Receptive fields of sensory cortical neurons are plastic, changing in response to alterations of neural activity or sensory experience1,2,3,4,5,6,7,8,9,10,11,12. In this way, cortical representations of the sensory environment can incorporate new information about the world, depending on the relevance or value of particular stimuli1,6,9. Neuromodulation is required for cortical plasticity, but it is uncertain how subcortical neuromodulatory systems, such as the cholinergic nucleus basalis, interact with and refine cortical circuits13,14,15,16,17,18,19,20,21,22,23,24. Here we determine the dynamics of synaptic receptive field plasticity in the adult primary auditory cortex (also known as AI) using in vivo whole-cell recording. Pairing sensory stimulation with nucleus basalis activation shifted the preferred stimuli of cortical neurons by inducing a rapid reduction of synaptic inhibition within seconds, which was followed by a large increase in excitation, both specific to the paired stimulus. Although nucleus basalis was stimulated only for a few minutes, reorganization of synaptic tuning curves progressed for hours thereafter: inhibition slowly increased in an activity-dependent manner to rebalance the persistent enhancement of excitation, leading to a retuned receptive field with new preference for the paired stimulus. This restricted period of disinhibition may be a fundamental mechanism for receptive field plasticity, and could serve as a memory trace9,25 for stimuli or episodes that have acquired new behavioural significance.
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We thank K. L. Arendt, T. Babcock, Y. Dan, E. de Villers-Sidani, M. R. DeWeese, M. P. Kilgard, D. Polley, L. Wilbrecht and J. A. Winer for comments and discussions, and S. Bao, W. Huang, K. Imaizumi, A. Tan and C.-L. Teng for technical assistance. D. Bliss created the artwork in Figs 1a and 3a. This work was supported by the NIDCD, the Conte Center for Neuroscience Research at UCSF, Hearing Research Inc., and the John C. and Edward Coleman Fund. R.C.F. is a recipient of the Jane Coffin Childs Postdoctoral Research Fellowship and the Sandler Translational Research Fellowship.
The file contains Supplementary Figures S1-S6 and their Legends.
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Noninvasive neurostimulation of left temporal lobe disrupts rapid talker adaptation in speech processing
Brain and Language (2019)