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Research ArticleNew Research, Cognition and Behavior

Early-Age Running Enhances Activity of Adult-Born Dentate Granule Neurons Following Learning in Rats

Olga Shevtsova, Yao-Fang Tan, Christina M. Merkley, Gordon Winocur and J. Martin Wojtowicz
eNeuro 14 August 2017, 4 (4) ENEURO.0237-17.2017; https://doi.org/10.1523/ENEURO.0237-17.2017
Olga Shevtsova
1Department of Physiology, University of Toronto, Toronto, Ontario M5S1A8, Canada
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Yao-Fang Tan
1Department of Physiology, University of Toronto, Toronto, Ontario M5S1A8, Canada
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Christina M. Merkley
1Department of Physiology, University of Toronto, Toronto, Ontario M5S1A8, Canada
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Gordon Winocur
2Rotman Research Institute, Baycrest Centre, Toronto, Ontario M6E2E1, Canada
3Department of Psychology, Trent University, Peterborough, K9J7B8, Canada
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J. Martin Wojtowicz
1Department of Physiology, University of Toronto, Toronto, Ontario M5S1A8, Canada
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  • Figure 1.
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    Figure 1.

    Experimental timeline. At one month of age, a group of 40 rats was exposed to running wheel while the other group was kept in standard cages for six weeks. All rats were trained on the contextual fear conditioning (CFC) task in context A. Two weeks after training, 10 rats from each group were tested in context A, A’, or B. The remaining rats served as untested controls. Mitotic marker CldU was injected three weeks before training. Ninety minutes after the test, all animals were perfused for immunohistochemistry.

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    Figure 2.

    c- Fos activity in DG neurons. A, Fluorescent microscopic images showing c-Fos cells in the DG of control and tested rats. White arrows indicate c-Fos-labeled cells in the GCL of the DG. B, The number (mean ± SEM) of c-Fos-labeled cells per DG. Tested animals showed significantly more c-Fos+ cells per DG than controls (*p < 0.05). A similar result was obtained for the CA1 field of the hippocampus (Fig. 2-1, Extended data). C, Running and individual tested groups. Controls, non-tested cage controls; A, tested in the familiar environment; A’, tested in the similar environment; B, tested in the novel environment. The number of c-Fos+ cells was greater in all tested groups compared to controls in runners and non-runners (*p < 0.05, n = 10 rats/group).

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    Figure 3.

    Neuronal activity in adult-born neurons in runners and non-runners. A, Confocal microscopic images showing c-Fos- and CldU-labeled cells within the subgranular zone (SGZ) of the GCL. White arrows indicate dual-labeled c-Fos+/CldU+ cells in the GCL. Boxed area is enlarged in the inset showing the double-labeled cell. Scale bars, 100 µm. B, Graph showing % expression of c-Fos+ cells in CldU+ cells within DG in control and tested groups. There is a significant effect of running in memory tested group (*p < 0.05, n = 10 rats/control group; n = 30 rats/memory-tested group). No difference in cell numbers between control and tested rats in non-runners.

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    Figure 4.

    c-Fos activity in adult-born neurons is enhanced by running. A, Representative images of c-Fos+/CldU+-labeled cells within the GCL. White arrow indicates dual-labeled cells. The inset shows a high magnification view of the c-Fos+/CldU+-labeled cell. Scale bars, 50 µm. B, Absolute numbers of double-labeled c-Fos+/CldU+ cells. Comparison of tested groups (controls, context A, A’, and B) within runners and non-runners. All three tested groups have significantly more cell numbers compared to controls (*p < 0.05, n = 10 rats/control group; n = 30 rats/memory tested group). The numbers of CldU+ cells did not differ in any of the groups (Fig. 4-1, Extended data). C, Graph showing % expression of c-Fos in CldU cells. Controls, non-tested cage controls; A, tested in the familiar environment; A’, tested in the similar environment; B, tested in the novel environment. The percentage of c-Fos expression in CldU cells was greater in all tested groups compared to controls in runners (*p < 0.05, n = 10 rats/group).

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    Figure 5.

    Results of CFC training and testing. Early running did not affect acquisition of the CF response during training. There were no differences among the group A (familiar environment) tested animals. The group A’ (similar environment) showed significantly (**p = 0.01) less freezing in runners. The group B (different environment) showed significantly (*p < 0.05) less freezing in runners.

Extended Data

  • Figures
  • Figure 2-1

    Activity-dependent regulation of c-Fos in the CA1 area of the hippocampus. Number (mean ± SEM) of c-Fos-labeled cells per CA1. Tested rats had significantly more cFos+ cells per CA1 compared to controls. Two-way ANOVA shows an effect of testing (F(3,79) = 10.838, *p = 0.001). There was no effect of running (F(1,79) = 1.131, p = 0.291) and no interaction (F(3,79) = 2.151, p = 0.101). Download Figure 2-1, TIF file.

  • Figure 4-1

    Cell survival in the DG. Graph showing number (mean ± SEM) of CldU-labeled cells per DG. No difference in the number of CldU+ cells was detected between groups. Two-way ANOVA shows no effect of running (F(1,79) = 1.749, p = 0.19), testing (F(1,79) = 0.56, p = 0.453) and no interactions. Download Figure 4-1, TIF file.

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July/August 2017
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Early-Age Running Enhances Activity of Adult-Born Dentate Granule Neurons Following Learning in Rats
Olga Shevtsova, Yao-Fang Tan, Christina M. Merkley, Gordon Winocur, J. Martin Wojtowicz
eNeuro 14 August 2017, 4 (4) ENEURO.0237-17.2017; DOI: 10.1523/ENEURO.0237-17.2017

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Early-Age Running Enhances Activity of Adult-Born Dentate Granule Neurons Following Learning in Rats
Olga Shevtsova, Yao-Fang Tan, Christina M. Merkley, Gordon Winocur, J. Martin Wojtowicz
eNeuro 14 August 2017, 4 (4) ENEURO.0237-17.2017; DOI: 10.1523/ENEURO.0237-17.2017
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Keywords

  • adult neurogenesis
  • dentate gyrus
  • hippocampus
  • learning and memory
  • plasticity

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