CB 1 Rs) induces LTD at the first central excitatory synapse between visceral fibers and NTS neurons. This LTD is presynaptically expressed. However, neither postsynaptic activation of NMDARs nor postsynaptic calcium influx are required for its induction. Direct activation of NMDARs triggers cannabinoid-dependent LTD. In addition, LTD is unaffected by blocking 2-arachidonyl-glycerol synthesis, but its induction threshold is lowered by preventing fatty acid degradation. Altogether, our data suggest that LTD in NTS neurons may be entirely expressed at the presynaptic level by local anandamide synthesis.

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Section: Discussionmentioning

confidence: 99%

Section: Ltd Induced By Lfs Requires Nmdars Not Located In the Postsymentioning

confidence: 99%

Anandamide, Cannabinoid Type 1 Receptor, and NMDA Receptor Activation Mediate Non-Hebbian Presynaptically Expressed Long-Term Depression at the First Central Synapse for Visceral Afferent Fibers

Khlaifia¹,

Farah²,

Gackière³

et al. 2013

Journal of Neuroscience

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“…In previous studies, we have shown that ST afferent pathways arising from myelinated and unmyelinated neurons can be distinguished by their susceptibility to blockade by the TRPV (vanilloid receptor) agonist capsaicin Jin et al, 2003). Namely, EPSCs mediated by unmyelinated afferents are typically blocked, whereas EPSCs mediated by myelinated afferents are unaffected.…”

Section: Myelinated and Unmyelinated St Pathways Activate Cvlm-and Pvmentioning

confidence: 99%

Cranial Visceral Afferent Pathways through the Nucleus of the Solitary Tract to Caudal Ventrolateral Medulla or Paraventricular Hypothalamus: Target-Specific Synaptic Reliability and Convergence Patterns

Bailey

Hermes

Andresen³

et al. 2006

J. Neurosci.

130

141

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Cranial visceral afferents activate central pathways that mediate systemic homeostatic processes. Afferent information arrives in the brainstem nucleus of the solitary tract (NTS) and is relayed to other CNS sites for integration into autonomic responses and complex behaviors. Little is known about the organization or nature of processing within NTS. We injected fluorescent retrograde tracers into two nuclei to identify neurons that project to sites involved in autonomic regulation: the caudal ventrolateral medulla (CVLM) or paraventricular nucleus of the hypothalamus (PVN). We found distinct differences in synaptic connections and performance in the afferent path through NTS to these neurons. Anatomical studies using confocal and electron microscopy found prominent, primary afferent synapses directly on somata and dendrites of CVLM-projecting NTS neurons identifying them as second-order neurons. In brainstem slices, afferent activation evoked large, constant latency EPSCs in CVLM-projecting NTS neurons that were consistent with the precise timing and rare failures of monosynaptic contacts on second-order neurons. In contrast, most PVN-projecting NTS neurons lacked direct afferent input and responded to afferent stimuli with highly variable, intermittently failing synaptic responses, indicating polysynaptic pathways to higher-order neurons. The afferent-evoked EPSCs in most PVN-projecting NTS neurons were smaller and unreliable but also often included multiple, convergent polysynaptic responses not observed in CVLM-projecting neurons. A few PVN-projecting NTS neurons had monosynaptic EPSC characteristics. Together, we found that cranial visceral afferent pathways are structured distinctly within NTS depending on the projection target. Such, intra-NTS pathway architecture will substantially impact performance of autonomic or neuroendocrine reflex arcs.

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“…For example, evidence from intracellular recordings in horizontal slices (22,34) (22,34,35). The exception is a small population of second order NTS neurons with apparently myelinated ST afferent innervation (36). Methods of approach are critical considerations for interpreting results and, clearly, alternative explanations are needed to account for NMDA receptor responses in the NTS.…”

Section: The Case For the Strong Synapsementioning

confidence: 99%

“…We began with the premise that peripheral cellular differences in cranial afferent neurons (e.g., at the nodose ganglion) are present in the central, presynaptic terminals of these same sensory neurons. The expectation (Figure 2) is that pathways through the NTS would be divided on the basis of afferent class (34,36,56).…”

Section: Cellular Basis Of Nts Neurotransmissionmentioning

confidence: 99%

Differentiation of autonomic reflex control begins with cellular mechanisms at the first synapse within the nucleus tractus solitarius

Andresen

Doyle

Bailey

et al. 2004

Braz J Med Biol Res

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Visceral afferents send information via cranial nerves to the nucleus tractus solitarius (NTS). The NTS is the initial step of information processing that culminates in homeostatic reflex responses. Recent evidence suggests that strong afferent synaptic responses in the NTS are most often modulated by depression and this forms a basic principle of central integration of these autonomic pathways. The visceral afferent synapse is uncommonly powerful at the NTS with large unitary response amplitudes and depression rather than facilitation at moderate to high frequencies of activation. Substantial signal depression occurs through multiple mechanisms at this very first brainstem synapse onto second order NTS neurons. This review highlights new approaches to the study of these basic processes featuring patch clamp recordings in NTS brain slices and optical techniques with fluorescent tracers. The vanilloid receptor agonist, capsaicin, distinguishes two classes of second order neurons (capsaicin sensitive or capsaicin resistant) that appear to reflect unmyelinated and myelinated afferent pathways. The differences in cellular properties of these two classes of NTS neurons indicate clear functional differentiation at both the pre-and postsynaptic portions of these first synapses. By virtue of their position at the earliest stage of these pathways, such mechanistic differences probably impart important differentiation in the performance over the entire reflex pathways.

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Ketamine Differentially Blocks Sensory Afferent Synaptic Transmission in Medial Nucleus Tractus Solitarius (mNTS)

Cited by 36 publications

References 46 publications

Anandamide, Cannabinoid Type 1 Receptor, and NMDA Receptor Activation Mediate Non-Hebbian Presynaptically Expressed Long-Term Depression at the First Central Synapse for Visceral Afferent Fibers

Anandamide, Cannabinoid Type 1 Receptor, and NMDA Receptor Activation Mediate Non-Hebbian Presynaptically Expressed Long-Term Depression at the First Central Synapse for Visceral Afferent Fibers

Cranial Visceral Afferent Pathways through the Nucleus of the Solitary Tract to Caudal Ventrolateral Medulla or Paraventricular Hypothalamus: Target-Specific Synaptic Reliability and Convergence Patterns

Differentiation of autonomic reflex control begins with cellular mechanisms at the first synapse within the nucleus tractus solitarius

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