Parvalbumin interneuron ErbB4 controls ongoing network oscillations and olfactory behaviours in mice

Abstract

Parvalbumin (PV)-positive interneurons modulate the processing of odour information. However, little is known about how PV interneurons dynamically remodel neural circuit responses in the olfactory bulb (OB) and their physiological significance. This study showed that a reinforced odour-discrimination task upregulated ErbB4 kinase activity in the mouse OB. ErbB4 knockout in the OB impaired the dishabituation of odour responses and discrimination of complex odours, whereas odour memory or adaptation was not altered in mice. ErbB4-positive neurones were localised throughout the OB, whereas ErbB4 was largely expressed in PV-positive interneurons within the internal and external plexiform layers. Similarly, ErbB4 ablation in PV interneurons disrupted olfactory discrimination and dishabituation in mice. ErbB4 knockout in PV interneurons disrupted the odour-evoked responses of mitral/tufted cells and increased the power of the ongoing local field potential in awake mice. We also observed a decrease in the frequency of miniature inhibitory postsynaptic currents and deficits in stimulus-evoked recurrent and lateral inhibition of mitral cells following PV-ErbB4 loss, suggesting a broad impairment in inhibitory microcircuits. These findings demonstrate that PV-ErbB4 signalling regulates inhibitory microcircuit activity, ongoing oscillations, and OB output, which underlie normal olfactory behaviour.