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. 2010 Feb 2;107(5):2367-72.
doi: 10.1073/pnas.0911725107. Epub 2010 Jan 19.

Running enhances spatial pattern separation in mice

David J Creer  1 , Carola Romberg, Lisa M Saksida, Henriette van Praag, Timothy J Bussey
Affiliations

Running enhances spatial pattern separation in mice

David J Creer et al. Proc Natl Acad Sci U S A. .

Abstract

Increasing evidence suggests that regular exercise improves brain health and promotes synaptic plasticity and hippocampal neurogenesis. Exercise improves learning, but specific mechanisms of information processing influenced by physical activity are unknown. Here, we report that voluntary running enhanced the ability of adult (3 months old) male C57BL/6 mice to discriminate between the locations of two adjacent identical stimuli. Improved spatial pattern separation in adult runners was tightly correlated with increased neurogenesis. In contrast, very aged (22 months old) mice had impaired spatial discrimination and low basal cell genesis that was refractory to running. These findings suggest that the addition of newly born neurons may bolster dentate gyrus-mediated encoding of fine spatial distinctions.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Mice were trained to distinguish between arrays of stimuli displayed on a touch screen in an operant chamber. (A) Three stimulus arrays were used during the experiments. (i) Mice were initially trained with an intermediate separation between stimuli for task training. Thereafter, animals started probe sessions with big (ii) and small (iii) stimulus separation conditions. (B) Mice were housed with or without a running wheel. (C) Timeline of the study.
Fig. 2.
Fig. 2.
Acquisition of big and small separation between stimuli. Mice were trained to reach a criterion of seven of eight trials correct. (A) Runners (run) performed better than controls (con) in acquisition in the small separation condition (*P < 0.05) but not in the big separation condition (P > 0.24). (B) Trend toward a correlation between trials to acquisition of the small separation and newly born neuron density was observed (P = 0.13). Photomicrographs of BrdU-positive cells in control (C) and runner (D) dentate gyrus 10 weeks after the last injection. (Scale bar: 50 μm)
Fig. 3.
Fig. 3.
Reversal of stimulus reinforcement in the big and small conditions. The reinforcement of the stimuli was reversed each time a mouse reached criterion so that the previously correct location became the incorrect location and vice versa. (A) There was no difference between the groups in the big separation condition in the number of reversals. con, control; run, runner. (B) Runners performed better than controls in the reversal task when the separation between stimuli was small (*P < 0.002). (C) Significant correlation between task performance in the small condition and newly born neuron density was observed (P < 0.03). Confocal images of BrdU-positive cells in the dentate gyrus of sections derived from control (D) and runner (E) mice 10 weeks after the last injection. Sections were immunofluorescent double-labeled for BrdU (green) and NeuN (red). (Scale bar: 50 μm) (F) Newly born neuron density was increased in runners as compared with controls (*P < 0.0001).
Fig. 4.
Fig. 4.
Intermediate spatial pattern separation in aged mice. Mice (n = 8) were trained for 10 days under sedentary conditions (block 1). Thereafter, mice were divided into sedentary (n = 4) and runner (n = 4) groups, injected with BrdU over 5 days, and trained for an additional 10 days on the same task (block 2). (A) Running improved performance on acquisition of the task in block 2 as compared with block 1 (P < 0.03). (B) Reversal performance was not influenced by exercise. con, control; run, runner. The number of BrdU-labeled cells did not differ between controls (C) and runners (D) at 17 days. (E and F) Lectin-stained vessel density was quantified using imaging software. There was no change in dentate gyrus vasculature in running aged mice (F) as compared with controls (E). (Scale bar: 100 μm.)
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