The role of olfactory sensory neurons in improving working memory following aerobic exercise training in adult male rats

Document Type : Research Paper

Authors

1 Tarbiat Modares University, Tehran, Iran

2 Sport Sciences Research Institute of Iran

Abstract

Objectives: Nasal breathing has many health benefits, especially in exercise. Airflow through the nose stimulates the Olfactory Bulb (OB) during the breathing cycle, associated with the airflow intensity. This information reaches the OB and causes oscillations that transfer to other brain areas. Brain rhythms have been associated with different cognitive states and play functional roles in network computation, such as memory. Accordingly, this study investigates the effect of olfactory sensory neurons (OSNs) in improving working memory following aerobic exercise training in rats.
Methods and Materials: In this study, we used sixteen male Wistar rats (12-14 weeks, weighing 250-300 g). After implanting an electrode in the OB and HIP for Local field potentials recording, animals were divided into two exercises and two control groups. At the beginning of each week, one exercise group and one control group, to destroy the OSNs, received 300 mg/kg methimazole. After completing the exercise protocol (7 weeks/ 5 Days/week), we simultaneously recorded LFPs from rat Hip and OB during a Y-maze working memory task. Two-way variance analysis was used for statistical analysis.
Results: Our results showed that destroying olfactory sensory neurons significantly reduces the working memory capacity (P=0.04). On the other hand, the power of the delta and theta frequency bands increased and working memory improved in exercise groups (P=0.01).
Conclusions: We propose that the non-invasive stimulation of OSNs during nasal breathing may be a mechanism for improving working memory through exercise.

Keywords

Main Subjects


  1. Erickson KI, Hillman C, Stillman CM, Ballard RM, Bloodgood B, Conroy DE, et al. Physical activity, cognition, and brain outcomes: a review of the 2018 physical activity guidelines. Medicine and science in sports and exercise. 2019;51(6):1242.
  2. Bherer L, Erickson KI, Liu-Ambrose T. A review of the effects of physical activity and exercise on cognitive and brain functions in older adults. Journal of aging research. 2013;2013.
  3. Snigdha S, De Rivera C, Milgram NW, Cotman CW. Exercise enhances memory consolidation in the aging brain. Frontiers in aging neuroscience. 2014;6:3.
  4. Liu-Ambrose T, Eng JJ. Exercise training and recreational activities to promote executive functions in chronic stroke: a proof-of-concept study. Journal of Stroke and Cerebrovascular Diseases. 2015;24(1):130-7.
  5. Angevaren M, Aufdemkampe G, Verhaar HJ, Aleman A, Vanhees L. Physical activity and enhanced fitness to improve cognitive function in older people without known cognitive impairment. Cochrane database of systematic reviews. 2008(2).
  6. Hillman CH, Erickson KI, Kramer AF. Be smart, exercise your heart: exercise effects on brain and cognition. Nature reviews neuroscience. 2008;9(1):58-65.
  7. Buchman A, Boyle P, Yu L, Shah R, Wilson R, Bennett D. Total daily physical activity and the risk of AD and cognitive decline in older adults. Neurology. 2012;78(17):1323-9.
  8. Yolanda S, Pamungkas GC, Andraini T, Santoso DIS, Sidik SB, Widhowati LN. Effect of aerobic exercise on short-and long-term memory in adult male wistar rats. International Journal of Applied Pharmaceutics. 2020;12(Special Issue 3):15-8.
  9. Liu Y, Yan T, Chu JM-T, Chen Y, Dunnett S, Ho Y-S, et al. The beneficial effects of physical exercise in the brain and related pathophysiological mechanisms in neurodegenerative diseases. Laboratory Investigation. 2019;99(7):943-57.
  10. Romero B, Coburn JW, Brown LE, Galpin AJ. Metabolic Demands Of Heavy Metal Drumming. Medicine & Science in Sports & Exercise. 2015;47(5S):765-6.
  11. Nielsen H, Boesen M, Secher N. Near‐infrared spectroscopy determined brain and muscle oxygenation during exercise with normal and resistive breathing. Acta Physiologica Scandinavica. 2001;171(1):63-70.
  12. Bennett WD, Zeman KL, Jarabek AM. Nasal contribution to breathing with exercise: effect of race and gender. Journal of Applied Physiology. 2003;95(2):497-503.
  13. LaComb CO, Tandy RD, Lee SP, Young JC, Navalta JW. Oral versus nasal breathing during moderate to high intensity submaximal aerobic exercise. International Journal of Kinesiology & Sports Science. 2017;5(1).
  14. Allen R. The health benefits of nose breathing. 2017.
  15. Nguyen Chi V, Muller C, Wolfenstetter T, Yanovsky Y, Draguhn A, Tort AB, et al. Hippocampal Respiration-Driven Rhythm Distinct from Theta Oscillations in Awake Mice. J Neurosci. 2016;36(1):162-77.
  16. Buzsaki G, Moser EI. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci. 2013;16(2):130-8.
  17. Vanderwolf CH, Szechtman H. Electrophysiological correlates of stereotyped sniffing in rats injected with apomorphine. Pharmacol Biochem Behav. 1987;26(2):299-304.
  18. Franco K, Litaker D, Locala J, Bronson D. The cost of delirium in the surgical patient. Psychosomatics. 2001;42(1):68-73.
  19. Girard TD, Jackson JC, Pandharipande PP, Pun BT, Thompson JL, Shintani AK, et al. Delirium as a predictor of long-term cognitive impairment in survivors of critical illness. Critical care medicine. 2010;38(7):1513.
  20. Grosmaitre X, Santarelli LC, Tan J, Luo M, Ma M. Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nature neuroscience. 2007;10(3):348-54.
  21. Heck DH, Kozma R, Kay LM. The rhythm of memory: how breathing shapes memory function. Journal of Neurophysiology. 2019;122(2):563-71.
  22. Desai R, Tailor A, Bhatt T. Effects of yoga on brain waves and structural activation: A review. Complementary therapies in clinical practice. 2015;21(2):112-8.
  23. Ito J, Roy S, Liu Y, Cao Y, Fletcher M, Lu L, et al. Whisker barrel cortex delta oscillations and gamma power in the awake mouse are linked to respiration. Nature communications. 2014;5(1):3572.
  24. Yanovsky Y, Ciatipis M, Draguhn A, Tort AB, Brankačk J. Slow oscillations in the mouse hippocampus entrained by nasal respiration. Journal of Neuroscience. 2014;34(17):5949-64.
  25. Zelano C, Jiang H, Zhou G, Arora N, Schuele S, Rosenow J, et al. Nasal respiration entrains human limbic oscillations and modulates cognitive function. Journal of Neuroscience. 2016;36(49):12448-67.
  26. Hensch TKJNRN. Critical period plasticity in local cortical circuits. 2005;6(11):877.
  27. Paxinos G, Watson CR, Emson PC. AChE-stained horizontal sections of the rat brain in stereotaxic coordinates. Journal of neuroscience methods. 1980;3(2):129-49.
  28. Genter MB, Deamer NJ, Blake BL, Wesley DS, Levi PE. Olfactory toxicity of methimazole: dose-response and structure-activity studies and characterization of flavin-containing monooxygenase activity in the Long-Evans rat olfactory mucosa. Toxicologic pathology. 1995;23(4):477-86.
  29. Zeynali F, Raoufy MR, Gharakhanlou R. Olfactory Sensory Neurons Facilitate Aerobic Exercise-Induced Spatial Memory Improvement. Basic and Clinical Neuroscience.0-.
  30. Chae C-H, Jung S-L, An S-H, Jung C-K, Nam S-N, Kim H-T. Treadmill exercise suppresses muscle cell apoptosis by increasing nerve growth factor levels and stimulating p-phosphatidylinositol 3-kinase activation in the soleus of diabetic rats. Journal of physiology and biochemistry. 2011;67:235-41.
  31. Powers SK, Criswell D, Lawler J, Martin D, Lieu F-K, Ji LL, et al. Rigorous exercise training increases superoxide dismutase activity in ventricular myocardium. American Journal of Physiology-Heart and Circulatory Physiology. 1993;265(6):H2094-H8.
  32. Salimi M, Tabasi F, Nazari M, Ghazvineh S, Salimi A, Jamaati H, et al. The olfactory bulb modulates entorhinal cortex oscillations during spatial working memory. The Journal of Physiological Sciences. 2021;71:1-9.
  33. Ogawa T, Okihara H, Kokai S, Abe Y, Karin Harumi UK, Makiguchi M, et al. Nasal obstruction during adolescence induces memory/learning impairments associated with BDNF/TrkB signaling pathway hypofunction and high corticosterone levels. Journal of Neuroscience Research. 2018;96(6):1056-65.
  34. Wang X-Q, Wang G-W. Effects of treadmill exercise intensity on spatial working memory and long-term memory in rats. Life sciences. 2016;149:96-103.
  35. Uysal N, Kiray M, Sisman A, Camsari U, Gencoglu C, Baykara B, et al. Effects of voluntary and involuntary exercise on cognitive functions, and VEGF and BDNF levels in adolescent rats. Biotechnic & Histochemistry. 2015;90(1):55-68.
  36. Ghazvineh S, Salimi M, Nazari M, Garousi M, Tabasi F, Dehdar K, et al. Rhythmic air-puff into nasal cavity modulates activity across multiple brain areas: A non-invasive brain stimulation method to reduce ventilator-induced memory impairment. Respiratory Physiology & Neurobiology. 2021;287:103627.
  37. Li J-Y, Kuo TB, Hung C-T, Yang CC. Voluntary exercise enhances hippocampal theta rhythm and cognition in the rat. Behavioural Brain Research. 2021;399:112916.
  38. Li J-Y, Kuo TB, Yen J-C, Tsai S-C, Yang CC. Voluntary and involuntary running in the rat show different patterns of theta rhythm, physical activity, and heart rate. Journal of neurophysiology. 2014;111(10):2061-70.
  39. Li J-Y, Kuo TB, Yang CC. Aged rats show dominant modulation of lower frequency hippocampal theta rhythm during running. Experimental gerontology. 2016;83:63-70.
  40. Smith PJ, Blumenthal JA, Hoffman BM, Cooper H, Strauman TA, Welsh-Bohmer K, et al. Aerobic exercise and neurocognitive performance: a meta-analytic review of randomized controlled trials. Psychosomatic medicine. 2010;72(3):239.
  41. Colgin LL. Rhythms of the hippocampal network. Nature Reviews Neuroscience. 2016;17(4):239-49.