Running Enhances Spatial Pattern Separation in Mice

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2010 Feb 6

PMID 20133882

Citations 260

Authors

David J Creer

Carola Romberg

Lisa M Saksida

Henriette van Praag

Timothy J Bussey

Affiliations

Soon will be listed here.

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.

Citing Articles

Hippocampal Functional Connectivity and Cognitive Stability in Parasellar Meningiomas (Studied by the "Virtually Implanted Electrode" Method).

Savkina E, Vartanov A, Kaverina M, Kuleva A, Galkin M, Krotkova O Sovrem Tekhnologii Med. 2025; 16(6):5-15.

PMID: 39896149 PMC: 11780584. DOI: 10.17691/stm2024.16.6.01.

Pharmacological Enhancement of Adult Hippocampal Neurogenesis Improves Behavioral Pattern Separation in Young and Aged Male Mice.

Chang W, Tegang K, Samuels B, Saxe M, Wichmann J, David D Biol Psychiatry Glob Open Sci. 2025; 5(2):100419.

PMID: 39830600 PMC: 11741898. DOI: 10.1016/j.bpsgos.2024.100419.

Engagement in moderate-intensity physical activity supports overnight memory retention in older adults.

Chappel-Farley M, Berisha D, Dave A, Sanders R, Kline C, Janecek J Sci Rep. 2024; 14(1):31873.

PMID: 39738288 PMC: 11686232. DOI: 10.1038/s41598-024-83336-0.

Effect of adult hippocampal neurogenesis on pattern separation and its applications.

Wang Z, Yang K, Sun X Cogn Neurodyn. 2024; 18(5):1-14.

PMID: 39568526 PMC: 11564429. DOI: 10.1007/s11571-024-10110-3.

Environmental enrichment in middle age rats improves spatial and object memory discrimination deficits.

Miranda M, Navas M, Zanoni Saad M, Piromalli Girado D, Weisstaub N, Bekinschtein P Front Behav Neurosci. 2024; 18:1478656.

PMID: 39494036 PMC: 11528545. DOI: 10.3389/fnbeh.2024.1478656.

References

Colcombe S, Erickson K, Raz N, Webb A, Cohen N, McAuley E . Aerobic fitness reduces brain tissue loss in aging humans. J Gerontol A Biol Sci Med Sci. 2003; 58(2):176-80. DOI: 10.1093/gerona/58.2.m176. View

van Praag H, Kempermann G, Gage F . Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci. 1999; 2(3):266-70. DOI: 10.1038/6368. View

Neeper S, Gomez-Pinilla F, Choi J, Cotman C . Exercise and brain neurotrophins. Nature. 1995; 373(6510):109. DOI: 10.1038/373109a0. View

van Praag H . Neurogenesis and exercise: past and future directions. Neuromolecular Med. 2008; 10(2):128-40. DOI: 10.1007/s12017-008-8028-z. View

Nakazawa K, McHugh T, Wilson M, Tonegawa S . NMDA receptors, place cells and hippocampal spatial memory. Nat Rev Neurosci. 2004; 5(5):361-72. DOI: 10.1038/nrn1385. View

Pereira A, Huddleston D, Brickman A, Sosunov A, Hen R, McKhann G . An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci U S A. 2007; 104(13):5638-43. PMC: 1838482. DOI: 10.1073/pnas.0611721104. View

Nakazawa K, Quirk M, Chitwood R, Watanabe M, Yeckel M, Sun L . Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science. 2002; 297(5579):211-8. PMC: 2877140. DOI: 10.1126/science.1071795. View

Gazzaley A, Sheridan M, Cooney J, DEsposito M . Age-related deficits in component processes of working memory. Neuropsychology. 2007; 21(5):532-9. DOI: 10.1037/0894-4105.21.5.532. View

Eriksson P, Perfilieva E, Bjork-Eriksson T, Alborn A, Nordborg C, Peterson D . Neurogenesis in the adult human hippocampus. Nat Med. 1998; 4(11):1313-7. DOI: 10.1038/3305. View

10.

Squire L, Stark C, Clark R . The medial temporal lobe. Annu Rev Neurosci. 2004; 27:279-306. DOI: 10.1146/annurev.neuro.27.070203.144130. View

11.

Leutgeb J, Leutgeb S, Moser M, Moser E . Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science. 2007; 315(5814):961-6. DOI: 10.1126/science.1135801. View

12.

Jessberger S, Clark R, Broadbent N, Clemenson Jr G, Consiglio A, Lie D . Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem. 2009; 16(2):147-54. PMC: 2661246. DOI: 10.1101/lm.1172609. View

13.

Farmer J, Zhao X, van Praag H, Wodtke K, Gage F, Christie B . Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience. 2004; 124(1):71-9. DOI: 10.1016/j.neuroscience.2003.09.029. View

14.

Treves A, Rolls E . Computational analysis of the role of the hippocampus in memory. Hippocampus. 1994; 4(3):374-91. DOI: 10.1002/hipo.450040319. View

15.

Lou S, Liu J, Chang H, Chen P . Hippocampal neurogenesis and gene expression depend on exercise intensity in juvenile rats. Brain Res. 2008; 1210:48-55. DOI: 10.1016/j.brainres.2008.02.080. View

16.

Clark P, Brzezinska W, Thomas M, Ryzhenko N, Toshkov S, Rhodes J . Intact neurogenesis is required for benefits of exercise on spatial memory but not motor performance or contextual fear conditioning in C57BL/6J mice. Neuroscience. 2008; 155(4):1048-58. DOI: 10.1016/j.neuroscience.2008.06.051. View

17.

Stranahan A, Khalil D, Gould E . Running induces widespread structural alterations in the hippocampus and entorhinal cortex. Hippocampus. 2007; 17(11):1017-22. PMC: 2956984. DOI: 10.1002/hipo.20348. View

18.

Cotman C, Berchtold N, Christie L . Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci. 2007; 30(9):464-72. DOI: 10.1016/j.tins.2007.06.011. View

19.

Morton A, Skillings E, Bussey T, Saksida L . Measuring cognitive deficits in disabled mice using an automated interactive touchscreen system. Nat Methods. 2006; 3(10):767. DOI: 10.1038/nmeth1006-767. View

20.

Koehl M, Meerlo P, Gonzales D, Rontal A, Turek F, Abrous D . Exercise-induced promotion of hippocampal cell proliferation requires beta-endorphin. FASEB J. 2008; 22(7):2253-62. DOI: 10.1096/fj.07-099101. View