Abstract

Contrast gain control is the systematic adjustment of neuronal gain in response to the contrast of sensory input. It is widely observed in sensory cortical areas and has been proposed to be a canonical neuronal computation. Here, we investigated whether shunting inhibition from parvalbumin-positive interneurons—a mechanism involved in gain control in visual cortex—also underlies contrast gain control in auditory cortex. First, we performed extracellular recordings in the auditory cortex of anesthetized male mice and optogenetically manipulated the activity of parvalbumin-positive interneurons while varying the contrast of the sensory input. We found that both activation and suppression of parvalbumin interneuron activity altered the overall gain of cortical neurons. However, despite these changes in overall gain, we found that manipulating parvalbumin interneuron activity did not alter the strength of contrast gain control in auditory cortex. Furthermore, parvalbumin-positive interneurons did not show increases in activity in response to high-contrast stimulation, which would be expected if they drive contrast gain control. Finally, we performed in vivo whole-cell recordings in auditory cortical neurons during high- and low-contrast stimulation and found that no increase in membrane conductance was observed during high-contrast stimulation. Taken together, these findings indicate that while parvalbumin-positive interneuron activity modulates the overall gain of auditory cortical responses, other mechanisms are primarily responsible for contrast gain control in this cortical area.NEW & NOTEWORTHY We investigated whether contrast gain control is mediated by shunting inhibition from parvalbumin-positive interneurons in auditory cortex. We performed extracellular and intracellular recordings in mouse auditory cortex while presenting sensory stimuli with varying contrasts and manipulated parvalbumin-positive interneuron activity using optogenetics. We show that while parvalbumin-positive interneuron activity modulates the gain of cortical responses, this activity is not the primary mechanism for contrast gain control in auditory cortex.

Highlights

  • Contrast gain control is a common computational principle in multiple sensory systems (Carandini and Heeger 2012)

  • We investigated whether shunting inhibition from positive interneurons (PVIs) or fluctuations in membrane potential contribute mechanistically to contrast gain control in mouse auditory cortex

  • We investigated the biophysical basis of contrast gain control in mouse auditory cortex by examining the potential involvement of two mechanisms: PVI-mediated shunting inhibition and membrane potential variability

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Summary

Introduction

Contrast gain control is a common computational principle in multiple sensory systems (Carandini and Heeger 2012). In primary visual cortex (V1), gain control has been attributed to a combination of inhibition from parvalbumin (PV)-positive interneurons (PVIs; Atallah et al 2012; Wilson et al 2012), shunting inhibition (Carandini and Heeger 1994; Carandini et al 1997), fluctuations in membrane potential (Finn et al 2007), and synaptic depression. Each of these mechanisms could contribute to contrast gain control in auditory cortex

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