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Published December 2016 | Accepted Version + Supplemental Material
Journal Article Open

Unstable neurons underlie a stable learned behavior

Abstract

Motor skills can be maintained for decades, but the biological basis of this memory persistence remains largely unknown. The zebra finch, for example, sings a highly stereotyped song that is stable for years, but it is not known whether the precise neural patterns underlying song are stable or shift from day to day. Here we demonstrate that the population of projection neurons coding for song in the premotor nucleus, HVC, change from day to day. The most dramatic shifts occur over intervals of sleep. In contrast to the transient participation of excitatory neurons, ensemble measurements dominated by inhibition persist unchanged even after damage to downstream motor nerves. These observations offer a principle of motor stability: spatiotemporal patterns of inhibition can maintain a stable scaffold for motor dynamics while the population of principal neurons that directly drive behavior shift from one day to the next.

Additional Information

© 2016 Macmillan Publishers Limited. Received 29 January 2016. Accepted 07 September 2016. Published online 10 October 2016. Corrected online 13 October 2016. The authors thank H. Eichenbaum and the Center for Neuroscience at BU for the loan of the Inscopix microscope. Special thanks to D.S. Kim and L. Looger for providing the GCaMP6 DNA and to the GENIE project at Janelia Farm Research Campus, Howard Hughes Medical Institute. This work was supported by a grant from CELEST, an NSF Science of Learning Center (SBE-0354378) and by grants from NINDS (R01-NS089679-01 and 1U01NS090454-01). Data Availability: The data that support the findings of this study are available from the corresponding author upon reasonable request. The latest version of the custom Matlab scripts used for analysis in this manuscript are available at https://github.com/gardner-lab/HVC-Stability-Analysis. These authors contributed equally to this work. William A Liberti III & Jeffrey E Markowitz Author Contributions: W.A.L., J.E.M., G.G. and D.P.L. performed the experiment; J.E.M. and W.A.L. analyzed the data; L.N.P. provided software for the custom microscope; D.C.L., D.N.K., T.V. and C.L. provided the lentivirus; T.V. and C.L. discovered the cell-type-specificity of the viral vector. W.A.L., J.E.M. and T.J.G. designed the experiment and wrote the manuscript. The authors declare no competing financial interests.

Attached Files

Accepted Version - nihms815429.pdf

Supplemental Material - nn.4405-S1.pdf

Supplemental Material - nn.4405-S2.pdf

Supplemental Material - nn.4405-SF1.jpg

Supplemental Material - nn.4405-SF2.jpg

Supplemental Material - nn.4405-SF3.jpg

Supplemental Material - nn.4405-SF4.jpg

Supplemental Material - nn.4405-SF5.jpg

Supplemental Material - nn.4405-SF6.jpg

Supplemental Material - nn.4405-SF7.jpg

Supplemental Material - nn.4405-SF8.jpg

Supplemental Material - nn.4405-SF9.jpg

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