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Experience leaves a lasting structural trace in cortical circuits

Abstract

Sensory experiences exert a powerful influence on the function and future performance of neuronal circuits in the mammalian neocortex1,2,3. Restructuring of synaptic connections is believed to be one mechanism by which cortical circuits store information about the sensory world4,5. Excitatory synaptic structures, such as dendritic spines, are dynamic entities6,7,8 that remain sensitive to alteration of sensory input throughout life6,9. It remains unclear, however, whether structural changes at the level of dendritic spines can outlast the original experience and thereby provide a morphological basis for long-term information storage. Here we follow spine dynamics on apical dendrites of pyramidal neurons in functionally defined regions of adult mouse visual cortex during plasticity of eye-specific responses induced by repeated closure of one eye (monocular deprivation). The first monocular deprivation episode doubled the rate of spine formation, thereby increasing spine density. This effect was specific to layer-5 cells located in binocular cortex, where most neurons increase their responsiveness to the non-deprived eye3,10. Restoring binocular vision returned spine dynamics to baseline levels, but absolute spine density remained elevated and many monocular deprivation-induced spines persisted during this period of functional recovery. However, spine addition did not increase again when the same eye was closed for a second time. This absence of structural plasticity stands out against the robust changes of eye-specific responses that occur even faster after repeated deprivation3. Thus, spines added during the first monocular deprivation experience may provide a structural basis for subsequent functional shifts. These results provide a strong link between functional plasticity and specific synaptic rearrangements, revealing a mechanism of how prior experiences could be stored in cortical circuits.

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Figure 1: Monocular deprivation in adult mice increases the rate of spine gain in L5 neurons in binocular cortex.
Figure 2: Monocular deprivation in adult mice does not alter spine dynamics in L2/3 neurons.
Figure 3: MD-induced increase in spine density on L5 neurons outlasts the altered experience.
Figure 4: A second MD increases the size of spines gained during the first MD, without additional spine gain.

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Acknowledgements

We thank T. Keck for contributing control data for Supplementary Fig. 7a, and M. Sperling and B. Pichler for programming help. This work was supported by the Max Planck Society, the Wellcome Trust and the Humboldt Foundation.

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Correspondence to Mark Hübener.

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Hofer, S., Mrsic-Flogel, T., Bonhoeffer, T. et al. Experience leaves a lasting structural trace in cortical circuits. Nature 457, 313–317 (2009). https://doi.org/10.1038/nature07487

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