Modulation and control of synaptic transmission across the MNTB

Kopp-Scheinpflug, Cornelia; Steinert, Joern R.; Forsythe, Ian D.

doi:10.1016/j.heares.2011.02.007

Cited by 29 publications

(30 citation statements)

References 105 publications

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“…This suggests that the inhibitory pathways to the MSO are adapted for speed. Consistent with this, MNTB neurons receive powerful excitatory drive from the calyx of Held and have intrinsic physiology that allows rapid, reliable, and temporally precise firing (Kopp-Scheinpflug et al, 2011; Borst and Soria van Hoeve, 2012). However, direct recordings between synaptically coupled MNTB and MSO neurons have not been previously reported, leaving the timing and strength of MNTB inhibition of MSO neurons unresolved.…”

Section: Introductionmentioning

confidence: 67%

“…For the MNTB, it is reasonable to assume that the fast and reliable conversion of calyx of Held input into action potentials, as evidenced by strong phase locking to auditory stimuli in vivo , enables MNTB neurons to provide reliable and temporally precise inhibition to the MSO (for reviews, see Kopp-Scheinpflug et al, 2011; Borst and Soria van Hoeve, 2012). Our results suggest three reasons why inhibition from LNTB neurons might be more nuanced, particularly during sustained stimuli.…”

Section: Discussionmentioning

confidence: 99%

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The relative contributions of MNTB and LNTB neurons to inhibition in the medial superior olive assessed through single and paired recordings

Roberts¹,

Seeman²,

Golding³

2014

Front. Neural Circuits

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The medial superior olive (MSO) senses microsecond differences in the coincidence of binaural signals, a critical cue for detecting sound location along the azimuth. An important component of this circuit is provided by inhibitory neurons of the medial and lateral nuclei of the trapezoid body (MNTB and LNTB, respectively). While MNTB neurons are fairly well described, little is known about the physiology of LNTB neurons. Using whole cell recordings from gerbil brainstem slices, we found that LNTB and MNTB neurons have similar membrane time constants and input resistances and fire brief action potentials, but only LNTB neurons fire repetitively in response to current steps. We observed that LNTB neurons receive graded excitatory and inhibitory synaptic inputs, with at least some of the latter arriving from other LNTB neurons. To address the relative timing of inhibition to the MSO from the LNTB versus the MNTB, we examined inhibitory responses to auditory nerve stimulation using a slice preparation that retains the circuitry from the auditory nerve to the MSO intact. Despite the longer physical path length of excitatory inputs driving contralateral inhibition, inhibition from both pathways arrived with similar latency and jitter. An analysis of paired whole cell recordings between MSO and MNTB neurons revealed a short and reliable delay between the action potential peak in MNTB neurons and the onset of the resulting IPSP (0.55 ± 0.01 ms, n = 4, mean ± SEM). Reconstructions of biocytin-labeled neurons showed that MNTB axons ranged from 580 to 858 μm in length (n = 4). We conclude that while both LNTB and MNTB neurons provide similarly timed inhibition to MSO neurons, the reliability of inhibition from the LNTB at higher frequencies is more constrained relative to that from the MNTB due to differences in intrinsic properties, the strength of excitatory inputs, and the presence of feedforward inhibition.

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Section: Introductionmentioning

confidence: 67%

Section: Discussionmentioning

confidence: 99%

The relative contributions of MNTB and LNTB neurons to inhibition in the medial superior olive assessed through single and paired recordings

Roberts¹,

Seeman²,

Golding³

2014

Front. Neural Circuits

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“…Third, each inhibitory pathway contains a synapse specialized for short latency transmission. MNTB neurons receive input via the calyx of Held, the excitatory synapse from globular bushy cells that drives postsynaptic firing with high security (Mc Laughlin et al, 2008; Lorteije et al, 2009; Kopp-Scheinpflug et al, 2011; Borst and Soria van Hoeve, 2012). Calyceal synapses have been found on neurons in the posteroventral portion of the LNTB (Spirou et al, 1998), although their source has not yet been identified.…”

Section: Discussionmentioning

confidence: 99%

A Mechanistic Understanding of the Role of Feedforward Inhibition in the Mammalian Sound Localization Circuitry

Roberts

Seeman

Golding

2013

Neuron

131

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SUMMARY Feedforward inhibition sharpens the precision of neurons throughout ascending auditory pathways, including the binaural neurons of the medial superior olive (MSO). However, the biophysical influence of inhibition is poorly understood, particularly at higher frequencies where the relative phase of inhibition and excitation becomes ambiguous. Here, we show in gerbil MSO principal cells in vitro that feedforward inhibition precedes direct excitation, providing a concurrent hyperpolarization and conductance shunt during EPSP summation. We show with dual patch recordings and dynamic clamp that both the linearity and temporal fidelity of synaptic integration is improved by reducing Kv1 potassium channel conductance during inhibition, which counters membrane shunting even at high frequencies where IPSPs sum. The reduction of peak excitation by preceding inhibition lowers spike probability, narrowing but not shifting the window for detecting binaural coincidence. The interplay between inhibition and potassium conductances thus improves the consistency and resolution of ITD coding across different frequencies.

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“…The calyx of Held synapse thus works as a relay suited to providing reliable inhibitory signals (Borst and Soria van Hoeve, 2012). Interestingly, the generation of those signals is itself subject to modulation by glycinergic transmission (Kopp-Scheinpflug et al, 2011). Glycine released from inhibitory fibers exerts its effects in the MNTB via pre- and postsynaptic GlyRs.…”

Section: Introductionmentioning

confidence: 99%

Differential Distribution of Glycine Receptor Subtypes at the Rat Calyx of Held Synapse

et al. 2012

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The properties of glycine receptors (GlyRs) depend upon their subunit composition. While the prevalent adult forms of GlyRs are heteromers, previous reports suggested functional α homomeric receptors in mature nervous tissues. Here we show two functionally different GlyRs populations in the rat medial nucleus of trapezoid body (MNTB). Postsynaptic receptors formed α1/β containing clusters on somatodendritic domains of MNTB principal neurons, co-localizing with glycinergic nerve endings to mediate fast, phasic inhibitory postsynaptic currents (IPSCs). By contrast, presynaptic receptors on glutamatergic calyx of Held terminals were composed of dispersed, homomeric α1 receptors. Interestingly, the parent cell bodies of the calyces of Held, the globular bushy cells (GBCs) of the cochlear nucleus, expressed somatodendritic receptors (α1/β heteromers) and showed similar clustering and pharmacological profile as GlyRs on MNTB principal cells. These results suggest that specific targeting of glycine receptor β subunit produces segregation of GlyR subtypes involved in two different mechanisms of modulation of synaptic strength.

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Modulation and control of synaptic transmission across the MNTB

Cited by 29 publications

References 105 publications

The relative contributions of MNTB and LNTB neurons to inhibition in the medial superior olive assessed through single and paired recordings

The relative contributions of MNTB and LNTB neurons to inhibition in the medial superior olive assessed through single and paired recordings

A Mechanistic Understanding of the Role of Feedforward Inhibition in the Mammalian Sound Localization Circuitry

Differential Distribution of Glycine Receptor Subtypes at the Rat Calyx of Held Synapse

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