Structural dynamics of synapses in living animals

Current Opinion in Neurobiology

Volumn 14, Issue 1, 2004, Pages 105-111

  Kasthuri, Narayanan ^a   Lichtman, Jeff W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

2P; General term for the group of fluorescent proteins; GFP; Green fluorescent protein; Neuromuscular junction; NMJ; Two photon; XFP; Yellow fluorescent protein; YFP

Indexed keywords

BRAIN RADIOGRAPHY; IMAGING SYSTEM; IN VIVO STUDY; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; NEUROANATOMY; NEUROBIOLOGY; NONHUMAN; OPTICS; PRIORITY JOURNAL; REVIEW; SYNAPSE;

EID: 1342264160     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2004.01.013     Document Type: Review

References (56)

1. Kim J.H., Udo H., Li H.L., Youn T.Y., Chen M., Kandel E.R., Bailey C.H. Presynaptic activation of silent synapses and growth of new synapses contribute to intermediate and long-term facilitation in Aplysia. Neuron. 40:2003;151-165.
2. Lichtman J.W., Colman H. Synapse elimination and indelible memory. Neuron. 25:2000;269-278.
3. Purves D., Hadley R.D. Changes in the dendritic branching of adult mammalian neurones revealed by repeated imaging in situ. Nature. 315:1985;404-406.
4. Purves D., Hadley R.D., Voyvodic J.T. Dynamic changes in the dendritic geometry of individual neurons visualized over periods of up to three months in the superior cervical ganglion of living mice. J Neurosci. 6:1986;1051-1060.
5. Yoshikami D., Okun L.M. Staining of living presynaptic nerve terminals with selective fluorescent dyes. Nature. 310:1984;53-56.
6. Magrassi L., Purves D., Lichtman J.W. Fluorescent probes that stain living nerve terminals. J Neurosci. 7:1987;1207-1214.
7. Lichtman J.W., Magrassi L., Purves D. Visualization of neuromuscular junctions over periods of several months in living mice. J Neurosci. 7:1987;1215-1222.
8. Purves D., Lichtman J.W. Synaptic sites on reinnervated nerve cells visualized at two different times in living mice. J Neurosci. 7:1987;1492-1497.
9. Purves D., Voyvodic J.T., Magrassi L., Yawo H. Nerve terminal remodeling visualized in living mice by repeated examination of the same neuron. Science. 238:1987;1122-1126.
10. Harris L.W., Purves D. Rapid remodeling of sensory endings in the corneas of living mice. J Neurosci. 9:1989;2210-2214.
11. Balice-Gordon R.J., Lichtman J.W. In vivo visualization of the growth of pre- and postsynaptic elements of neuromuscular junctions in the mouse. J Neurosci. 10:1990;894-908.
12. Balice-Gordon R.J., Lichtman J.W. In vivo observations of pre- and postsynaptic changes during the transition from multiple to single innervation at developing neuromuscular junctions. J Neurosci. 13:1993;834-855.
13. Balice-Gordon R.J., Lichtman J.W. Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature. 372:1994;519-524.
14. Akaaboune M., Culican S.M., Turney S.G., Lichtman J.W. Rapid and reversible effects of activity on acetylcholine receptor density at the neuromuscular junction in vivo. Science. 286:1999;503-507.
15. Barker D., Ip M.C. Sprouting and degeneration of mammalian motor axons in normal and de-afferentated skeletal muscle. Proc R Soc Lond B Biol Sci. 163:1966;538-554.
16. Wernig A., Herrera A.A. Sprouting and remodelling at the nerve-muscle junction. Prog Neurobiol. 27:1986;251-291.
17. Wigston D.J. Remodeling of neuromuscular junctions in adult mouse soleus. J Neurosci. 9:1989;639-647.
18. Herrera A.A., Banner L.R., Nagaya N. Repeated, in vivo observation of frog neuromuscular junctions: remodelling involves concurrent growth and retraction. J Neurocytol. 19:1990;85-99.
19. Hill R.R., Robbins N., Fang Z.P. Plasticity of presynaptic and postsynaptic elements of neuromuscular junctions repeatedly observed in living adult mice. J Neurocytol. 20:1991;165-182.
20. Hill R.R., Robbins N. Mode of enlargement of young mouse neuromuscular junctions observed repeatedly in vivo with visualization of pre- and postsynaptic borders. J Neurocytol. 20:1991;183-194.
21. Langenfeld-Oster B., Dorlochter M., Wernig A. Regular and photodamage-enhanced remodelling in vitally stained frog and mouse neuromuscular junctions. J Neurocytol. 22:1993;517-530.
22. Wigston D.J. Repeated in vivo visualization of neuromuscular junctions in adult mouse lateral gastrocnemius. J Neurosci. 10:1990;1753-1761.
23. Rich M., Lichtman J.W. Motor nerve terminal loss from degenerating muscle fibers. Neuron. 3:1989;677-688.
24. van Mier P., Lichtman J.W. Regenerating muscle fibers induce directional sprouting from nearby nerve terminals: studies in living mice. J Neurosci. 14:1994;5672-5686.
25. Rich M.M., Lichtman J.W. In vivo visualization of pre- and postsynaptic changes during synapse elimination in reinnervated mouse muscle. J Neurosci. 9:1989;1781-1805.
26. Astrow S.H., Pitaevski V., Herrera A.A. Precision of reinnervation and synaptic remodeling observed in neuromuscular junctions of living frogs. J Neurosci. 16:1996;5130-5140.
27. Tucker K.L. In vivo imaging of the mammalian nervous system using fluorescent proteins. Histochem Cell Biol. 115:2001;31-39.
28. Ormo M., Cubitt A.B., Kallio K., Gross L.A., Tsien R.Y., Remington S.J. Crystal structure of the Aequorea victoria green fluorescent protein. Science. 273:1996;1392-1395.
29. Llopis J., McCaffery J.M., Miyawaki A., Farquhar M.G., Tsien R.Y. Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. Proc Natl Acad Sci USA. 95:1998;6803-6808.
30. Heim R., Tsien R.Y. Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr Biol. 6:1996;178-182.
31. Feng G., Mellor R.H., Bernstein M., Keller-Peck C., Nguyen Q.T., Wallace M., Nerbonne J.M., Lichtman J.W., Sanes J.R. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron. 28:2000;41-51.
32. Okabe S., Miwa A., Okado H. Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J Neurosci. 21:2001;6105-6114.
33. Ebihara T., Kawabata I., Usui S., Sobue K., Okabe S. Synchronized formation and remodeling of postsynaptic densities: long-term visualization of hippocampal neurons expressing postsynaptic density proteins tagged with green fluorescent protein. J Neurosci. 23:2003;2170-2181.
34. Umeda T., Okabe S. Visualizing synapse formation and remodeling: recent advances in real-time imaging of CNS synapses. Neurosci Res. 40:2001;291-300.
35. Gensler S., Sander A., Korngreen A., Traina G., Giese G., Witzemann V. Assembly and clustering of acetylcholine receptors containing GFP-tagged epsilon or gamma subunits: selective targeting to the neuromuscular junction in vivo. Eur J Biochem. 268:2001;2209-2217.
36. Trachtenberg J.T., Chen B.E., Knott G.W., Feng G., Sanes J.R., Welker E., Svoboda K. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature. 420:2002;788-794 In this paper, 2P microscopy was used to image, through a craniotomy, GFP expression in dendrites and spines of layer 5 neurons in barrel cortex of transgenic mice. The number of new spines that were added or eliminated was measured in superficial cortex over intervals of days to several weeks. The number of spines changed considerably over time: 20% disappeared in one day and 50%, in one month. A method to photo-convert GFP using antibodies for correlated light, and electron microscopy was also used.
37. Denk W., Strickler J.H., Webb W.W. Two-photon laser scanning fluorescence microscopy. Science. 248:1990;73-76.
38. Theer P., Hasan M.T., Denk W. Two-photon imaging to a depth of 1000 microm in living brains by use of a Ti:Al2O3 regenerative amplifier. Opt Lett. 28:2003;1022-1024 The authors describe an adaptation for 2P microscopy that allows imaging to greater depths (approaching 1 mm). The use of a regenerative amplifier increases the power in individual 2P pulses, while decreasing the frequency of pulses, thus, leaving the total power relatively constant.
39. Jung J.C., Schnitzer M.J. Multiphoton endoscopy. Opt Lett. 28:2003;902-904.
40. Helmchen F., Fee M.S., Tank D.W., Denk W. A miniature head-mounted two-photon microscope. high-resolution brain imaging in freely moving animals. Neuron. 31:2001;903-912.
41. Knobel K.M., Davis W.S., Jorgensen E.M., Bastiani M.J. UNC-119 suppresses axon branching in C. elegans. Development. 128:2001;4079-4092.
42. Zito K., Parnas D., Fetter R.D., Isacoff E.Y., Goodman C.S. Watching a synapse grow: noninvasive confocal imaging of synaptic growth in Drosophila. Neuron. 22:1999;719-729.
43. Clyne P.J., Brotman J.S., Sweeney S.T., Davis G. Green fluorescent protein tagging Drosophila proteins at their native genomic Loci with small p elements. Genetics. 165:2003;1433-1441.
44. Jontes J.D., Buchanan J., Smith S.J. Growth cone and dendrite dynamics in zebrafish embryos: early events in synaptogenesis imaged in vivo. Nat Neurosci. 3:2000;231-237.
45. Walsh M.K., Lichtman J.W. In vivo time-lapse imaging of synaptic takeover associated with naturally occurring synapse elimination. Neuron. 37:2003;67-73 Innervation to developing muscle fibers was monitored as fibers underwent the transition from multiple to single innervation. The two motor axons to a single muscle fiber were labeled with two distinct fluorophores (cyan fluorescent protein and YFP) and the post-synaptic receptors were labeled a third color (with red fluorescent α-bugarotoxin). Winning inputs gradually occupied the synaptic territory of losing inputs but the process did not always occur in a monotonic fashion.
46. Witte S., Stier H., Cline H.T. In vivo observations of timecourse and distribution of morphological dynamics in Xenopus retinotectal axon arbors. J Neurobiol. 31:1996;219-234.
47. Alsina B., Vu T., Cohen-Cory S. Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF. Nat Neurosci. 4:2001;1093-1101.
48. Ruthazer E.S., Akerman C.J., Cline H.T. Control of axon branch dynamics by correlated activity in vivo. Science. 301:2003;66-70 Additions and eliminations of retinal ganglion cell axon branches were imaged in tadpole tectum. Competition between axons from the two eyes was experimentally induced. By differentially labeling the territory occupied by the two eyes after fixation, branch addition was shown to be equally likely to occur in all territories but that branch elimination occurred preferentially in the territory where the two eyes overlapped.
49. Baker M.W., Kauffman B., Macagno E.R., Zipser B. In vivo dynamics of CNS sensory arbor formation: a time-lapse study in the embryonic leech. J Neurobiol. 56:2003;41-53 Single sensory axons, projecting into the CNS in developing leech, were labeled by iontophoretic injection of fluorescently tagged dextran and then followed over the course of several hours. The time-lapse images show the transformation of an immature axonal arbor into a mature one. Some of the images also suggest sites where synapses are being established.
50. Gan W.B., Kwon E., Feng G., Sanes J.R., Lichtman J.W. Synaptic dynamism measured over minutes to months: age-dependent decline in an autonomic ganglion. Nat Neurosci. 6:2003;956-960 Confocal microscopy in transgenic mice that express YFP in pre-synaptic axons innervating the submandibular ganglion was used to examine the stability of pre-synaptic contacts over extended periods of time (months to years). Younger animals demonstrate dynamism in their pre-synaptic contacts but older animals show less plasticity, in that the synaptic patterns can be recognized on the same post-synaptic neuron over the timeframe of a year.
51. Grutzendler J., Kasthuri N., Gan W.B. Long-term dendritic spine stability in the adult cortex. Nature. 420:2002;812-816 Two-photon microscopy was used to image, through a thinned-skull, the rate of spine addition and elimination in primary visual cortex in transgenic mice that express YFP in pyramidal neurons. Dendritic spines in superficial layers showed stability in the adult visual cortex (96% remain stable over a one-month period).
52. Meyer M.P., Niell C.M., Smith S.J. Brain imaging: how stable are synaptic connections? Curr Biol. 13:2003;R180-R182.
53. Mizrahi A., Katz L.C. Dendritic stability in the adult olfactory bulb. Nat Neurosci. 6:2003;1201-1207 Dendritic branches were imaged in the olfactory bulb of adult transgenic mice, expressing YFP in a subset of neurons. Despite ongoing neurogenesis of the innervation to these dendrites, little change was seen in the dendritic branching patterns.
54. Nguyen Q.T., Sanes J.R., Lichtman J.W. Pre-existing pathways promote precise projection patterns. Nat Neurosci. 5:2002;861-867.
55. Reddy L.V., Koirala S., Sugiura Y., Herrera A.A., Ko C.P. Glial cells maintain synaptic structure and function and promote development of the neuromuscular junction in vivo. Neuron. 40:2003;563-580.
56. Gan W.B., Grutzendler J., Wong W.T., Wong R.O., Lichtman J.W. Multicolor 'DiOlistic' labeling of the nervous system using lipophilic dye combinations. Neuron. 27:2000;219-225.