Spread of synaptic depression mediated by presynaptic cytoplasmic signaling

Science

Volumn 272, Issue 5264, 1996, Pages 998-1001

  Cash, Sydney ^a   Zucker, Robert S ^b   Poo, Mu Ming ^a,c  

^a Columbia University ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL INTERACTION; EXTRACELLULAR MATRIX; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; XENOPUS;

EID: 0029759681     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.272.5264.998     Document Type: Article

References (37)

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7. In the hippocampal CA1 region or dentate gyrus, heterosynaptic depression also accompanies induction of LTP [G. S. Lynch, T. Dunwiddie, V. Gribkoff, Nature 266, 737 (1977); W. C. Abraham and G. V. Goddard, ibid. 305, 717 (1983); J. E. Bradler and G. Barrionuevo, Neuroscience 35, 265 (1990); B. R. Christie and W. C. Abraham, Synapse 10, 1 (1992)], and LTD at one synapse may reverse LTP at another [D. Muller, S. Hefft, A. Figurov, Neuron 14, 599 (1995)]. Furthermore, LTP induced at one synapse in CA1 stratum oriens may be accompanied by potentiation in a second untetanized pathway [S. Otani, J. A. Connor, W. B. Levy, Learn. Memory 2, 101 (1995)]. Heterosynaptic effects may also occur in prefrontal neurons [J. C. Hirsch, G. Barrionuevo, F. Crepel, Synapse 12, 82 (1992)] and cerebellar Purkinje cells [P. Vincent and A. Marty, Neuron 11, 885 (1993); A. Marty and I. Llano, Curr. Opin. Neurobiol. 5, 335 (1995)].
8. In the hippocampal CA1 region or dentate gyrus, heterosynaptic depression also accompanies induction of LTP [G. S. Lynch, T. Dunwiddie, V. Gribkoff, Nature 266, 737 (1977); W. C. Abraham and G. V. Goddard, ibid. 305, 717 (1983); J. E. Bradler and G. Barrionuevo, Neuroscience 35, 265 (1990); B. R. Christie and W. C. Abraham, Synapse 10, 1 (1992)], and LTD at one synapse may reverse LTP at another [D. Muller, S. Hefft, A. Figurov, Neuron 14, 599 (1995)]. Furthermore, LTP induced at one synapse in CA1 stratum oriens may be accompanied by potentiation in a second untetanized pathway [S. Otani, J. A. Connor, W. B. Levy, Learn. Memory 2, 101 (1995)]. Heterosynaptic effects may also occur in prefrontal neurons [J. C. Hirsch, G. Barrionuevo, F. Crepel, Synapse 12, 82 (1992)] and cerebellar Purkinje cells [P. Vincent and A. Marty, Neuron 11, 885 (1993); A. Marty and I. Llano, Curr. Opin. Neurobiol. 5, 335 (1995)].
9. In the hippocampal CA1 region or dentate gyrus, heterosynaptic depression also accompanies induction of LTP [G. S. Lynch, T. Dunwiddie, V. Gribkoff, Nature 266, 737 (1977); W. C. Abraham and G. V. Goddard, ibid. 305, 717 (1983); J. E. Bradler and G. Barrionuevo, Neuroscience 35, 265 (1990); B. R. Christie and W. C. Abraham, Synapse 10, 1 (1992)], and LTD at one synapse may reverse LTP at another [D. Muller, S. Hefft, A. Figurov, Neuron 14, 599 (1995)]. Furthermore, LTP induced at one synapse in CA1 stratum oriens may be accompanied by potentiation in a second untetanized pathway [S. Otani, J. A. Connor, W. B. Levy, Learn. Memory 2, 101 (1995)]. Heterosynaptic effects may also occur in prefrontal neurons [J. C. Hirsch, G. Barrionuevo, F. Crepel, Synapse 12, 82 (1992)] and cerebellar Purkinje cells [P. Vincent and A. Marty, Neuron 11, 885 (1993); A. Marty and I. Llano, Curr. Opin. Neurobiol. 5, 335 (1995)].
10. In the hippocampal CA1 region or dentate gyrus, heterosynaptic depression also accompanies induction of LTP [G. S. Lynch, T. Dunwiddie, V. Gribkoff, Nature 266, 737 (1977); W. C. Abraham and G. V. Goddard, ibid. 305, 717 (1983); J. E. Bradler and G. Barrionuevo, Neuroscience 35, 265 (1990); B. R. Christie and W. C. Abraham, Synapse 10, 1 (1992)], and LTD at one synapse may reverse LTP at another [D. Muller, S. Hefft, A. Figurov, Neuron 14, 599 (1995)]. Furthermore, LTP induced at one synapse in CA1 stratum oriens may be accompanied by potentiation in a second untetanized pathway [S. Otani, J. A. Connor, W. B. Levy, Learn. Memory 2, 101 (1995)]. Heterosynaptic effects may also occur in prefrontal neurons [J. C. Hirsch, G. Barrionuevo, F. Crepel, Synapse 12, 82 (1992)] and cerebellar Purkinje cells [P. Vincent and A. Marty, Neuron 11, 885 (1993); A. Marty and I. Llano, Curr. Opin. Neurobiol. 5, 335 (1995)].
11. In the hippocampal CA1 region or dentate gyrus, heterosynaptic depression also accompanies induction of LTP [G. S. Lynch, T. Dunwiddie, V. Gribkoff, Nature 266, 737 (1977); W. C. Abraham and G. V. Goddard, ibid. 305, 717 (1983); J. E. Bradler and G. Barrionuevo, Neuroscience 35, 265 (1990); B. R. Christie and W. C. Abraham, Synapse 10, 1 (1992)], and LTD at one synapse may reverse LTP at another [D. Muller, S. Hefft, A. Figurov, Neuron 14, 599 (1995)]. Furthermore, LTP induced at one synapse in CA1 stratum oriens may be accompanied by potentiation in a second untetanized pathway [S. Otani, J. A. Connor, W. B. Levy, Learn. Memory 2, 101 (1995)]. Heterosynaptic effects may also occur in prefrontal neurons [J. C. Hirsch, G. Barrionuevo, F. Crepel, Synapse 12, 82 (1992)] and cerebellar Purkinje cells [P. Vincent and A. Marty, Neuron 11, 885 (1993); A. Marty and I. Llano, Curr. Opin. Neurobiol. 5, 335 (1995)].
12. In the hippocampal CA1 region or dentate gyrus, heterosynaptic depression also accompanies induction of LTP [G. S. Lynch, T. Dunwiddie, V. Gribkoff, Nature 266, 737 (1977); W. C. Abraham and G. V. Goddard, ibid. 305, 717 (1983); J. E. Bradler and G. Barrionuevo, Neuroscience 35, 265 (1990); B. R. Christie and W. C. Abraham, Synapse 10, 1 (1992)], and LTD at one synapse may reverse LTP at another [D. Muller, S. Hefft, A. Figurov, Neuron 14, 599 (1995)]. Furthermore, LTP induced at one synapse in CA1 stratum oriens may be accompanied by potentiation in a second untetanized pathway [S. Otani, J. A. Connor, W. B. Levy, Learn. Memory 2, 101 (1995)]. Heterosynaptic effects may also occur in prefrontal neurons [J. C. Hirsch, G. Barrionuevo, F. Crepel, Synapse 12, 82 (1992)] and cerebellar Purkinje cells [P. Vincent and A. Marty, Neuron 11, 885 (1993); A. Marty and I. Llano, Curr. Opin. Neurobiol. 5, 335 (1995)].
13. In the hippocampal CA1 region or dentate gyrus, heterosynaptic depression also accompanies induction of LTP [G. S. Lynch, T. Dunwiddie, V. Gribkoff, Nature 266, 737 (1977); W. C. Abraham and G. V. Goddard, ibid. 305, 717 (1983); J. E. Bradler and G. Barrionuevo, Neuroscience 35, 265 (1990); B. R. Christie and W. C. Abraham, Synapse 10, 1 (1992)], and LTD at one synapse may reverse LTP at another [D. Muller, S. Hefft, A. Figurov, Neuron 14, 599 (1995)]. Furthermore, LTP induced at one synapse in CA1 stratum oriens may be accompanied by potentiation in a second untetanized pathway [S. Otani, J. A. Connor, W. B. Levy, Learn. Memory 2, 101 (1995)]. Heterosynaptic effects may also occur in prefrontal neurons [J. C. Hirsch, G. Barrionuevo, F. Crepel, Synapse 12, 82 (1992)] and cerebellar Purkinje cells [P. Vincent and A. Marty, Neuron 11, 885 (1993); A. Marty and I. Llano, Curr. Opin. Neurobiol. 5, 335 (1995)].
14. In the hippocampal CA1 region or dentate gyrus, heterosynaptic depression also accompanies induction of LTP [G. S. Lynch, T. Dunwiddie, V. Gribkoff, Nature 266, 737 (1977); W. C. Abraham and G. V. Goddard, ibid. 305, 717 (1983); J. E. Bradler and G. Barrionuevo, Neuroscience 35, 265 (1990); B. R. Christie and W. C. Abraham, Synapse 10, 1 (1992)], and LTD at one synapse may reverse LTP at another [D. Muller, S. Hefft, A. Figurov, Neuron 14, 599 (1995)]. Furthermore, LTP induced at one synapse in CA1 stratum oriens may be accompanied by potentiation in a second untetanized pathway [S. Otani, J. A. Connor, W. B. Levy, Learn. Memory 2, 101 (1995)]. Heterosynaptic effects may also occur in prefrontal neurons [J. C. Hirsch, G. Barrionuevo, F. Crepel, Synapse 12, 82 (1992)] and cerebellar Purkinje cells [P. Vincent and A. Marty, Neuron 11, 885 (1993); A. Marty and I. Llano, Curr. Opin. Neurobiol. 5, 335 (1995)].
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21. 2, 2.5 mM KCl, and 10 mM Hepes (pH7.3)].
22. 2, 2.5 mM KCl, and 10 mM Hepes (pH7.3)].
23. + for 10 s. Myocytes loaded with nitr-5-AM were transferred to the recording chamber containing untreated Xenopus nerve-muscle cultures. Cell manipulation was performed as previously described (14).
24. The distance refers to the center-to-center distance between the spherical myocytes. The diameter of the myocytes was 29 ± 7 μm (mean ± SEM, n = 50). Physical contact between the two myocytes was avoided because these cells undergo electrical coupling after contact in culture [M. Chow and M.-m. Poo, J. Physiol. (London) 346, 181 (1984)].
25. 2+ imaging with the fluorescent dye fluo-3 in separate myocyte cultures and with a 10-s UV light exposure through the same optics.
26. 2+ imaging with the fluorescent dye fluo-3 in separate myocyte cultures and with a 10-s UV light exposure through the same optics.
27. 2, and 10 mM Hepes (pH 7.2). Recordings were made at room temperature in Hepes-buffered Ringer's solution, to which B27 supplement [1 : 100 (v/v); Gibco] was added to provide antioxidants to help prevent UV-induced cell damage. Extracellular stimulation of the presynaptic neuron was achieved with a patch electrode at the cell body under loose-seal conditions. The recorded membrane current was filtered at 1 kHz and stored on videotape, for later playback on a storage oscilloscope ( TDS320; Tektronix) or an oscillographic recorder (TA240; Gould) and for analysis by computer with the SCAN program (J. Dempster, University of Strathclyde, Glasgow, UK).
28. 2, and 10 mM Hepes (pH 7.2). Recordings were made at room temperature in Hepes-buffered Ringer's solution, to which B27 supplement [1 : 100 (v/v); Gibco] was added to provide antioxidants to help prevent UV-induced cell damage. Extracellular stimulation of the presynaptic neuron was achieved with a patch electrode at the cell body under loose-seal conditions. The recorded membrane current was filtered at 1 kHz and stored on videotape, for later playback on a storage oscilloscope ( TDS320; Tektronix) or an oscillographic recorder (TA240; Gould) and for analysis by computer with the SCAN program (J. Dempster, University of Strathclyde, Glasgow, UK).
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31. The site of innervation on spherical myocytes is centrally located on the substrate-facing surface and not at the apparent perimeter of the myocyte (6). Therefore, distances between the two myocytes were obtained by measuring the distance between the centers of the two myocytes along the neurite. Two myocytes may be located on the same neurite without branches, on two different branches of the same neurite, or on two different neuntes, regardless of their relative distances from the cell body.
32. Local perfusion of culture medium was achieved with a large suction micropipette (inner diameter, 10 to 20 μm) connected by means of fluid-filled tubing to a fluid reservoir. The suction or outflow pressure was adjusted by changing the level of the fluid reservoir relative to that of the culture dish. The flow pattern was tested before the experiment with medium containing trypan blue (Fig. 4B) and was monitored during the experiment by observing the movement of small cell debris in the culture.
33. 2 = 2Dt, where s is the average distance of diffusion over time t, and D is the diffusion coefficient. For a globular protein of 45 kD, such as ovalbumin, the diffusion coefficient in these Xenopus neurites was 15.8 ± 2.1 μm2/5 [S. Popov and M.-m. Poo, J. Neurosci. 12, 77 (1992)]. Thus, the average time required for diffusion of a cytosolic protein of 45 kD over a distance of 150 to 200 μm is ∼ 12 to 20 min. Simple diffusional signaling between the synapses could thus account for the delay in the onset of synaptic depression observed at distant sites. Active retrograde transport could achieve a rate of 30 to 180 μm/min [R. D. Allen, J. Metuzals, I. Tasaki, S. T. Brady, S. P. Gilbert, Science 218, 1127 (1982)], allowing more rapid signaling than diffusion.
34. 2 = 2Dt, where s is the average distance of diffusion over time t, and D is the diffusion coefficient. For a globular protein of 45 kD, such as ovalbumin, the diffusion coefficient in these Xenopus neurites was 15.8 ± 2.1 μm2/5 [S. Popov and M.-m. Poo, J. Neurosci. 12, 77 (1992)]. Thus, the average time required for diffusion of a cytosolic protein of 45 kD over a distance of 150 to 200 μm is ∼ 12 to 20 min. Simple diffusional signaling between the synapses could thus account for the delay in the onset of synaptic depression observed at distant sites. Active retrograde transport could achieve a rate of 30 to 180 μm/min [R. D. Allen, J. Metuzals, I. Tasaki, S. T. Brady, S. P. Gilbert, Science 218, 1127 (1982)], allowing more rapid signaling than diffusion.
35. 2+, the nature of which remains obscure. In principle, the latter could be a membrane-permeant diffusible signal that acts locally at the synapse. Alternatively, the signal may be mediated by membrane-bound surface molecules that act across the synaptic cleft. Evidence suggests that nitric oxide (NO) may mediate a presynaptic modulation of transmitter secretion induced by long-term repetitive postsynaptic depolarizations at Xenopus neuromuscular junctions [T. Wang, Z. Xie, B. Lu, Nature 374, 262 (1995)]. Our attempts to demonstrate a role for NO in hetereosynaptic or ACh-induced synaptic depression, which may involve mechanisms distinct from those activated by long-term repetitive depolarizations, have so far been unsuccessful.
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37. Supported by grants from NSF (IBN 22106) to M.-m.P. and NIH (NS 15114) to R.S.Z.