Inhibitory Neural Circuits in the Mammalian Auditory Midbrain

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Abstract

The auditory midbrain is the critical integration center in the auditory pathway of vertebrates. Synaptic inhibition plays a key role during information processing in the auditory midbrain, and these inhibitory neural circuits are seen in all vertebrates and are likely essential for hearing. Here, we review the structure and function of the inhibitory neural circuits of the auditory midbrain. First, we provide an overview on how these inhibitory circuits are organized within different clades of vertebrates. Next, we focus on recent findings in the mammalian auditory midbrain, the most studied of the vertebrates, and discuss how the mammalian auditory midbrain is functionally coordinated.

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Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex.

Aaron M. Kerlin, Mark Andermann, Vladimir K. Berezovskii … (2010)

Different subtypes of GABAergic neurons in sensory cortex exhibit diverse morphology, histochemical markers, and patterns of connectivity. These subtypes likely play distinct roles in cortical function, but their in vivo response properties remain unclear. We used in vivo calcium imaging, combined with immunohistochemical and genetic labels, to record visual responses in excitatory neurons and up to three distinct subtypes of GABAergic neurons (immunoreactive for parvalbumin, somatostatin, or vasoactive intestinal peptide) in layer 2/3 of mouse visual cortex. Excitatory neurons had sharp response selectivity for stimulus orientation and spatial frequency, while all GABAergic subtypes had broader selectivity. Further, bias in the responses of GABAergic neurons toward particular orientations or spatial frequencies tended to reflect net biases of the surrounding neurons. These results suggest that the sensory responses of layer 2/3 GABAergic neurons reflect the pooled activity of the surrounding population--a principle that may generalize across species and sensory modalities. 2010 Elsevier Inc. All rights reserved.

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Spontaneous events outline the realm of possible sensory responses in neocortical populations.

Artur Luczak, Péter Barthó, Kenneth D M Harris (2009)

Neocortical assemblies produce complex activity patterns both in response to sensory stimuli and spontaneously without sensory input. To investigate the structure of these patterns, we recorded from populations of 40-100 neurons in auditory and somatosensory cortices of anesthetized and awake rats using silicon microelectrodes. Population spike time patterns were broadly conserved across multiple sensory stimuli and spontaneous events. Although individual neurons showed timing variations between stimuli, these were not sufficient to disturb a generally conserved sequential organization observed at the population level, lasting for approximately 100 ms with spiking reliability decaying progressively after event onset. Preserved constraints were also seen in population firing rate vectors, with vectors evoked by individual stimuli occupying subspaces of a larger but still constrained space outlined by the set of spontaneous events. These results suggest that population spike patterns are drawn from a limited "vocabulary," sampled widely by spontaneous events but more narrowly by sensory responses.

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Dendritic integration of excitatory synaptic input.

Jeffrey Magee (2000)

A fundamental function of nerve cells is the transformation of incoming synaptic information into specific patterns of action potential output. An important component of this transformation is synaptic integration--the combination of voltage deflections produced by a myriad of synaptic inputs into a singular change in membrane potential. There are three basic elements involved in integration: the amplitude of the unitary postsynaptic potential; the manner in which non-simultaneous unitary events add in time (temporal summation), and the addition of unitary events occurring simultaneously in separate regions of the dendritic arbor (spatial summation). This review discusses how passive and active dendritic properties, and the functional characteristics of the synapse, shape these three elements of synaptic integration.

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Author and article information

Journal

Journal ID (nlm-ta): J Exp Neurosci

Journal ID (iso-abbrev): J Exp Neurosci

Journal ID (publisher-id): EXN

Journal ID (hwp): spexn

Title: Journal of Experimental Neuroscience

Publisher: SAGE Publications (Sage UK: London, England )

ISSN (Electronic): 1179-0695

Publication date (Electronic): 12 December 2018

Publication date Collection: 2018

Volume: 12

Electronic Location Identifier: 1179069518818230

Affiliations

[1 ]Department of Physiology, School of Medicine, Kanazawa Medical University, Uchinada, Japan

[2 ]Department of Anatomy, School of Medicine, Kanazawa Medical University, Uchinada, Japan

Author notes

[*]Munenori Ono, Department of Physiology, School of Medicine, Kanazawa Medical University, Uchinada 920-0293, Ishikawa, Japan. Email: onomn@ 123456kanazawa-med.ac.jp

Author information

Munenori Ono https://orcid.org/0000-0003-4516-9283

Article

Publisher ID: 10.1177_1179069518818230 Publisher-manuscript ID: EXN-18-0042.R1

DOI: 10.1177/1179069518818230

PMC ID: 6291857

SO-VID: 2ed4478e-57e5-442b-9ecc-5f59b5f8980b

License:

This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License ( http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages ( https://us.sagepub.com/en-us/nam/open-access-at-sage).

History

Date received : 7 June 2018

Date accepted : 15 November 2018

Funding

Funded by: Japan Society for the Promotion of Science, FundRef https://doi.org/10.13039/501100001691;

Award ID: 16H01501

Funded by: Japan Society for the Promotion of Science, FundRef https://doi.org/10.13039/501100001691;

Award ID: 16K07026

Funded by: Japan Society for the Promotion of Science, FundRef https://doi.org/10.13039/501100001691;

Award ID: JP16K11200

Funded by: Takahashi Industrial and Economic Research Foundation, FundRef https://doi.org/10.13039/100008965;

Funded by: Kanazawa Medical University, FundRef https://doi.org/10.13039/501100004043;

Award ID: S2016-8

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cover-date January-December 2018

Keywords: auditory pathway,midbrain,inhibitory neural circuits,synaptic inputs

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Keywords: auditory pathway, midbrain, inhibitory neural circuits, synaptic inputs

Inhibitory Neural Circuits in the Mammalian Auditory Midbrain

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Abstract

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BIO Integration

Most cited references 140

Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex.

Spontaneous events outline the realm of possible sensory responses in neocortical populations.

Dendritic integration of excitatory synaptic input.

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