Synaptic pharmacology of the superior olivary complex studied in mouse brain slice

Wu, Shu Hui; Kelly, Jack B.

doi:10.1523/jneurosci.12-08-03084.1992

Cited by 87 publications

(59 citation statements)

References 87 publications

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“…These PSPs had onset latencies of 5.5±0.8 ms (n = 6) in P1-P2 mice and 5.0±0.5 ms (n = 13) in P4-P7 mice. These values are comparable to those reported for newborn rats [11] and gerbils [15] and about 3 ms longer than the latencies reported for 3-week-old mice [17]. In slices prepared from P1 and P2 mice MNTB-evoked PSPs (recorded in perforatedpatch mode) were always depolarizing from the resting membrane potential (n = 8, V rest −51.8 ± 1.4 mV) (Fig.…”

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confidence: 88%

Glycinergic/GABAergic synapses in the lateral superior olive are excitatory in neonatal C57Bl/6J mice

Kullmann

Kandler

2001

Developmental Brain Research

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The lateral superior olive (LSO), a nucleus involved in sound localization, receives tonotopically organized, inhibitory input from the medial nucleus of the trapezoid body (MNTB). To better understand the development of this glycinergic/GABAergic pathway, we used Gramicidinperforated patch clamp recordings to characterize MNTB-evoked postsynaptic potentials in LSO neurons of neonatal C57Bl/6J mice. We found that during the first postnatal week, MNTB-evoked responses change from being depolarizing to being hyperpolarizing. Most interestingly, depolarizing glycinergic/GABAergic synaptic potentials were able to trigger action potentials, demonstrating that the MNTB-LSO pathway can act as a true excitatory pathway. This transient excitatory action of immature MNTB-LSO synapses might play an important role in activitydependent sharpening of the tonotopic organization of inhibitory connections in the LSO. KeywordsBrainstem slice; Auditory system; Development; Sound localization; ChlorideThe lateral superior olive (LSO) is the first binaural nucleus in the ascending auditory pathway of mammals. Neurons in the LSO encode interaural intensity differences and thus play an important role in localizing sound in space (for a review see [1]). Information from the contralateral ear reaches the LSO via a highly tonotopically organized, inhibitory pathway that arises in the medial nucleus of the trapezoid body (MNTB). This MNTB-LSO pathway uses the neurotransmitter glycine and, in neonatal animals, also uses GABA [12]. During early postnatal development, the spatial connectivity pattern of this inhibitory MNTB-LSO pathway is sharpened by activity-dependent mechanisms resulting in the precise tonotopic organization seen in adult animals (for review see [15,16]). During the first postnatal week, glycinergic/GABAergic MNTB-LSO synapses are not hyperpolarizing as in adult animals, but are depolarizing due to a high internal chloride concentration of LSO neurons [7,11]. It has been suggested that this depolarization renders the MNTB pathway excitatory and that the excitatory nature is part of the mechanism by which activity in the MNTB-LSO pathways exerts its effect on neuronal growth, survival, and synaptic In the present study, we examined whether and at what age the MNTB-LSO pathway is depolarizing and whether it can elicit action potentials in LSO neurons of mice. While the development of the MNTB-LSO pathway has been intensively studied in rats and gerbils [16], very little is known about its development in mice. However, as the mouse has become a favored species for developmental studies due to its genetic possibilities, information about the immature MNTB-LSO pathway in mice has become important.Experiments were performed in C57Bl/6J mice (Jackson Laboratory, Bar Harbor, ME). Experimental procedures were in accordance with NIH guidelines and were approved by the IACUC at the University of Pittsburgh. Coronal slices (250 µm thick) of the auditory brainstem were prepared from animals aged postnatal day (P) 1-P7 as previ...

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confidence: 88%

Glycinergic/GABAergic synapses in the lateral superior olive are excitatory in neonatal C57Bl/6J mice

Kullmann

Kandler

2001

Developmental Brain Research

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“…In the present study, similar signals were observed when using electrodes with impedances of approximately 6 MW. An increase in electrode impedance resulted in the signal waveforms becoming more biphasic, similar to the waveforms shown by Wu and Kelly (1992).…”

Section: Complex Waveforms In Mntb Unit Dischargesmentioning

confidence: 54%

“…The waveforms of the extracellularly recorded pre&action potential compounds described in these previous studies differed somewhat from each other, but these differences most probably only reflect different recording conditions (Pfeiffer 1966;Guinan and Li 1990;Wu and Kelly 1992). The form and the polarity of extracellularly recorded signals depend on the input impedance of the recording electrode and also on the spatial relation between the tip of the electrode and the recorded neuron.…”

Section: Complex Waveforms In Mntb Unit Dischargesmentioning

confidence: 83%

“…By using retrograde electrical stimulation while recording from the MNTB of cats, they were able to selectively evoke only the postsynaptic component of the signal complexes (Guinan and Li 1990). Wu and Kelly (1992) subsequently succeeded in showing that the prepotential reflected the discharge activity of the presynaptic calyx. Their study was based on orthodromic electrical stimulation and extracellular recordings from MNTB neurons in mouse brain slices.…”

Section: Complex Waveforms In Mntb Unit Dischargesmentioning

confidence: 96%

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The Medial Nucleus of the Trapezoid Body in the Gerbil Is More Than a Relay: Comparison of Pre- and Postsynaptic Activity

Kopp-Scheinpflug

Lippe

Dörrscheidt

et al. 2003

JARO - Journal of the Association for Research in Otolaryngolog

114

158

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The medial nucleus of the trapezoid body (MNTB) plays an important role in the processing of interaural intensity differences, a feature that is critical for the localization of sound sources. It is generally believed that the MNTB functions primarily as a passive relay in converting excitatory input originating from the contralateral cochlear nucleus (CN) into an inhibitory input to the ipsilateral lateral superior olive. However, studies showing that the MNTB itself is also the target of inhibitory input suggest that the MNTB may serve more than a sign-converting function. To examine the fidelity of signal transmission at the CN-MNTB synapse, presynaptic calyceal potentials (''prepotentials''), reflecting the excitatory input to the MNTB neuron, and postsynaptic action potentials were simultaneously monitored with the same electrode during in vivo extracellular recordings from the gerbil's MNTB. Presynaptic activity differed from postsynaptic activity in several respects: (1) Spontaneous and sound-evoked discharge rates were greater presynaptically than postsynaptically. (2) Frequency tuning was sharper postsynaptically than presynaptically. (3) Calyceal terminals and MNTB neurons both showed phasic-tonic response patterns to tonal stimulation, but the duration of the onset response and the level of the tonic component were reduced postsynaptically. (4) Phase-locking to sound frequencies up to 1 kHz was greater postsynaptically than presynaptically. (5) The rate-intensity characteristics of pre-and postsynaptic activities differed significantly from each other in half of the MNTB neurons. To test the hypothesis that acoustically evoked inhibition of MNTB neurons contributed to the relatively lower levels of postsynaptic discharge, two-tone stimulation was applied, wherein the response to one tone-burst, set at the neuron's characteristic frequency, can be reduced by addition of a second ''inhibitory'' tone. The inhibitory tone caused a much larger reduction in post-than in presynaptic activity, indicating an acoustically evoked inhibitory influence directly on MNTB units. These findings show that transmission at the CN-MNTB synapse does not occur in a fixed one-to-one manner and that the response of MNTB neurons reflects the integration of their excitatory and inhibitory inputs.

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“…The neurotransmitter released by the calyx of Held onto the principal neuron is glutamate (Banks and Smith 1992;Wu and Kelly 1992). Released glutamate activates AMPA and, depending on the age of the animal (Futai et al 2001; Values are means Ϯ SD.…”

Section: All Inputs Mediated By Ampa Receptorsmentioning

confidence: 99%

Multiple Large Inputs to Principal Cells in the Mouse Medial Nucleus of the Trapezoid Body

Bergsman¹,

Camilli²,

McCormick³

2004

Journal of Neurophysiology

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The calyx of Held is a giant nerve terminal that forms a synapse directly onto the principal cells of the medial nucleus of the trapezoid body (MNTB) in the mammalian auditory brain stem. This central synapse, which is involved in sound localization, has become widely used for studying synaptic transmission. Anatomical studies of this nucleus have indicated that each principal cell is innervated by only one calyx. Here we use previously established electrophysiological criteria of excitatory postsynaptic current amplitude, kinetics, and transmitter type, as well as other characteristics commonly reported for this synapse, to examine the input properties of principal neurons. Our findings indicate that some principal cells receive more than one strong excitatory input. These inputs meet previously established electrophysiological criteria for identification as calyceal nerve terminals. Implications for the execution and analysis of experiments to avoid errors due to such multiple inputs are discussed.

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Synaptic pharmacology of the superior olivary complex studied in mouse brain slice

Cited by 87 publications

References 87 publications

Glycinergic/GABAergic synapses in the lateral superior olive are excitatory in neonatal C57Bl/6J mice

Glycinergic/GABAergic synapses in the lateral superior olive are excitatory in neonatal C57Bl/6J mice

The Medial Nucleus of the Trapezoid Body in the Gerbil Is More Than a Relay: Comparison of Pre- and Postsynaptic Activity

Multiple Large Inputs to Principal Cells in the Mouse Medial Nucleus of the Trapezoid Body

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