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Articles, Development/Plasticity/Repair

Aerobic Exercise Protects Retinal Function and Structure from Light-Induced Retinal Degeneration

Eric C. Lawson, Moon K. Han, Jana T. Sellers, Micah A. Chrenek, Adam Hanif, Marissa A. Gogniat, Jeffrey H. Boatright and Machelle T. Pardue
Journal of Neuroscience 12 February 2014, 34 (7) 2406-2412; DOI: https://doi.org/10.1523/JNEUROSCI.2062-13.2014
Eric C. Lawson
1Department of Ophthalmology, Emory University School of Medicine, Atlanta, Georgia 30322, and
2Rehab R&D Center, Atlanta Veterans Administration Medical Center, Decatur, Georgia 30033
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Moon K. Han
2Rehab R&D Center, Atlanta Veterans Administration Medical Center, Decatur, Georgia 30033
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Jana T. Sellers
1Department of Ophthalmology, Emory University School of Medicine, Atlanta, Georgia 30322, and
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Micah A. Chrenek
1Department of Ophthalmology, Emory University School of Medicine, Atlanta, Georgia 30322, and
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Adam Hanif
2Rehab R&D Center, Atlanta Veterans Administration Medical Center, Decatur, Georgia 30033
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Marissa A. Gogniat
2Rehab R&D Center, Atlanta Veterans Administration Medical Center, Decatur, Georgia 30033
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Jeffrey H. Boatright
1Department of Ophthalmology, Emory University School of Medicine, Atlanta, Georgia 30322, and
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Machelle T. Pardue
1Department of Ophthalmology, Emory University School of Medicine, Atlanta, Georgia 30322, and
2Rehab R&D Center, Atlanta Veterans Administration Medical Center, Decatur, Georgia 30033
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  • Figure 1.
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    Figure 1.

    Aerobic exercise protects retinal function after light exposure. A, Representative ERG waveforms from the brightest flash stimulus (2.1 log cd s/m2). B, Maximum a- and b-wave amplitudes did not diminish between 1 and 2 weeks after light exposure. Stimulus response curves at 2 weeks after light exposure for dark-adapted a-wave (C) and b-wave (D) amplitudes. Bright + Treadmill-treated mice (red) had significantly greater amplitudes at 0.8 and 2.1 log cd s/m2 compared with Bright + Inactive mice (blue) for both the a-wave and b-wave (two-way repeated-measures ANOVA; a-wave, F(3,239) = 14.896, p < 0.001; b-wave, F(3,239) = 8.759, p < 0.001), indicating preservation of photoreceptor and inner retinal function. Values are mean ± SEM. Holm–Sidak post hoc comparisons: *p < 0.05, **p < 0.003.

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    Figure 2.

    Aerobic exercise preserved photoreceptor structure after LIRD. Retinal micrographs from BALB/c mice exposed to Dim + Inactive (A), Dim + Treadmill (B), Bright + Inactive (C, D), or Bright + Treadmill (E, F). Images represent retinal sections taken 1.0 mm from the optic nerve. For the bright light-exposed groups, we presented micrographs showing the maximal (C, E) and minimal (D, F) number of photoreceptor nuclei for each group. Mice that received bright light and treadmill exercise treatment (E, F) had thicker outer nuclear layers, and outer and inner photoreceptor segments than those of the Bright + Inactive group (C, D). G, The number of photoreceptors in exercised mice exposed to bright light was significantly decreased at all retinal locations but significantly preserved by exercise (two-way repeated-measures ANOVA, main effect of treatment, F(3,147) = 75.9, p < 0.001). H, Bright + Treadmill mice had significantly more total photoreceptor nuclei compared with Bright + Inactive mice (one-way ANOVA F(3,36) = 78.3, p < 0.001). Holm–Sidak post hoc comparisons: *p < 0.001. OS, Outer segments; IS, inner segments; OPL, outer plexiform layer; INL, inner nuclear layer; IPL, inner plexiform layer; GCL, ganglion cell layer. Values are mean ± SEM.

  • Figure 3.
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    Figure 3.

    Aerobic exercise increases local and systemic BDNF protein levels. Naive BALB/c mice exercised on a treadmill had significantly greater BDNF protein levels in the (A) serum (Student's t test, *p = 0.003), (B) hippocampus (Student's t test, *p = 0.004), and (C) retina (Student's t test, *p = 0.024) compared with inactive mice. Values are mean ± SEM.

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    Figure 4.

    Treatment with the TrkB antagonist, ANA-12, eliminates protective effects of aerobic exercise on retinal degeneration. ANA-12 had no effect on normal photoreceptor (A) and inner retinal (B) function as measured by ERG a- and b-wave amplitudes, respectively, in dim-exposed mice. C, Representative ERG waveforms from the brightest flash (2.1 log cd s/m2) taken 1 week after bright light exposure illustrate that the Treadmill + ANA-12 group had reduced amplitude responses compared with Treadmill + Vehicle; arrows indicate a- and b-waves. D, E, Stimulus response curves for dark-adapted a-wave (D) and b-wave (E) amplitudes for all groups at 1 week after light exposure. Bright + Treadmill + Vehicle-treated mice (green) showed significantly greater amplitudes at bright flash intensities compared with Bright + Treadmill + ANA-12 mice (orange) for the a-wave (two-way repeated-measures ANOVA; F(12,184) = 2.31, p = 0.01) and b-wave (F(12,184) = 2.29, p = 0.01), indicating elimination of the protective effect of aerobic exercise using a BDNF trkB receptor antagonist. Bright + Treadmill + ANA-12, Bright + Inactive + Vehicle, and Bright + Inactive + ANA-12 groups had no significant differences. Holm-Sidak post hoc comparisons: *p < 0.05, **p < 0.01, ***p < 0.001. Significance differences between Bright + Treadmill + Vehicle and the color-coded treatment group. F, Bright + Treadmill + Vehicle mice had significantly more total photoreceptor nuclei compared with Bright + Treadmill + ANA-12 mice and Bright + Inactive mice injected with either ANA-12 or vehicle (one-way ANOVA by ranks, H = 14.85, p = 0.002). Values are mean ± SEM.

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The Journal of Neuroscience: 34 (7)
Journal of Neuroscience
Vol. 34, Issue 7
12 Feb 2014
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Aerobic Exercise Protects Retinal Function and Structure from Light-Induced Retinal Degeneration
Eric C. Lawson, Moon K. Han, Jana T. Sellers, Micah A. Chrenek, Adam Hanif, Marissa A. Gogniat, Jeffrey H. Boatright, Machelle T. Pardue
Journal of Neuroscience 12 February 2014, 34 (7) 2406-2412; DOI: 10.1523/JNEUROSCI.2062-13.2014

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Aerobic Exercise Protects Retinal Function and Structure from Light-Induced Retinal Degeneration
Eric C. Lawson, Moon K. Han, Jana T. Sellers, Micah A. Chrenek, Adam Hanif, Marissa A. Gogniat, Jeffrey H. Boatright, Machelle T. Pardue
Journal of Neuroscience 12 February 2014, 34 (7) 2406-2412; DOI: 10.1523/JNEUROSCI.2062-13.2014
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Keywords

  • retinal degeneration
  • exercise
  • photoreceptors
  • brain-derived neurotrophic factor
  • neuroprotection
  • treadmill

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