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

Abstract

Andresen MC, Peters JH. Comparison of baroreceptive to other afferent synaptic transmission to the medial solitary tract nucleus. Am J Physiol Heart Circ Physiol 295: H2032-H2042, 2008. First published September 12, 2008 doi:10.1152/ajpheart.00568.2008.-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., ADNϩ) and measured synaptic responses to solitary tract (ST) activation recorded from dye-identified neurons in medial NTS in horizontal brain stem slices. Every ADNϩ NTS neuron received constant-latency STevoked excitatory postsynaptic currents (EPSCs) (jitter Ͻ192 s, 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 ADNϩ EPSCs averaged ϳ70% for five shocks at 50 Hz, but single-shock failure rates did not exceed 4%. Whether adjacent ADNϪ or those from unlabeled animals, other second-order NTS neurons (jitters Ͻ200 s) had ST transmission properties indistinguishable from ADNϩ. 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 ADNϩ 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 frequencydependent 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). myelinated; unmyelinated; C-fibers; capsaicin; quantal release; glutamate; convergence VISCERAL AFFERENTS, THE IX and Xth cranial nerves, enter the brain at the solitary tract nucleus (NTS) (5). These afferents provide information for vital homeostatic reflexes that coordinate systemic control of cardiovascular, respiratory, and gastrointestinal function, as well as visceral aspects of integrated satiety, body temperature, neuroendocrine, and stress responses (19,24,41,67). These diverse afferents belong to two broad classes, those with myelinated or unmyelinated axons, and each class distinctively expresses characteristic ion channels and receptors (32,43,48). Patterns of the distribution of afferent fibers outline a loose viscerotopy (46, 52). However, cellular heterogeneity, even within NTS subregions, is substantial and includes varied afferent so...

Kv1.3 channels regulate synaptic transmission in the nucleus of solitary tract

“…Interestingly, the evoked EPSCs that were not altered by MgTx were significantly larger in amplitude than those that were. Data from Andresen and Peters (2008) support the conclusion that the larger nonresponsive EPSCs in our study were present in neurons innervated by A-or Ah-type fibers. Those authors compared the peak amplitudes of capsaicin-resistant tract evoked EPSCs, presumably innervated by myelinated fibers, with capsaicin-sensitive EPSCs, innervated by C-type unmyelinated fibers.…”

Influence of Vagotomy on Monosynaptic Transmission at Second-Order Nucleus Tractus Solitarius Synapses

“…The existence of two failure-type populations of synapses in the rat NTS is in accord with observations recently reported by Andresen and Peters (2008). Outside of the decreased amplitude of the initial evEPSC in high-failure synapses and the longer latency of high-failure synapses, all other tested electrophysiological parameters of these two synaptic populations were identical.…”

“…Bailey et al 2008), the subsequent four evEPSCs not only progressively decrease in amplitude but have a higher probability of failure. The degree of synaptic failure exhibited during the 50-Hz train of stimuli has been used to define two separate classes of monosynaptic EPSCs evoked by electrical ST stimulation (Andresen and Peters 2008). In accordance with this previous study, we designated synapses with less than a 5% failure rate as "low-failure synapses" and those with a failure rate equal to or over 5% as "high-failure synapses."…”

H2O2 induces delayed hyperexcitability in nucleus tractus solitarii neurons

“…Likewise, the lack of effect on PPR, use-dependent depression, as well as asynchronous and miniature EPSC frequency suggests that H 2 O 2 did not alter glutamate release from TS terminals. Across all cells tested, H 2 O 2 also did not alter TS-EPSCs regardless of initial current amplitude or failure rate (not shown), indicators of synapses containing myelinated (A-type) or unmyelinated (C-type) afferents (Andresen and Peters, 2008), suggesting the H 2 O 2 response was not fiber type specific. Conversely, 500 μM H 2 O 2 decreased sEPSC frequency, but not amplitude, in the neurons studied.…”