Do changes in neuronal structure underlie cortical plasticity1,2? Here we used time-lapse two-photon microscopy3,4 of pyramidal neurons in layer 2/3 of developing rat barrel cortex5 to image the structural dynamics of dendritic spines and filopodia. We found that these protrusions were highly motile: spines and filopodia appeared, disappeared or changed shape over tens of minutes. To test whether sensory experience drives this motility we trimmed whiskers one to three days before imaging. Sensory deprivation markedly (∼40%) reduced protrusive motility in deprived regions of the barrel cortex during a critical period around postnatal days (P)11–13, but had no effect in younger (P8–10) or older (P14–16) animals. Unexpectedly, whisker trimming did not change the density, length or shape of spines and filopodia. However, sensory deprivation during the critical period degraded the tuning of layer 2/3 receptive fields. Thus sensory experience drives structural plasticity in dendrites, which may underlie the reorganization of neural circuits.
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Bailey,C. H. & Kandel,E. R. Structural changes accompanying memory formation. Annu. Rev. Physiol. 55, 397–426 (1993).
Buonomano,D. V. & Merzenich,M. M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 21, 149–186 (1998).
Denk,W., Strickler,J. H. & Webb, W. W. Two-photon laser scanning microscopy. Science 248, 73–76 ( 1990).
Denk,W. & Svoboda,K. Photon upmanship: why multiphoton imaging is more than a gimmick. Neuron 18, 351–357 (1997).
Woolsey,T. A. & van der Loos,H. The structural organization of layer IV in the somatosensory region (S1) of mouse cerebral cortex. Brain Res. 17, 205–242 ( 1970).
Harris,K. M. & Kater,S. B. Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu. Rev. Neurosci. 17, 341–371 (1994).
Purpura,D. in Advances in Neurology (ed. Kreutzberg, G. W.) 91– 116 (Raven, New York, 1975).
Fiala,J. C., Feinberg,M., Popov,V. & Harris,K. M. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J. Neurosci. 18, 8900–8911 (1998).
Micheva,K. D. & Beaulieu,C. Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry. J. Comp. Neurol. 373, 340–354 (1996).
Miller,M. & Peters,A. Maturation of rat visual cortex. II. A combined Golgi-electron microscope study of pyramidal neurons. J. Comp. Neurol. 203, 555–573 (1981).
Dailey,M. E. & Smith,S. J. The dynamics of dendritic structure in developing hippocampal slices. J. Neurosci. 16, 2983–2994 (1996).
Maletic-Savatic,M., Malinow,R. & Svoboda, K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923–1927 (1999).
Ziv,N. E. & Smith,S. J. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17, 91–102 (1996).
Horch,H. W., Kruttgen,A., Portbury,S. D. & Katz,L. C. Destabilization of cortical dendrites and spines by BDNF. Neuron 23, 353–364 ( 1999).
Engert,F. & Bonhoeffer,T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66–70 (1999).
Toni,N., Buchs,P. A., Nikonenko,I., Bron,C. R. & Muller,D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402, 421–425 ( 1999).
Diamond,M. E., Huang,W. & Ebner,F. F. Laminar comparison of somatosensory cortical plasticity. Science 265, 1885–1888 (1994).
Fox,K., Glazewski,S., Chen,C. M., Silva,A. & Li,X. Mechanisms underlying experience-dependent potentiation and depression of vibrissae responses in barrel cortex. J. Physiol. (Paris) 90, 263–269 (1996).
Malinow,R. in Imaging Living Cells (eds Yuste, R., Lanni, F. & Konnerth, A.) 58.1–58.8 (Cold Spring Harbor Press, Cold Spring Harbor, 1999).
Svoboda,K., Denk,W., Kleinfeld,D. & Tank,D. W. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385, 161–165 ( 1997).
Chapin,J. K. & Lin,C. S. in The Cerebral Cortex of the Rat (eds Kolb, B. & Tees, R. C.) 341–380 (MIT Press, Cambridge, Massachusetts, 1990).
Welker,W. I. Analysis of sniffing of the albino rat. Behavior 22 , 223–244 (1964).
Moore,C. I. & Nelson,S. B. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J. Neurophysiol. 80, 2882– 2892 (1998).
Zhu,J. J. & Connors,B. W. Intrinsic firing patterns and whisker-evoked synaptic responses of neurons in the rat barrel cortex. J. Neurophysiol. 81, 1171–1183 (1999).
Fischer,M., Kaech,S., Knutti,D. & Matus,A. Rapid actin-based plasticity in dendritic spines. Neuron 20, 847–854 (1998).
Winfield,D. A. The postnatal development of synapses in the visual cortex of the cat and the effects of eyelid closure. Brain Res. 206, 166–171 (1981).
Vees,A. M., Micheva,K. D., Beaulieu,C. & Descarries,L. Increased number and size of dendritic spines in ipsilateral barrel field cortex following unilateral whisker trimming in postnatal rat. J. Comp. Neurol. 400, 110–124 (1998).
Movshon,J. A. & Dursteler,M. R. Effects of brief periods of unilateral eye closure on the kitten's visual system. J. Neurophysiol. 40, 1255–1265 ( 1977).
Simons,D. J. & Land,P. W. Early experience of tactile stimulation influences organization of somatic sensory cortex. Nature 326, 694–697 (1987).
Schlaggar,B. L., Fox,K. & O'Leary,D. D. M. Postsynaptic control of plasticity in developing somatosensory cortex. Nature 364, 623– 626 (1993).
We thank B. Burbach and E. Nimchinsky for help with experiments, K. Greenwood for help with analysis, Z. Mainen, M. Maravall, E. Ruthazer and B. Sabatini for comments on the manuscript, and the Malinow laboratory for help with viruses. This work was supported by IBRO (BL), HFSP, the Mathers and Pew Foundations (K.S.) and an NIH training grant to SHNY Stony Brook (B.C.).
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Lendvai, B., Stern, E., Chen, B. et al. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404, 876–881 (2000). https://doi.org/10.1038/35009107
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