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Science 3 May 1996:
Vol. 272. no. 5262, pp. 716 - 719
DOI: 10.1126/science.272.5262.716
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Reports

Direct Measurement of Coupling Between Dendritic Spines and Shafts

Karel Svoboda, David W. Tank, Winfried Denk *

Characterization of the diffusional and electrotonic coupling of spines to the dendritic shaft is crucial to understanding neuronal integration and synaptic plasticity. Two-photon photobleaching and photorelease of fluorescein dextran were used to generate concentration gradients between spines and shafts in rat CA1 pyramidal neurons. Diffusional reequilibration was monitored with two-photon fluorescence imaging. The time course of reequilibration was exponential, with time constants in the range of 20 to 100 milliseconds, demonstrating chemical compartmentalization on such time scales. These values imply that electrical spine neck resistances are unlikely to exceed 150 megohms and more likely range from 4 to 50 megohms.

Biological Computation Research Department, Bell Laboratories, Lucent Technologies, 600 Mountain Avenue, Murray Hill, NJ 07974, USA.
* To whom correspondence should be addressed. E-mail: denk{at}bell-labs.com.


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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