Spine motility: a means towards an end?

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Abstract

From the first glimpse of moving spines half a decade ago, the prevailing view has been that spine contortions and wiggling, especially during development, maximize encounters with presynaptic growth cones or synaptic boutons. Other new evidence has revealed that spines continue to be motile even after they settle on a presynaptic partner and form a synapse. We present the evidence for each view, and discuss how spines with synapses could move relative to their apparently stable presynaptic partners. Thus, spine motility might not simply be a means towards an end of synapse formation, but could continue, albeit at a lower rate, during synapse turnover after development ends.

Section snippets

Is all spine motility the same?

Although the idea was presented two decades ago that dendritic spines are dynamic structures 23, 24, it was not until the pioneering studies of Smith and colleagues that the first glimpses of the dynamic nature of dendritic filopodia were appreciated [4]. Using confocal time-lapse microscopy, Steve Smith's group demonstrated that dendritic filopodia of young hippocampal neurons growing in slice cultures were highly motile and transient [4]. Much of the motility they observed consisted of rapid

Motility before synaptogenesis: reaching out and touching someone

Because motile filopodia are more numerous during synaptogenesis, a theory has been proposed that these structures might mediate cell-cell contact prior to synaptogenesis 4, 21, 25. A synaptogenic role for filopodial motility was first tested with a combination of dynamic imaging approaches, by correlating filopodial motility with the incidence of synaptic vesicle recycling, and therefore a functional synapse, with the dye FM4–64 (a fluorescent endocytosis label [25]). As the number of

Spine motility after synaptic contact

The studies already discussed indicate that although presynaptic terminals seem to regulate the stability or maintenance of spines, synaptic contacts do not appear to limit spine motility. This suggests that spine motility does not function merely as ‘the means towards an end’ (the end being synaptogenesis), but that spine motility plays a role in events after synapse formation. That spines with synapses can move was first suggested by Matus and colleagues, who observed persistent spine

Concluding remarks

Evidence exists for heightened spine motility during synaptogenesis, supporting previous hypotheses that spine motility serves behaviorally to maximize encounters with presynaptic elements, which was considered previously to be the endpoint of this process. One crucial issue is whether spine motility is required for synaptogenesis. To address this, ideally motility should be arrested for a long enough period to determine the consequences for synaptogenesis. Studies by Svoboda and colleagues [30]

Acknowledgements

We gratefully acknowledge Rafael Yuste, Peter Scheiffele and Phil Buttery for useful discussion, and Phil Buttery for help with the illustrations. Supported by NIH grant NS16951.

References (47)

  • E.G. Gray

    Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscopic study

    J. Anat.

    (1959)
  • R. Yuste et al.

    Dendritic spines as basic functional units of neuronal integration

    Nature

    (1995)
  • M.E. Dailey et al.

    The dynamics of dendritic structure in developing hippocampal slices

    J. Neurosci.

    (1996)
  • A. Dunaevsky

    Developmental regulation of spine motility in the mammalian central nervous system

    Proc. Natl. Acad. Sci. U. S. A.

    (1999)
  • F. Engert et al.

    Dendritic spine changes associated with hippocampal long-term synaptic plasticity

    Nature

    (1999)
  • M. Maletic-Savatic

    Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity

    Science

    (1999)
  • W.T. Wong

    Rapid dendritic remodeling in the developing retina: dependence on neurotransmission and reciprocal regulation by Rac and Rho

    J. Neurosci.

    (2000)
  • C. Blackstone et al.

    Postsynaptic calcium signaling microdomains in neurons

    Front. Biosci.

    (2002)
  • R. Yuste

    From form to function: calcium compartmentalization in dendritic spines

    Nat. Neurosci.

    (2000)
  • J.T. Trachtenberg

    Long-term in vivo imaging of experience-dependent synaptic plasticity in the adult cortex

    Nature

    (2002)
  • J. Grutzendler

    Long-term dendritic spine stability in the adult cortex

    Nature

    (2002)
  • H. Hering et al.

    Dendritic spines: structure, dynamics and regulation

    Nat. Neurosci.

    (2001)
  • R. Yuste et al.

    Morphological changes in dendritic spines associated with long-term synaptic plasticity

    Annu. Rev. Neurosci.

    (2001)

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