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Long-term modification of cortical synapses improves sensory perception

Abstract

Synapses and receptive fields of the cerebral cortex are plastic. However, changes to specific inputs must be coordinated within neural networks to ensure that excitability and feature selectivity are appropriately configured for perception of the sensory environment. We induced long-lasting enhancements and decrements to excitatory synaptic strength in rat primary auditory cortex by pairing acoustic stimuli with activation of the nucleus basalis neuromodulatory system. Here we report that these synaptic modifications were approximately balanced across individual receptive fields, conserving mean excitation while reducing overall response variability. Decreased response variability should increase detection and recognition of near-threshold or previously imperceptible stimuli. We confirmed both of these hypotheses in behaving animals. Thus, modification of cortical inputs leads to wide-scale synaptic changes, which are related to improved sensory perception and enhanced behavioral performance.

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Figure 1: Example of A1 synaptic receptive field modification induced by nucleus basalis pairing.
Figure 2: Conservation of total excitation after pairing.
Figure 3: Best stimuli depression depends on recent sensory experience.
Figure 4: Pairing decreases synaptic variance to enhance detection and recognition of sensory stimuli.
Figure 5: Nucleus basalis pairing modifies spiking receptive fields.
Figure 6: Nucleus basalis pairing improves auditory detection.
Figure 7: Nucleus basalis pairing improves recognition.
Figure 8: Pairing under anesthesia improves perception.

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Acknowledgements

We thank L.F. Abbott, T. Babcock, M. Berry, E. Chang, Z. Chen, E. de Villers-Sidani, A.L. Dorrn, P. Dutta, A. Fairhall, S.P. Gandhi, G. Glassner, C.A. Hoeffer, K. Imaizumi, B.J. Jones, N. Kopell, R. Liu, G. Myers, P. O'Hara, J. Shih, A.Y. Tan, C.-L. Teng and L. Wilbrecht for comments, discussions and technical assistance. J. Pivkova created the artwork in Figure 1a. This work was supported by the US National Institute on Deafness and Other Communication Disorders (grant DC009635 to R.C.F., grant DC009836 to D.B.P. and grant DC02260 to C.E.S.), US National Science Foundation (grants 0615308 and 0627126 to P.A.L.), Intel Research (P.A.L.), DoCoMo Capital and Foundation Capital (P.A.L.), the Conte Center for Neuroscience Research at the University of California, San Francisco (grant MH077970 to M.M.M. and C.E.S.), Hearing Research Inc. (C.E.S.), the John C. and Edward Coleman Fund (M.M.M. and C.E.S.) and the US National Academies Keck Future Initiatives (R.C.F. and P.A.L.). A.J.B. is supported by a US National Science Foundation Predoctoral Fellowship. M.W. is supported by a Sequoia Capital Stanford Graduate Fellowship. I.C. is supported by an US National Institute of Mental Health training grant. P.A.L. is supported by a Microsoft Research New Faculty Fellowship. R.C.F. is supported by a Sloan Research Fellowship.

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R.C.F., I.C., D.B.P., M.M.M. and C.E.S. designed the experiments. R.C.F., I.C. and A.R.O.M. performed the electrophysiological experiments. R.C.F., I.C., A.J.B., K.Y., B.A.S., N.Z. and H.B. performed the behavioral experiments. M.W. and P.A.L. designed and built the wireless device. R.C.F. wrote the manuscript. All authors discussed the manuscript.

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Correspondence to Robert C Froemke.

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Froemke, R., Carcea, I., Barker, A. et al. Long-term modification of cortical synapses improves sensory perception. Nat Neurosci 16, 79–88 (2013). https://doi.org/10.1038/nn.3274

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