Complementary control of sensory adaptation by two types of cortical interneurons.

Ryan G Natan,John J Briguglio,Laetitia Mwilambwe-Tshilobo,Sara I Jones,Ethan M Goldberg,Maria Neimark Geffen,Mark Aizenberg

doi:10.7554/elife.09868

Ryan G Natan, John J Briguglio + Show 5 more

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https://doi.org/10.7554/elife.09868

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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.

Highlights

Across sensory modalities, cortical neurons exhibit adaptation, attenuating their responses to redundant stimuli (Das and Gilbert, 1999; Ulanovsky et al, 2003; Garcia-Lazaro et al, 2007; Asari and Zador, 2009; Khatri et al, 2009)
stimulus-specific adaptation (SSA) was measured from the firing rate (FR) of neurons in response to tones presented as a series of ‘oddball’ stimuli
Optogenetic suppression of either positive interneurons (PVs) or somatostatin-positive interneurons (SOMs) led to a reduction in SSA in putative excitatory neurons (Figure 3)

Summary

Introduction

Cortical neurons exhibit adaptation, attenuating their responses to redundant stimuli (Das and Gilbert, 1999; Ulanovsky et al, 2003; Garcia-Lazaro et al, 2007; Asari and Zador, 2009; Khatri et al, 2009). In the primary auditory cortex (A1), the vast majority of neurons exhibit stimulus-specific adaptation (SSA, Figure 1). When presented with a sequence of two tones, one of which occurs frequently (termed ‘standard’) and another rarely (termed ‘deviant’), the neuron’s response to the standard tone becomes weaker, but the response to the deviant tone remains strong (Ulanovsky et al, 2003; Szymanski et al, 2009; Farley et al, 2010; Fishman and Steinschneider, 2012). Cortical circuits are proposed to contribute to and amplify SSA in A1 (Ulanovsky et al, 2003, Szymanski et al, 2009, Bauerle et al, 2011, Fishman and Steinschneider, 2012, Escera and Malmierca, 2014), through a combination of plastic modulation of thalamocortical inputs and intra-cortical inhibitory circuits, which would allow for

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