1. Cell Biology
  2. Neuroscience

Mitochondrial support of persistent presynaptic vesicle mobilization with age-dependent synaptic growth after LTP

  1. Heather L Smith
  2. Jennifer N Bourne
  3. Guan Cao
  4. Michael A Chirillo
  5. Linnaea E Ostroff
  6. Deborah J Watson
  7. Kristen M Harris  Is a corresponding author
  1. Center for Learning and Memory, Institute for Neuroscience, University of Texas at Austin, United States
  2. University of Colorado Denver - Anschutz Medical Campus, United States
  3. New York University, New York
https://doi.org/10.7554/eLife.15275
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Cite this article
  1. Heather L Smith
  2. Jennifer N Bourne
  3. Guan Cao
  4. Michael A Chirillo
  5. Linnaea E Ostroff
  6. Deborah J Watson
  7. Kristen M Harris
(2016)
Mitochondrial support of persistent presynaptic vesicle mobilization with age-dependent synaptic growth after LTP
eLife 5:e15275.
https://doi.org/10.7554/eLife.15275
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10 figures and 1 table

Figures

Figure 1
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Stable responses during control stimulation and expression of LTP following TBS in S. radiatum of area CA1 in acute hippocampal slices.

(A) P15 slice in interface chamber. Recording electrode (R) between two stimulating electrodes (S1 and S2) separated by more than 500 µm. Rectangles indicate the regions from which tissue was …

https://doi.org/10.7554/eLife.15275.002
Figure 2
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Maintenance of SSBs and increase in MSBs following induction of LTP by TBS at P15.

(A) Spine density (#/µm length of reconstructed dendrite) from perfusion-fixed (PF) decreased under control stimulation (Con) and increased at 120 min after TBS induction of LTP (F (2, 60)=26.45, p<0…

https://doi.org/10.7554/eLife.15275.003
Figure 3
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Presynaptic boutons with mitochondria had more vesicles than those without mitochondria in PF hippocampal area CA1 at P15.

(A) Three neighboring presynaptic boutons located along the same axon (translucent gray). Bouton 1 (b1) was an MSB with two postsynaptic partners (PSDs, red) that contained a mitochondrion (navy), …

https://doi.org/10.7554/eLife.15275.004
Figure 4
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Synapses had fewer vesicles and PSD areas were smaller as distance from an axonal mitochondrion increased.

(A) Nondocked vesicles versus mitochondrial distance (Dm) had a statistically significant breakpoint at 2.97 ± 0.67 µm (t(165) = 4.4, p<0.001). (B) The breakpoint for docked vesicles per PSD area …

https://doi.org/10.7554/eLife.15275.005
Figure 5
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The relative distribution of mitochondrial distances from synapses was unchanged for control and LTP conditions at P15.

Representative axons are shown from the control (Con) and TBS sites for each time point (5’, 30’, 120’ = minutes) after the induction of LTP at P15. Each axon is oriented to illustrate sequentially …

https://doi.org/10.7554/eLife.15275.006
Figure 6
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Mobilization of presynaptic vesicles was restricted to presynaptic boutons with or near mitochondria.

Representative 3D reconstructions of boutons with mitochondria (navy, top row) and without mitochondria (second row) with PSDs (red), docked vesicles (blue), and nondocked vesicles (green) at (A) 5 …

https://doi.org/10.7554/eLife.15275.007
Figure 7
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Effect of synapse size and mitochondrial presence on vesicle mobilization following TBS at P15.

Synapses with mitochondria located among the presynaptic vesicles (Mito) were compared to those without mitochondria (>1 µm to Mito). At 30 min following TBS, boutons with mitochondria had (A) fewer …

https://doi.org/10.7554/eLife.15275.008
Figure 8
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Vesicle mobilization was also greatest in presynaptic boutons that contained a mitochondrion at 120 min following TBS in adult hippocampus.

(A–B) Representative EMs of presynaptic boutons (green B) from 120 min control (A1 mito, A2 no mito) and TBS (B1 mito, B2 no mito) conditions (red arrows, PSDs in A1, B2, scale bar is 0.5 µm). (C) …

https://doi.org/10.7554/eLife.15275.009
Figure 9
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Changes in mitochondrial dimensions in P15 and adult hippocampal axons.

(A–B) Representative 3D reconstructions of axons from P15 and adult (Adult) control and TBS conditions at 120 min. (Total axon segment lengths – Lt, black lines – mitochondrial dimensions, length – …

https://doi.org/10.7554/eLife.15275.010
Figure 10
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Synaptic and nonsynaptic mitochondria exhibited non-orthodox configurations after TBS-induction of LTP at both ages.

(A1) The orthodox mitochondrial configuration had cristae with uniformly thin widths (<20 nm) and homogeneously gray matrices. (A2) The condensed mitochondrial configuration had wider and more …

https://doi.org/10.7554/eLife.15275.011

Tables

Table 1

Sample sizes for axons, boutons, vesicles, and mitochondria under each condition. Table 1 provides total n’s for each of the figures. Dashes mean that category was not used in a particular figure. Fi…

https://doi.org/10.7554/eLife.15275.012

Age

P15

Adult

Time

Perfused

5 min

30 min

120 min

120 min

Condition

R88

R89

CON

LTP

CON

LTP

CON

LTP

CON

LTP

# dendrites

9

8

19

20

23

28

24

22

8

8

# bricks

2

2

–

–

–

–

4

4

6, 4

6, 4

Total Brick Volume (µm2)

54

65

–

–

–

-

147

125

165, 99

222, 145

Axons (total n)

Figure 3, 4

85 (44)

77 (37)

–

-

–

–

–

–

–

–

Figure 5, 6

–

–

132

108

143

184

88

144

–

–

Figure 7

–

–

–

–

143

184

88

144

–

-

Figure 8

–

-

–

–

–

–

–

–

225

289

Figure 9

–

–

–

–

–

–

71

121

80

80

Figure 9 axon length

–

–

–

–

–

–

12.5 ± 2.9

13.0 ± 2.9

11.0 ± 1.4

12.6 ± 1.7

Boutons (total n)

Figure 2

89

84

–

–

–

–

165

208

–

–

Figure 3, 4

77

113

–

–

–

–

–

–

–

–

Figure 5, 6

–

–

132

108

143

184

88

144

–

–

Figure 7

–

–

–

–

143

184

88

144

–

-

Figure 8

–

-

–

-

–

-

–

-

225

289

Mitochondria (total n)

Figure 3H,I

36

39

–

-

–

–

–

–

–

–

Figure 9C

–

–

–

-

–

-

128

196

265

334

Figure 9D,E

–

-

–

-

–

-

80

80

80

80

Figure 9F

–

–

–

–

–

–

71

121

80

80

Figure 10A–C

–

–

–

–

–

–

88

105

161

159

Figure 10D

–

–

–

–

–

–

33

36

40

40

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