Rapidly Deactivating AMPA Receptors Determine Excitatory Synaptic Transmission to Interneurons in the Nucleus Tractus Solitarius From Rat

Titz, Stefan; Keller, Bernhard U.

doi:10.1152/jn.1997.78.1.82

Cited by 34 publications

(61 citation statements)

References 41 publications

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“…These "auditory" currents (Parks 2000) are faster than most AMPAR-mediated currents reported from many other areas in the brain, which have decay time constants of several milliseconds or more. These include synapses in hippocampus (Hestrin et al 1990;Jonas et al 1993;Walker et al 2002), cerebellum (Llano et al 1991;Silver et al 1992), neocortex (Hestrin 1992(Hestrin , 1993Stern et al 1992), and nonauditory brain stem (Raman et al 1994;Titz and Keller 1997), with few exceptions (but see Silver et al 1996). Even using techniques designed to circumvent voltage-clamp error (Häusser and Roth 1997;Walker et al 2002), most decay time constants of EPSCs recorded outside the auditory brain stem are not in the submillisecond range.…”

Section: Discussionmentioning

confidence: 99%

Synaptic Physiology in the Cochlear Nucleus Angularis of the Chick

MacLeod

Carr²

2005

Journal of Neurophysiology

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. Nucleus angularis (NA), one of the two cochlear nuclei in birds, is important for processing sound intensity for localization and most likely has role in sound recognition and other auditory tasks. Because the synaptic properties of auditory nerve inputs to the cochlear nuclei are fundamental to the transformation of auditory information, we studied the properties of these synapses onto NA neurons using whole cell patch-clamp recordings from auditory brain stem slices from embryonic chickens (E16 -E20). We measured spontaneous excitatory postsynaptic currents (EPSCs), and evoked EPSCs and excitatory postsynaptic potentials (EPSPs) by using extracellular stimulation of the auditory nerve. These excitatory EPSCs were mediated by AMPA and N-methyl-D-aspartate (NMDA) receptors. The spontaneous EPSCs mediated by AMPA receptors had submillisecond decay kinetics (556 s at E19), comparable with those of other auditory brain stem areas. The spontaneous EPSCs increased in amplitude and became faster with developmental age. Evoked EPSC and EPSP amplitudes were graded with stimulus intensity. The average amplitude of the EPSC evoked by minimal stimulation was twice as large as the average spontaneous EPSC amplitude (ϳ110 vs. ϳ55 pA), suggesting that single fibers make multiple contacts onto each postsynaptic NA neuron. Because of their small size, minimal EPSPs were subthreshold, and we estimate at least three to five inputs were required to reach threshold. In contrast to the fast EPSCs, EPSPs in NA had a decay time constant of ϳ12.5 ms, which was heavily influenced by the membrane time constant. Thus NA neurons spatially and temporally integrate auditory information arriving from multiple auditory nerve afferents. I N T R O D U C T I O NThe synaptic properties of auditory nerve inputs onto their postsynaptic targets in the cochlear nuclei are fundamental to the transformation of auditory information. In birds, acoustic cues for sound localization are segregated into parallel streams: in vivo recordings showed that cochlear nucleus magnocellularis (NM) encodes timing cues, whereas cochlear nucleus angularis (NA) encodes intensity cues (Konishi et al. 1985;Sullivan and Konishi 1984;Takahashi et al. 1984). Recent work studying the morphology, physiology, and auditory responses in NA suggest that this nucleus is also important for encoding sound for nonlocalization tasks, such as sound recognition and discrimination (Köppl and Carr 2003;.At the brain stem level, the cellular and synaptic specializations that allow temporal coding of sound phase for the computation of interaural time differences are well understood (Carr et al. 2001;Trussell 1999). Studies of nucleus magnocellularis neurons have revealed a suite of anatomical and physiological specializations that enable the precise encoding of the temporal properties of auditory nerve inputs, including large, calyceal synapses, very fast AMPA receptor (AMPAR)-mediated synaptic currents, short membrane time constants, and fast synaptic potentials (Carr et al. 2001;Jhaveri an...

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Section: Discussionmentioning

confidence: 99%

Synaptic Physiology in the Cochlear Nucleus Angularis of the Chick

MacLeod

Carr²

2005

Journal of Neurophysiology

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“…9), moving the stimulation electrode off of the visible ST resulted in either no response or an elevation in threshold shock intensity for evoking the same response, a finding consistent with greater current intensity required to spread from the off-ST site to reach the same axon within the ST. When stimulation electrodes are placed quite close (ϳ150 m) to NTS neurons in transverse slices (20,77), shocks commonly recruit both EPSCs and monosynaptic inhibitory postsynaptic currents (IPSCs, i.e., local nonafferent axons) (18,77).…”

Section: Second-order Baroreceptive Nts Neurons Receive Reliable Lowmentioning

confidence: 99%

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

Andresen

Peters

2008

American Journal of Physiology-Heart and Circulatory Physiology

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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...

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“…Because the stimulation electrode was placed 1-3 mm from the site of the recorded neuron soma, we minimized the possibility of direct focal stimulation of non-ST axons [Doyle et al (2004), their Fig. 1] or local cell bodies (Titz and Keller, 1997). The second-order neurons were identified using jitter (Ͻ150 sec), synaptic failure rates, and ionotropic GluR antagonists as described previously Doyle et al, 2004).…”

Section: Nts Slicesmentioning

confidence: 99%

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

Jin¹,

Bailey²,

Andresen³

2004

J. Neurosci.

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The balance between excitation and inhibition dictates central integration. Glutamatergic and GABAergic neurotransmission dominate this process. Cranial primary afferents enter the brainstem to release glutamate (Glu) onto second-order neurons within the caudal nucleus tractus solitarius (NTS) to initiate autonomic reflexes. The simplest pathways for these reflexes contain as few as two central neurons, but display robust frequency-dependent behavior. Within NTS, multiple metabotropic Glu receptors (mGluRs) are present, but their roles are poorly understood. Using synaptically discriminated second-order NTS neurons in brainstem slices and mechanically dissociated NTS neurons with intact boutons, we show that Glu differentially controls GABA release via distinct presynaptic mGluRs. In second-order NTS neurons recorded in slices, activation of primary afferents at frequencies as low as 10 shocks per second released sufficient Glu to alter rates of spontaneous IPSCs (sIPSCs). In both approaches, group I mGluRs increased GABA release in some neurons, but, on different neurons, group II and group III mGluRs decreased the sIPSC rate. mGluR actions were remarkably rapid, with onset and reversal beginning within 100 msec. In all cases, mGluR actions were exclusively presynaptic, and mGluRs did not alter postsynaptic properties in second-order neurons in either slices or isolated neurons. Tests with capsaicin and ␣␤-methylene ATP suggest that myelinated and unmyelinated afferent pathways engage both mGluR-GABA mechanisms. Afferent Glu spillover provides heterosynaptic cross talk with GABAergic inhibition in NTS. This process may critically shape the dynamic character and use dependence for cranial afferent transmission at the first stage of autonomic reflexes.

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Rapidly Deactivating AMPA Receptors Determine Excitatory Synaptic Transmission to Interneurons in the Nucleus Tractus Solitarius From Rat

Cited by 34 publications

References 41 publications

Synaptic Physiology in the Cochlear Nucleus Angularis of the Chick

Synaptic Physiology in the Cochlear Nucleus Angularis of the Chick

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

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

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