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The Journal of Neuroscience, December 3, 2008, 28(49):13094-13105; doi:10.1523/JNEUROSCI.3074-08.2008

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Development/Plasticity/Repair
Activity-Dependent Dynamic Microtubule Invasion of Dendritic Spines

Xindao Hu,¹ Chris Viesselmann,² Sookin Nam,² Elliott Merriam,¹ and Erik W. Dent^1,2

¹Neuroscience Training Program and ²Department of Anatomy, University of Wisconsin–Madison, Madison, Wisconsin 53706

Correspondence should be addressed to Erik W. Dent, Department of Anatomy, University of Wisconsin–Madison, 1300 University Avenue, 332 SMI, Madison, WI 53706. Email: ewdent{at}wisc.edu

Dendritic spines are the primary sites of contact with presynaptic axons on excitatory hippocampal and cortical neurons. During development and plasticity spines undergo marked changes in structure that directly affect the functional communication between neurons. Elucidating the cytoskeletal events that induce these structural changes is fundamental to understanding synaptic biology. Actin plays a central role in the spine cytoskeleton, however the role of microtubules in spine function has been studied little. Although microtubules have a prominent role in transporting material throughout the dendrite that is destined for spines, they are not thought to directly influence spine structure or function. Using total internal reflectance fluorescent microscopy we discovered that microtubules rapidly invade dendritic protrusions of mature CNS neurons (up to 63 d in vitro), occasionally being associated with marked changes in spine morphology in the form of transient spine head protrusions (tSHPs). Two microtubules can occupy a spine simultaneously and microtubule targeting can occur from both the proximal and distal dendrite. A small percentage of spines are targeted at a time and all targeting events are transient, averaging only a few minutes. Nevertheless, over time many spines on a dendrite are targeted by microtubules. Importantly, we show that increasing neuronal activity enhances both the number of spines invaded by microtubules and the duration of these invasions. This study provides new insight into the dynamics of the neuronal cytoskeleton in mature CNS neurons and suggests that microtubules play an important, direct role in spine morphology and function.

Key words: cytoskeleton; activity; hippocampus; cortex; synapse; plasticity

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Received June 3, 2008; revised Oct. 14, 2008; accepted Oct. 16, 2008.

Correspondence should be addressed to Erik W. Dent, Department of Anatomy, University of Wisconsin–Madison, 1300 University Avenue, 332 SMI, Madison, WI 53706. Email: ewdent{at}wisc.edu

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