A novel class of inferior colliculus principal neurons labeled in vasoactive intestinal peptide-cre mice

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Abstract

Located in the midbrain, the inferior colliculus (IC) is the hub of the central auditory system. Although the IC plays important roles in speech processing, sound localization, and other auditory computations, the organization of the IC microcircuitry remains largely unknown. Using a multifaceted approach in mice, we have identified vasoactive intestinal peptide (VIP) neurons as a novel class of IC principal neurons. VIP neurons are glutamatergic stellate cells with sustained firing patterns. Their extensive axons project to long-range targets including the auditory thalamus, auditory brainstem, superior colliculus, and periaqueductal gray. Using optogenetic circuit mapping, we found that VIP neurons integrate input from the contralateral IC and the dorsal cochlear nucleus. The dorsal cochlear nucleus also drove feedforward inhibition to VIP neurons, indicating that inhibitory circuits within the IC shape the temporal integration of ascending inputs. Thus, VIP neurons are well-positioned to influence auditory computations in a number of brain regions.

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All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 3, 4, 5, 7, and 8 and Table 2.

Article and author information

Author details

David Goyer

Kresge Hearing Research Institute, Department of Otolaryngology - Head and Neck Surgery, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Marina Augusto Silveira

Kresge Hearing Research Institute, Department of Otolaryngology - Head and Neck Surgery, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Alexander P George

Kresge Hearing Research Institute, Department of Otolaryngology - Head and Neck Surgery, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Nichole L Beebe

Department of Anatomy and Neurobiology, Northeast Ohio Medical University, Rootstown, United States

Competing interests
The authors declare that no competing interests exist.
Ryan M Edelbrock

Department of Anatomy and Neurobiology, Northeast Ohio Medical University, Rootstown, United States

Competing interests
The authors declare that no competing interests exist.
Peter T Malinski

Kresge Hearing Research Institute, Department of Otolaryngology - Head and Neck Surgery, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Brett R Schofield

Department of Anatomy and Neurobiology, Northeast Ohio Medical University, Rootstown, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-0875-7759
Michael Thomas Roberts

Kresge Hearing Research Institute, Department of Otolaryngology - Head and Neck Surgery, University of Michigan, Ann Arbor, United States

For correspondence
microb@umich.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-2835-8752

Funding

Deutsche Forschungsgemeinschaft (401540516)

David Goyer

Hearing Health Foundation (Emerging Research Grant)

Michael Thomas Roberts

National Institutes of Health (DC016880)

Michael Thomas Roberts

National Institutes of Health (DC004391)

Brett R Schofield

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experiments were approved by the University of Michigan Institutional Animal Care and Use Committee (protocol # PRO00006642 and PRO00008773) and were in accordance with NIH guidelines for the care and use of laboratory animals.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.