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Social isolation delays the positive effects of running on adult neurogenesis

Abstract

Social isolation can exacerbate the negative consequences of stress and increase the risk of developing psychopathology. However, the influence of living alone on experiences generally considered to be beneficial to the brain, such as physical exercise, remains unknown. We report here that individual housing precludes the positive influence of short-term running on adult neurogenesis in the hippocampus of rats and, in the presence of additional stress, suppresses the generation of new neurons. Individual housing also influenced corticosterone levels—runners in both housing conditions had elevated corticosterone during the active phase, but individually housed runners had higher levels of this hormone in response to stress. Moreover, lowering corticosterone levels converted the influence of short-term running on neurogenesis in individually housed rats from negative to positive. These results suggest that, in the absence of social interaction, a normally beneficial experience can exert a potentially deleterious influence on the brain.

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Figure 1: Social isolation reverses the positive influence of short-term running on adult neurogenesis.
Figure 2: Social context mediates the running effect on cell proliferation; newly generated cells express neuronal, glial and endothelial markers.
Figure 3: Glucocorticoid levels are altered by running and social housing.
Figure 4: Lowering glucocorticoid levels reverses the suppression of neurogenesis in isolated runners.
Figure 5: A long duration of physical activity enhances cell proliferation in the dentate gyrus of socially isolated rats.
Figure 6: Daily stress interacts with running and social housing to alter cell proliferation.
Figure 7: The duration of previous isolation affects the response of cell proliferation to running alone.

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Acknowledgements

The authors acknowledge the assistance of C. Gross, Y. Kozorovitskiy, B. Leuner and C. Mirescu in the preparation of this manuscript. This work was supported by a National Research Service Award predoctoral fellowship to A.S. and a National Institutes of Mental Health grant to E.G.

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Correspondence to Elizabeth Gould.

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Supplementary information

Supplementary Fig. 1

Differences in the amount of running do not explain differences in neurogenesis across housing conditions or glucocorticoid status. (PDF 18 kb)

Supplementary Fig. 2

The volume of the dentate gyrus increases with prolonged physical activity. (PDF 64 kb)

Supplementary Fig. 3

The increase in neurogenesis with short-term running in group-housed animals is sustained over longer periods of activity. (PDF 106 kb)

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Stranahan, A., Khalil, D. & Gould, E. Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 9, 526–533 (2006). https://doi.org/10.1038/nn1668

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