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Behavioural Neurology
Volume 2017, Article ID 6137071, 6 pages
https://doi.org/10.1155/2017/6137071
Research Article

Effect of Voluntary Wheel Running on Striatal Dopamine Level and Neurocognitive Behaviors after Molar Loss in Rats

1Capital University of Physical Education and Sports, Beijing 100191, China
2Beijing Xicheng District Desheng Community Health Service Center, Beijing 100120, China
3Peking University School and Hospital of Stomatology, Beijing 100081, China
4Department of Psychiatry, Yale University School of Medicine, New Haven, CT 06511, USA

Correspondence should be addressed to Jianzhang Liu; nc.ude.umjb@gnahznaijuil and Kun Liu; ude.elay@uil.nuk

Linlin Zhang and Yi Feng contributed equally to this work.

Received 9 June 2017; Revised 25 August 2017; Accepted 2 October 2017; Published 5 December 2017

Academic Editor: Francesca Trojsi

Copyright © 2017 Linlin Zhang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Q. Pang, X. Hu, X. Li, J. Zhang, and Q. Jiang, “Behavioral impairments and changes of nitric oxide and inducible nitric oxide synthase in the brains of molarless KM mice,” Behavioural Brain Research, vol. 278, pp. 411–416, 2015. View at Publisher · View at Google Scholar · View at Scopus
  2. K. J. Joshipura, C. W. Douglass, and W. C. Willett, “Possible explanations for the tooth loss and cardiovascular disease relationship,” Annals of Periodontology, vol. 3, no. 1, pp. 175–183, 1998. View at Publisher · View at Google Scholar
  3. J. Luo, B. Wu, Q. Zhao et al., “Association between tooth loss and cognitive function among 3063 Chinese older adults: a community-based study,” PLoS One, vol. 10, no. 3, article e0120986, 2015. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Nilsson, J. Berglund, and S. Renvert, “Tooth loss and cognitive functions among older adults,” Acta Odontologica Scandinavica, vol. 72, no. 8, pp. 639–644, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. D. Lexomboon, M. Trulsson, I. Wårdh, and M. G. Parker, “Chewing ability and tooth loss: association with cognitive impairment in an elderly population study,” Journal of the American Geriatrics Society, vol. 60, no. 10, pp. 1951–1956, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Yamazaki, N. Wakabayashi, T. Kobayashi, and T. Suzuki, “Effect of tooth loss on spatial memory and TrkB-mRNA levels in rats,” Hippocampus, vol. 18, no. 6, pp. 542–547, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Kato, T. Usami, Y. Noda, M. Hasegawa, M. Ueda, and T. Nabeshima, “The effect of the loss of molar teeth on spatial memory and acetylcholine release from the parietal cortex in aged rats,” Behavioural Brain Research, vol. 83, no. 1-2, pp. 239–242, 1997. View at Publisher · View at Google Scholar · View at Scopus
  8. D. Davis, J. Fiske, B. Scott, and D. R. Radford, “The emotional effects of tooth loss: a preliminary quantitative study,” British Dental Journal, vol. 188, no. 09, pp. 503–506, 2000. View at Publisher · View at Google Scholar
  9. C. H. Hillman, K. I. Erickson, and A. F. Kramer, “Be smart, exercise your heart: exercise effects on brain and cognition,” Nature Reviews Neuroscience, vol. 9, no. 1, pp. 58–65, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. B. K. Tivadar, “Physical activity improves cognition: possible explanations,” Biogerontology, vol. 18, no. 4, pp. 477–483, 2017. View at Publisher · View at Google Scholar
  11. Z. Radak, S. Kumagai, A. W. Taylor, H. Naito, and S. Goto, “Effects of exercise on brain function: role of free radicals,” Applied Physiology, Nutrition, and Metabolism, vol. 32, no. 5, pp. 942–946, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. N. Okudan and M. Belviranli, “Effects of exercise training on hepatic oxidative stress and antioxidant status in aged rats,” Archives of Physiology and Biochemistry, vol. 122, no. 4, pp. 180–185, 2016. View at Publisher · View at Google Scholar · View at Scopus
  13. M. A. Moro, A. Almeida, J. P. Bolaños, and I. Lizasoain, “Mitochondrial respiratory chain and free radical generation in stroke,” Free Radical Biology & Medicine, vol. 39, no. 10, pp. 1291–1304, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. F. T. A. Pijlman, G. Wolterink, and J. M. Van Ree, “Physical and emotional stress have differential effects on preference for saccharine and open field behaviour in rats,” Behavioural Brain Research, vol. 139, no. 1-2, pp. 131–138, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Vaynman, Z. Ying, and F. Gomez‐Pinilla, “Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition,” European Journal of Neuroscience, vol. 20, no. 10, pp. 2580–2590, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. C. H. Chae, H. C. Lee, S. L. Jung et al., “Swimming exercise increases the level of nerve growth factor and stimulates neurogenesis in adult rat hippocampus,” Neuroscience, vol. 212, pp. 30–37, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Šumec, P. Filip, K. Sheardová, and M. Bareš, “Psychological benefits of nonpharmacological methods aimed for improving balance in Parkinson’s disease: a systematic review,” Behavioural Neurology, vol. 2015, Article ID 620674, 16 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  18. S. K. Mittal and C. Eddy, “The role of dopamine and glutamate modulation in Huntington disease,” Behavioural Neurology, vol. 26, no. 4, pp. 255–263, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Costa, A. Peppe, I. Mazzù, M. Longarzo, C. Caltagirone, and G. A. Carlesimo, “Dopamine treatment and cognitive functioning in individuals with Parkinson’s disease: the “cognitive flexibility” hypothesis seems to work,” Behavioural Neurology, vol. 2014, Article ID 260896, 11 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Venkatraman, B. L. Edlow, and M. H. Immordino-Yang, “The brainstem in emotion: a review,” Frontiers in Neuroanatomy, vol. 11, p. 15, 2017. View at Publisher · View at Google Scholar
  21. A. Nieoullon, “Dopamine and the regulation of cognition and attention,” Progress in Neurobiology, vol. 67, no. 1, pp. 53–83, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Nieoullon and A. Coquerel, “Dopamine: a key regulator to adapt action, emotion, motivation and cognition,” Current Opinion in Neurology, vol. 16, Supplement 2, pp. S3–S9, 2003. View at Publisher · View at Google Scholar
  23. R. A. Wise, “Roles for nigrostriatal—not just mesocorticolimbic—dopamine in reward and addiction,” Trends in Neurosciences, vol. 32, no. 10, pp. 517–524, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Gröger, R. Kolb, R. Schäfer, and U. Klose, “Dopamine reduction in the substantia nigra of Parkinson’s disease patients confirmed by in vivo magnetic resonance spectroscopic imaging,” PLoS One, vol. 9, no. 1, article e84081, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. D. Wang, X. Liu, and D. Qiao, “Modulatory effect of subthalamic nucleus on the development of fatigue during exhausting exercise: an in vivo electrophysiological and microdialysis study in rats,” Journal of Sports Science & Medicine, vol. 11, no. 2, pp. 286–293, 2012. View at Google Scholar
  26. S. Fediuc, J. E. Campbell, and M. C. Riddell, “Effect of voluntary wheel running on circadian corticosterone release and on HPA axis responsiveness to restraint stress in Sprague-Dawley rats,” Journal of Applied Physiology, vol. 100, no. 6, pp. 1867–1875, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Iida, T. Hara, D. Araki et al., “Memory-related gene expression profile of the male rat hippocampus induced by teeth extraction and occlusal support recovery,” Archives of Oral Biology, vol. 59, no. 2, pp. 133–141, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. O. Y. Calhan and V. Seyrantepe, “Mice with catalytically inactive cathepsin a display neurobehavioral alterations,” Behavioural Neurology, vol. 2017, Article ID 4261873, 11 pages, 2017. View at Publisher · View at Google Scholar
  29. M. Tahamtan, M. Allahtavakoli, M. Abbasnejad et al., “Exercise preconditioning improves behavioral functions following transient cerebral ischemia induced by 4-vessel occlusion (4-VO) in rats,” Archives of Iranian Medicine, vol. 16, no. 12, pp. 697–704, 2013. View at Google Scholar
  30. L. L. Furlanetti, M. D. Döbrössy, I. A. Aranda, and V. A. Coenen, “Feasibility and safety of continuous and chronic bilateral deep brain stimulation of the medial forebrain bundle in the naïve Sprague-Dawley rat,” Behavioural Neurology, vol. 2015, Article ID 256196, 13 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. D. B. Pahaye, E. N. Bum, G. S. Taïwé et al., “Neuroprotective and antiamnesic effects of Mitragyna inermis willd (Rubiaceae) on scopolamine-induced memory impairment in mice,” Behavioural Neurology, vol. 2017, Article ID 5952897, 11 pages, 2017. View at Publisher · View at Google Scholar
  32. C. Jenner, G. Reali, M. Puopolo, and M. C. Silveri, “Can cognitive and behavioural disorders differentiate frontal variant-frontotemporal dementia from Alzheimer’s disease at early stages?” Behavioural Neurology, vol. 17, no. 2, pp. 89–95, 2006. View at Publisher · View at Google Scholar
  33. S. Sil and T. Ghosh, “Cox-2 plays a vital role in the impaired anxiety like behavior in colchicine induced rat model of Alzheimer disease,” Behavioural Neurology, vol. 2016, Article ID 1501527, 8 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  34. B. C. Dickerson and R. A. Sperling, “Large-scale functional brain network abnormalities in Alzheimer’s disease: insights from functional neuroimaging,” Behavioural Neurology, vol. 21, no. 1-2, pp. 63–75, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. X. Xu, B. Cao, J. Wang, T. Yu, and Y. Li, “Decision-making deficits associated with disrupted synchronization between basolateral amygdala and anterior cingulate cortex in rats after tooth loss,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 60, pp. 26–35, 2015. View at Publisher · View at Google Scholar · View at Scopus
  36. E. J. Yang, U. Mahmood, H. Kim et al., “Alterations in protein phosphorylation in the amygdala of the 5XFamilial Alzheimer’s disease animal model,” Journal of Pharmacological Sciences, vol. 133, no. 4, pp. 261–267, 2017. View at Publisher · View at Google Scholar
  37. M. Onozuka, K. Watanabe, S. Nagasaki et al., “Impairment of spatial memory and changes in astroglial responsiveness following loss of molar teeth in aged SAMP8 mice,” Behavioural Brain Research, vol. 108, no. 2, pp. 145–155, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Oue, Y. Miyamoto, S. Okada et al., “Tooth loss induces memory impairment and neuronal cell loss in APP transgenic mice,” Behavioural Brain Research, vol. 252, pp. 318–325, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Sakamoto, T. Hara, A. Kurozumi et al., “Effect of occlusal rehabilitation on spatial memory and hippocampal neurons after long-term loss of molars in rats,” Journal of Oral Rehabilitation, vol. 41, no. 10, pp. 715–722, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. L. Bäckman, L. Nyberg, U. Lindenberger, S. C. Li, and L. Farde, “The correlative triad among aging, dopamine, and cognition: current status and future prospects,” Neuroscience & Biobehavioral Reviews, vol. 30, no. 6, pp. 791–807, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. J. H. Kim, J. M. Auerbach, J. A. Rodríguez-Gómez et al., “Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson’s disease,” Nature, vol. 418, no. 6893, pp. 50–56, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. P. Remy, M. Doder, A. Lees, N. Turjanski, and D. Brooks, “Depression in Parkinson’s disease: loss of dopamine and noradrenaline innervation in the limbic system,” Brain, vol. 128, no. 6, pp. 1314–1322, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. J. J. Annesi, “Effects of minimal exercise and cognitive behavior modification on adherence, emotion change, self-image, and physical change in obese women,” Perceptual and Motor Skills, vol. 91, no. 1, pp. 322–336, 2000. View at Publisher · View at Google Scholar
  44. F. Nozariyan, P. Shafiniya, V. Shahvali, and M. A. Makiyani, “Emotion changes during exercise in males’ physical education student,” vol. 9, 2016. View at Google Scholar
  45. T. Nozawa, Y. Taki, A. Kanno et al., “Effects of different types of cognitive training on cognitive function, brain structure, and driving safety in senior daily drivers: a pilot study,” Behavioural Neurology, vol. 2015, Article ID 525901, 18 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  46. A. S. Aguiar Jr., A. A. Castro, E. L. Moreira et al., “Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: involvement of hippocampal plasticity via AKT, CREB and BDNF signaling,” Mechanisms of Ageing and Development, vol. 132, no. 11-12, pp. 560–567, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. T. Kobila, Q. R. Liu, K. Gandhi, M. Mughal, Y. Shaham, and H. van Praag, “Running is the neurogenic and neurotrophic stimulus in environmental enrichment,” Learning & Memory, vol. 18, pp. 605–609, 2011. View at Publisher · View at Google Scholar
  48. S. J. Lee, T. W. Kim, H. K. Park et al., “Postnatal treadmill exercise alleviates prenatal stress-induced anxiety in offspring rats by enhancing cell proliferation through 5-Hydroxytryptamine 1A receptor activation,” International Neurourology Journal, vol. 20, Supplement 1, pp. S57–S64, 2016. View at Publisher · View at Google Scholar · View at Scopus
  49. E. E. Bernstein and R. J. McNally, “Acute aerobic exercise hastens emotional recovery from a subsequent stressor,” Health Psychology, vol. 36, no. 6, pp. 560–567, 2017. View at Publisher · View at Google Scholar
  50. X. Zhao, J. Aronowski, S. J. Liu et al., “Wheel-running modestly promotes functional recovery after a unilateral cortical lesion in rats,” Behavioural Neurology, vol. 16, no. 1, pp. 41–49, 2005. View at Publisher · View at Google Scholar
  51. Y. Lin, X. Lu, J. Dong et al., “Involuntary, forced and voluntary exercises equally attenuate neurocognitive deficits in vascular dementia by the BDNF–pCREB mediated pathway,” Neurochemical Research, vol. 40, no. 9, pp. 1839–1848, 2015. View at Publisher · View at Google Scholar · View at Scopus
  52. M. C. Lee, M. Okamoto, Y. F. Liu et al., “Voluntary resistance running with short distance enhances spatial memory related to hippocampal BDNF signaling,” Journal of Applied Physiology, vol. 113, no. 8, pp. 1260–1266, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. A. C. McKee, D. H. Daneshvar, V. E. Alvarez, and T. D. Stein, “The neuropathology of sport,” Acta Neuropathologica, vol. 127, no. 1, pp. 29–51, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. X. Xiao, Q. Lin, W. L. Lo et al., “Cerebral reorganization in subacute stroke survivors after virtual reality-based training: a preliminary study,” Behavioural Neurology, vol. 2017, Article ID 6261479, 8 pages, 2017. View at Publisher · View at Google Scholar
  55. M. Harvey, K. Muir, I. Reeves et al., “Long term improvements in activities of daily living in patients with hemispatial neglect,” Behavioural Neurology, vol. 23, no. 4, pp. 237–239, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Asghar, L. George, and M. F. Lokhandwala, “Exercise decreases oxidative stress and inflammation and restores renal dopamine D1 receptor function in old rats,” American Journal of Physiology-Renal Physiology, vol. 293, no. 3, pp. F914–F919, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. L. Pruimboom, C. L. Raison, and F. A. J. Muskiet, “Physical activity protects the human brain against metabolic stress induced by a postprandial and chronic inflammation,” Behavioural Neurology, vol. 2015, Article ID 569869, 11 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus