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. 2003 Dec 23;100(26):16024-9.
doi: 10.1073/pnas.2636949100. Epub 2003 Dec 8.

Motility of dendritic spines in visual cortex in vivo: changes during the critical period and effects of visual deprivation

Ania Majewska  1 , Mriganka Sur
Affiliations

Motility of dendritic spines in visual cortex in vivo: changes during the critical period and effects of visual deprivation

Ania Majewska et al. Proc Natl Acad Sci U S A. .

Erratum in

  • Proc Natl Acad Sci U S A. 2004 Mar 16;101(11):3991

Abstract

Cortical dendritic spines are highly motile postsynaptic structures onto which most excitatory synapses are formed. It has been postulated that spine dynamics might reflect synaptic plasticity of cortical neurons. To test this hypothesis, we have investigated spine dynamics during the critical period in mouse visual cortex in vivo with and without sensory deprivation. The motility of spines on apical dendrites of layer 5 neurons was assayed by time-lapse two-photon microscopy. Spines were motile at the ages examined, postnatal days (P)21-P42, although motility decreased between P21 and P28 and then remained stable through P42. Binocular deprivation from before the time of eye-opening up-regulated spine motility during the peak of the critical period (P28), without affecting average spine length, class distribution, or density. Deprivation at the start of the critical period had no effect on spine motility, whereas continued deprivation through the end of the critical period appeared to reduce spine motility slightly. We conclude that spine motility might be involved in critical-period plasticity and that reduction of activity during the critical period enhances spine dynamics.

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Figures

Fig. 1.
Fig. 1.
Imaging dendrites of layer 5 pyramidal neurons in the visual cortex in vivo.(A) Two-photon images of the apical tuft of a layer 5 pyramidal neuron from a P21 mouse. (Aa) A collapsed z stack showing the dendritic arbor. (Ab) Three-dimensional reconstruction showing the dendritic arbor from the side. (Scale bar, 50 μm.) (B) Examining the location of imaged neurons in histological sections. (Ba). Nissl stain of coronal section of cortex. Notice the thickening of layer 4 characteristic of primary visual cortex. (Scale bar, 1 mm.) (Bb) A higher-power image of the boxed area in Ba. (Bc) Fluorescence image of the area in Bb showing position of imaged GFP neuron. (Scale bar, 500 μm.) (Bd) Higher magnification of imaged neuron. (Scale bar, 50 μm.)
Fig. 2.
Fig. 2.
Spine motility during and beyond the critical period in mouse visual cortex in vivo.(A) Dendritic spines were motile over the time periods studied. Spines exhibited different kinds of motility such as (from top to bottom): retraction, elongation, spine head displacement and shape change, and growth of filopodia from the spine head. (Scale bar, 1 μm.) Movie 1 shows motile spines. (B) Motility of dendritic protrusions correlates with protrusion length or average length over the time course imaged (linear regression analysis; P < 0.001, n = 235 protrusions, P21–P42). (C) Time courses showing examples of changes in length of protrusions observed at P21. At any length, both stable and motile protrusions could be found.
Fig. 3.
Fig. 3.
Regulation of spine motility during the critical period in vivo. (A) Spine motility significantly declines during the critical period and remains at a basal level into early adulthood. *, P < 0.001. (B) The structure of dendritic spines in visual cortex does not change during the critical period. Mushroom spines were the most common type of protrusion at all ages studied. Filopodia were uncommon at these ages and were absent at P42. (Right) Examples of protrusions and classification; clockwise from top left, mushroom, thin, filopodia, and stubby. (Scale bars, 1 μm.) (C) The motility of all classes of spines is down-regulated during the critical period. (D) Distribution of motilities at the three ages studied. Mushroom spines were most common and comprised the least and most motile protrusions.
Fig. 4.
Fig. 4.
The effect of binocular deprivation on spine motility in vivo. (A) Binocular deprivation from P14 significantly increases spine motility at P28 by ≈60%. *, P < 0.001. There is no change in motility with deprivation at P21 and a slight reduction in motility in deprived mice at P42. (B) Deprivation does not alter the structure of protrusions in visual cortex at any age. (C) The increase in overall motility caused by deprivation at P28 is evident in all types of protrusions (Left). At P42, however, the deprivation-induced reduction in spine motility is mediated by a stabilization of stubby spines. m, mushroom; t, thin; s, stubby; f, filopodia.
Fig. 5.
Fig. 5.
Spine turnover during the critical period. (A)(Upper) An example of spine outgrowth from the dendrite during the imaging period. (Scale bar, 0.5 μm.) (Lower) An example of spine retraction into the dendrite during the imaging interval. (Scale bar, 1 μm.) Images are collapsed z stacks. (B) The abscissa plots the percent of total protrusions that were added or removed during the observation period of 2 h. Low rates of spine turnover were observed at all ages. Turnover rates were highest in young mice and were not visibly affected by binocular deprivation.
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