Complementary control of sensory adaptation by two types of cortical interneurons

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Abstract

Reliably detecting unexpected sounds is important for environmental awareness and survival. By selectively reducing responses to frequently, but not rarely, occurring sounds, auditory cortical neurons are thought to enhance the brain's ability to detect unexpected events through stimulus-specific adaptation (SSA). The majority of neurons in the primary auditory cortex exhibit SSA, yet little is known about the underlying cortical circuits. We found that two types of cortical interneurons differentially amplify SSA in putative excitatory neurons. Parvalbumin-positive interneurons (PVs) amplify SSA by providing non-specific inhibition: optogenetic suppression of PVs led to an equal increase in responses to frequent and rare tones. In contrast, somatostatin-positive interneurons (SOMs) selectively reduce excitatory responses to frequent tones: suppression of SOMs led to an increase in responses to frequent, but not to rare tones. A mutually coupled excitatory-inhibitory network model accounts for distinct mechanisms by which cortical inhibitory neurons enhance the brain's sensitivity to unexpected sounds.

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Ryan Gregory Natan

Department of Otorhinolaryngology Head and Neck Surgery, Neuroscience Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, United States

Competing interests
The authors declare that no competing interests exist.
John J Briguglio

Department of Otorhinolaryngology Head and Neck Surgery, Neuroscience Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, United States

Competing interests
The authors declare that no competing interests exist.
Laetitia Mwilambwe-Tshilobo

Department of Otorhinolaryngology Head and Neck Surgery, Neuroscience Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, United States

Competing interests
The authors declare that no competing interests exist.
Sara Jones

Department of Otorhinolaryngology Head and Neck Surgery, Neuroscience Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, United States

Competing interests
The authors declare that no competing interests exist.
Mark Aizenberg

Department of Otorhinolaryngology Head and Neck Surgery, Neuroscience Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, United States

Competing interests
The authors declare that no competing interests exist.
Ethan M Goldberg

Department of Neurology, University of Pennsylvania, Philadelphia, United States

Competing interests
The authors declare that no competing interests exist.
Maria Neimark Geffen

Department of Otorhinolaryngology Head and Neck Surgery, Neuroscience Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, United States

For correspondence
mgeffen@med.upenn.edu

Competing interests
The authors declare that no competing interests exist.

Ethics

Animal experimentation: All experimental procedures are in accordance with NIH guidelines and approved by the IACUC at University of Pennsylvania (protocol number 803266).

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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.