Oğuz YÜKSEL, Nazan UYSAL, Zeynep YÜCE, Başar KOÇ, Aslı KARAKILIÇ, Mehmet ATEŞ, Güven GÜVENDİ, Sevim KANDİŞ, Hikmet GÜMÜŞ, Servet KIZILDAĞ

Regular Aerobic Voluntary Exercise Increased Oxytocin in Female Mice: The Cause of Decreased Anxiety and Increased Empathy-Like Behaviors

Background: It is known that regular physical activity reduces anxiety. Low anxiety levels affect mood, emotions, and empathy. Oxytocin is a powerful hormone that regulates social interaction, sexual reproduction, maternal–infant bonding, milk release, empathy, and anxiety. Empathy is an important behavior in the living community; and also important for sportsmen during sportive competition and daily living life, because sportsmen are also role model of people.Aims: To investigate the effects of voluntary physical activity on oxytocin, anxiety, and empathy levels as well as the relationship between them.Study Design: Animal experiment.Methods: Male and female mice were made to exercise in running wheel cages for 6 weeks. Their empathy and anxiety levels were evaluated by using Helping Behavior test and elevated plus maze and open field test, respectively. And then the brain and blood oxytocin levels were measured.Results: Empathy-like behavior was improved in both genders of the exercise groups (door-opening time decreased in both genders of exercise groups, p for both=0.0001). As a response to exercise, both the brain and serum oxytocin levels increased in female mice (both of p=0.0001); however, in males, oxytocin levels increased in only the brain (p

PDF

___

Knöchel C, Oertel-Knöchel V, O’Dwyer L, Prvulovic D, Alves G, Kollmann B, et al. Cognitive and behavioural effects of physical exercise in psychiatric patients. Prog Neurobiol 2012;96:46-68.
Uysal N, Yuksel O, Kizildag S, Yuce Z, Gumus H, Karakilic A, et al. Regular aerobic exercise correlates with reduced anxiety and incresed levels of irisin in brain and white adipose tissue. Neurosci Lett 2018;676:92-7.
Uysal N, Tugyan K, Kayatekin BM, Acikgoz O, Bagriyanik HA, Gonenc S, et al. The effects of regular aerobic exercise in adolescent period on hippocampal neuron density, apoptosis and spatial memory. Neurosci Lett 2005;383:241-5.
Hubble K, Daughters K, Manstead ASR, Rees A, Thapar A, van Goozen SHM. Oxytocin increases attention to the eyes and selectively enhances self-reported affective empathy for fear. Neuropsychologia 2017;106:350-7.
Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M. Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat Rev Neurosci 2011;12:524-38.
Lukas M, Bredewold R, Neumann ID, Veenema AH. Maternal separation interferes with developmental changes in brain vasopressin and oxytocin receptor binding in male rats. Neuropharmacology 2010;58:78-87.
Jong TR, Menon R, Bludau A, Grund T, Biermeier V, Klampfl SM, et al. Salivary oxytocin concentrations in response to running, sexual self-stimulation, breastfeeding and the TSST: The Regensburg Oxytocin Challenge (ROC) study. Psychoneuroendocrinology 2015;62:381-8.
Bernstein EE, McNally RJ. Acute aerobic exercise helps overcome emotion regulation deficits. Cogn Emot 2017;31:834-43.
Harvey SB, Øverland S, Hatch SL, Wessely S, Mykletun A, Hotopf M. Exercise and the Prevention of Depression: Results of the HUNT Cohort Study. Am J Psychiatry 2018;175:28-36.
Paluska SA, Schwenk TL. Physical activity and mental health: current concepts. Sports Med 2000;29:167-80.
Shu J, Hassell S, Weber J, Ochsner KN, Mobbs D. The role of empathy in experiencing vicarious anxiety. J Exp Psychol Gen 2017;146:1164-88.
Adler A. Individual Psychology of Alfred Adler. New York, NY: Harper Perennial; 1964.
Gerdes KE, Segal E. Importance of empathy for social work practice: integrating new science. Soc Work 2011;56:141-8.
Sivaselvachandran S, Acland EL, Abdallah S, Martin LJ. Behavioral and mechanistic insight into rodent empathy. Neurosci Biobehav Rev 2018;91:130-7.
Meyza KZ, Bartal IB, Monfils MH, Panksepp JB, Knapska E. The roots of empathy: Through the lens of rodent models. Neurosci Biobehav Rev 2017;76:216-34.
Karakilic A, Kizildag S, Kandis S, Guvendi G, Koc B, Camsari GB, et al. The effects of acute foot shock stress on empathy levels in rats. Behav Brain Res 2018;349:31-6.
Erkuş A, Yakupoğlu S. A study developing empathy scale in the sports situations. Hacettepe J of Sports Sciences 2001;12:22-31. Uysal N, Kiray M, Sisman AR, Camsari UM, Gencoglu C, Baykara B, et al. Effects of voluntary and involuntary exercise on cognitive functions, and VEGF and BDNF levels in adolescent rats. Biotech Histochem 2015;90:55-68.
Goh J, Ladiges W. Voluntary Wheel Running in Mice. Curr Protoc Mouse Biol 2015;5:283-90.
Sato N, Tan L, Tate K, Okada M. Rats demonstrate helping behavior toward a soaked conspecific. Anim Cogn 2015;18:1039-47.
Casarrubea M, Roy V, Sorbera F, Magnusson MS, Santangelo A, Arabo A, et al. Temporal structure of the rat’s behavior in elevated plus maze test. Behav Brain Res 2013;237:290-9.
Aickin M, Gensler H. Adjusting for multiple testing when reporting research results: the Bonferroni vs Holm methods. Am J Public Health 1996;86:726-8.
Binder E, Droste SK, Ohl F, Reul JM. Regular voluntary exercise reduces anxiety-related behaviour and impulsiveness in mice. Behav Brain Res 2004;155:197-206.
Fuss J, Ben Abdallah NM, Vogt MA, Touma C, Pacifici PG, Palme R, et al. Voluntary exercise induces anxiety-like behavior in adult C57BL/6J mice correlating with hippocampal neurogenesis. Hippocampus 2010;20:364-76.
Kavussanu M, Boardley ID. The Prosocial and Antisocial Behavior in Sport Scale. J Sport Exerc Psychol 2009;31:97-117.
Balçikanli GS. Fair play in professional sports: Sportspersonship orientations of futsal players. FairPlay 2014;2:33-49.
Balcikanli GS, Yildiran I. Relationship between empathic skills of field hockey players and their prosocial behaviors. Gazi Beden Eğitimi ve Spor Bilimleri Derg 2018;23:1-8.
Shields DL, LaVoi NM, Bredemeier BL, Power FC. Predictors of poor sportspersonship in youth sports: personal attitudes and social influences. J Sport Exerc Psychol 2007;29:747-62.
Braga DC, Mori E, Higa KT, Morris M, Michelini LC. Central oxytocin modulates exercise-induced tachycardia. Am J Physiol Regul Integr Comp Physiol 2000;278:R1474-82.
Martins AS, Crescenzi A, Stern JE, Bordin S, Michelini LC. Hypertension and exercise training differentially affect oxytocin and oxytocin receptor expression in the brain. Hypertension 2005;46:1004-9.
Kim TK, Lee JE, Kim JE, Park JY, Choi J, Kim H, et al. G9a-Mediated Regulation of OXT and AVP Expression in the Basolateral Amygdala Mediates Stress-Induced Lasting Behavioral Depression and Its Reversal by Exercise. Mol Neurobiol 2016;53:2843-56.
Farina EV, Cappello F, Lipari L, Valentino A, Di Felice V, Valentino B. Presence of oxytocin, vasopressin and atrial natriuretic peptide and their modification in rat hypothalamic paraventricular nucleus during resistance training. Anat Histol Embryol 2014;43:159-63.
Bakos J, Hlavacova N, Makatsori A, Tybitanclova K, Zorad S, Hinghofer-Szalkay H, et al. Oxytocin levels in the posterior pituitary and in the heart are modified by voluntary wheel running. Regul Pept 2007;139:96-101.
Hew-Butler T, Noakes TD, Soldin SJ, Verbalis JG. Acute changes in endocrine and fluid balance markers during high-intensity, steady-state, and prolonged endurance running: unexpected increases in oxytocin and brain natriuretic peptide during exercise. Eur J Endocrinol 2008;159:729-37.