scholarly journals Presynaptic GABAergic receptors modulate inhibitory synaptic feedback in the avian cochlear nucleus angularis

2019 ◽  
Author(s):  
Stefanie L. Eisenbach ◽  
Sara E. Soueidan ◽  
Katrina M. MacLeod
Keyword(s):  
Brain Stem ◽  
Cochlear Nucleus ◽  
Gain Control ◽  
Short Term ◽  
Cochlear Nuclei ◽  
Inhibitory Circuitry ◽  
Inhibitory Feedback ◽  
Control Feedback ◽  
Olivary Nucleus ◽  
Nucleus Angularis

AbstractInhibition plays multiple critical roles in the neural processing of sound. In the avian auditory brain stem, the cochlear nuclei receive their principal inhibitory feedback from the superior olivary nucleus (SON) in lieu of local inhibitory circuitry. In the timing pathway, GABAergic inhibitory feedback underlies gain control to enhance sound localization. In the cochlear nucleus angularis (NA), which processes intensity information, how the inhibitory feedback is integrated is not well understood. Using whole cell patch-clamp recordings in chick brain stem slices, we investigated the effects of GABA release on the inhibitory (presumed SON) and excitatory (8th nerve) synaptic inputs onto NA neurons. Pharmacological activation of the metabotropic GABAB receptors with baclofen profoundly suppressed both evoked excitatory and inhibitory postsynaptic currents (EPSCs and IPSCs). Baclofen similarly reduced the frequency of spontaneous IPSCs and EPSCs, but had no significant effect on the current kinetics or amplitudes, indicating a presynaptic locus of modulation. Trains of IPSCs showed substantial transient and sustained short-term synaptic facilitation. Baclofen application reduced the initial IPSC amplitude, but enhanced the relative facilitation over the train via changes in release probability. Comparable levels of GABAB receptor mediated blockade also shifted short-term synaptic plasticity of EPSCs toward less depression. Evoked (but not spontaneous) release of GABA was sufficient to suppress basal release at inhibitory synapses in slices. Overall, the modulation of excitatory and inhibitory inputs of NA neurons via GABAB receptor activation appears to parallel that in the timing pathway.New and NoteworthyAvian cochlear nucleus angularis (NA) neurons are responsible for encoding sound intensity and provide level information for gain control feedback via the superior olivary nucleus. This GABAergic inhibitory feedback was itself modulated in NA via presynaptic, metabotropic GABAB receptor mediated suppression. Excitatory transmission was modulated by the same receptors, suggesting parallel homosynaptic and heterosynaptic mechanisms in both cochlear nuclei.

scholarly journals Spike threshold adaptation diversifies neuronal operating modes in the auditory brain stem

2019 ◽  
Vol 122 (6) ◽  
pp. 2576-2590
Author(s):  
Susan T. Lubejko ◽  
Bertrand Fontaine ◽  
Sara E. Soueidan ◽  
Katrina M. MacLeod
Keyword(s):  
Sodium Channel ◽  
Brain Stem ◽  
Cochlear Nucleus ◽  
Fine Tuning ◽  
Threshold Dynamics ◽  
Spike Threshold ◽  
Operating Modes ◽  
Auditory Brain Stem ◽  
Spike Initiation ◽  
Nucleus Angularis

Single neurons function along a spectrum of neuronal operating modes whose properties determine how the output firing activity is generated from synaptic input. The auditory brain stem contains a diversity of neurons, from pure coincidence detectors to pure integrators and those with intermediate properties. We investigated how intrinsic spike initiation mechanisms regulate neuronal operating mode in the avian cochlear nucleus. Although the neurons in one division of the avian cochlear nucleus, nucleus magnocellularis, have been studied in depth, the spike threshold dynamics of the tonically firing neurons of a second division of cochlear nucleus, nucleus angularis (NA), remained unexplained. The input-output functions of tonically firing NA neurons were interrogated with directly injected in vivo-like current stimuli during whole cell patch-clamp recordings in vitro. Increasing the amplitude of the noise fluctuations in the current stimulus enhanced the firing rates in one subset of tonically firing neurons (“differentiators”) but not another (“integrators”). We found that spike thresholds showed significantly greater adaptation and variability in the differentiator neurons. A leaky integrate-and-fire neuronal model with an adaptive spike initiation process derived from sodium channel dynamics was fit to the firing responses and could recapitulate >80% of the precise temporal firing across a range of fluctuation and mean current levels. Greater threshold adaptation explained the frequency-current curve changes due to a hyperpolarized shift in the effective adaptation voltage range and longer-lasting threshold adaptation in differentiators. The fine-tuning of the intrinsic properties of different NA neurons suggests they may have specialized roles in spectrotemporal processing. NEW & NOTEWORTHY Avian cochlear nucleus angularis (NA) neurons are responsible for encoding sound intensity for sound localization and spectrotemporal processing. An adaptive spike threshold mechanism fine-tunes a subset of repetitive-spiking neurons in NA to confer coincidence detector-like properties. A model based on sodium channel inactivation properties reproduced the activity via a hyperpolarized shift in adaptation conferring fluctuation sensitivity.

scholarly journals Computational Diversity in the Cochlear Nucleus Angularis of the Barn Owl

2003 ◽  
Vol 89 (4) ◽  
pp. 2313-2329 ◽  
Author(s):  
Christine Köppl ◽  
Catherine E. Carr
Keyword(s):  
Brain Stem ◽  
Cochlear Nucleus ◽  
Phase Locking ◽  
Sound Intensity ◽  
Nerve Fibers ◽  
Tuning Curves ◽  
Starting Point ◽  
Barn Owls ◽  
Different Response ◽  
Nucleus Angularis

The cochlear nucleus angularis (NA) is widely assumed to form the starting point of a brain stem pathway for processing sound intensity in birds. Details of its function are unclear, however, and its evolutionary origin and relationship to the mammalian cochlear-nucleus complex are obscure. We have carried out extracellular single-unit recordings in the NA of ketamine-anesthetized barn owls. The aim was to re-evaluate the extent of heterogeneity in NA physiology because recent studies of cellular morphology had established several distinct types. Extensive characterization, using tuning curves, phase locking, peristimulus time histograms and rate-level functions for pure tones and noise, revealed five major response types. The most common one was a primary-like pattern that was distinguished from auditory-nerve fibers by showing lower vector strengths of phase locking and/or lower spontaneous rates. Two types of chopper responses were found (chopper-transient and a rare chopper-sustained), as well as onset units. Finally, we routinely encountered a complex response type with a pronounced inhibitory component, similar to the mammalian typeIV. Evidence is presented that this range of response types is representative for birds and that earlier conflicting reports may be due to methodological differences. All five response types defined were similar to well-known types in the mammalian cochlear nucleus. This suggests convergent evolution of neurons specialized for encoding different behaviorally relevant features of the auditory stimulus. It remains to be investigated whether the different response types correlate with morphological types and whether they establish different processing streams in the auditory brain stem of birds.

scholarly journals A Role for Short-Term Synaptic Facilitation and Depression in the Processing of Intensity Information in the Auditory Brain Stem

2007 ◽  
Vol 97 (4) ◽  
pp. 2863-2874 ◽  
Author(s):  
K. M. MacLeod ◽  
T. K. Horiuchi ◽  
C. E. Carr
Keyword(s):  
Synaptic Plasticity ◽  
Brain Stem ◽  
Time Constant ◽  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Brain Slices ◽  
Fast Time ◽  
Short Term ◽  
Intensity Information

The nature of the synaptic connection from the auditory nerve onto the cochlear nucleus neurons has a profound impact on how sound information is transmitted. Short-term synaptic plasticity, by dynamically modulating synaptic strength, filters information contained in the firing patterns. In the sound-localization circuits of the brain stem, the synapses of the timing pathway are characterized by strong short-term depression. We investigated the short-term synaptic plasticity of the inputs to the bird's cochlear nucleus angularis (NA), which encodes intensity information, by using chick embryonic brain slices and trains of electrical stimulation. These excitatory inputs expressed a mixture of short-term facilitation and depression, unlike those in the timing nuclei that only depressed. Facilitation and depression at NA synapses were balanced such that postsynaptic response amplitude was often maintained throughout the train at high firing rates (>100 Hz). The steady-state input rate relationship of the balanced synapses linearly conveyed rate information and therefore transmits intensity information encoded as a rate code in the nerve. A quantitative model of synaptic transmission could account for the plasticity by including facilitation of release (with a time constant of ∼40 ms), and a two-step recovery from depression (with one slow time constant of ∼8 s, and one fast time constant of ∼20 ms). A simulation using the model fit to NA synapses and auditory nerve spike trains from recordings in vivo confirmed that these synapses can convey intensity information contained in natural train inputs.

Synaptic Physiology in the Cochlear Nucleus Angularis of the Chick

2005 ◽  
Vol 93 (5) ◽  
pp. 2520-2529 ◽  
Author(s):  
Katrina M. MacLeod ◽  
Catherine E. Carr
Keyword(s):  
Brain Stem ◽  
Time Constant ◽  
Auditory Nerve ◽  
Sound Intensity ◽  
Sound Recognition ◽  
Auditory Information ◽  
Decay Kinetics ◽  
Cochlear Nuclei ◽  
Auditory Brain Stem ◽  
Nucleus Angularis

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 μs 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 (∼110 vs. ∼55 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 ∼12.5 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.

Short-term adaptation of the pauser neuron in the dorsal cochlear nucleus of the cat

1987 ◽  
Vol 5 ◽  
pp. S15
Author(s):  
Teiji Tanahashi ◽  
Shigeisa Matsumuro ◽  
Shinji Kunushima
Keyword(s):  
Cochlear Nucleus ◽  
Dorsal Cochlear Nucleus ◽  
Short Term ◽  
Short Term Adaptation

scholarly journals Molecular Layer Inhibitory Interneurons Provide Feedforward and Lateral Inhibition in the Dorsal Cochlear Nucleus

2010 ◽  
Vol 104 (5) ◽  
pp. 2462-2473 ◽  
Author(s):  
Michael T. Roberts ◽  
Laurence O. Trussell
Keyword(s):  
Brain Stem ◽  
Lateral Inhibition ◽  
Cochlear Nucleus ◽  
Molecular Layer ◽  
Dorsal Cochlear Nucleus ◽  
Inhibitory Input ◽  
Auditory Information ◽  
Parallel Fibers ◽  
Sensory Inputs ◽  
Cartwheel Cells

In the outer layers of the dorsal cochlear nucleus, a cerebellum-like structure in the auditory brain stem, multimodal sensory inputs drive parallel fibers to excite both principal (fusiform) cells and inhibitory cartwheel cells. Cartwheel cells, in turn, inhibit fusiform cells and other cartwheel cells. At the microcircuit level, it is unknown how these circuit components interact to modulate the activity of fusiform cells and thereby shape the processing of auditory information. Using a variety of approaches in mouse brain stem slices, we investigated the synaptic connectivity and synaptic strength among parallel fibers, cartwheel cells, and fusiform cells. In paired recordings of spontaneous and evoked activity, we found little overlap in parallel fiber input to neighboring neurons, and activation of multiple parallel fibers was required to evoke or alter action potential firing in cartwheel and fusiform cells. Thus neighboring neurons likely respond best to distinct subsets of sensory inputs. In contrast, there was significant overlap in inhibitory input to neighboring neurons. In recordings from synaptically coupled pairs, cartwheel cells had a high probability of synapsing onto nearby fusiform cells or other nearby cartwheel cells. Moreover, single cartwheel cells strongly inhibited spontaneous firing in single fusiform cells. These synaptic relationships suggest that the set of parallel fibers activated by a particular sensory stimulus determines whether cartwheel cells provide feedforward or lateral inhibition to their postsynaptic targets.

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