Volume 6, Issue 3, May 2018, Page: 56-66
Physical Activity and Neural Correlates of Sad Facial Expressions in Premenstrual Syndrome
Ren-Jen Hwang, Department of Nursing, Chang Gung University of Science and Technology, Taoyuan, Taiwan; Department of Nursing, Chang Gung Memorial Hospital, Taoyuan, Taiwan
Hsin-Ju Chen, Department of Nursing, Chang Gung University of Science and Technology, Taoyuan, Taiwan
Zhan-Xian Guo, Department of Nursing, Chang Gung University of Science and Technology, Taoyuan, Taiwan
Yu-Sheun Lee, Department of Nursing, Chang Gung University of Science and Technology, Taoyuan, Taiwan; Department of Nursing, China Medical University Hospital, Taichung, Taiwan
Yueh-O Chuang, Department of Nursing, Chang Gung Memorial Hospital, Taoyuan, Taiwan
Received: May 1, 2018;       Accepted: Jun. 4, 2018;       Published: Jun. 28, 2018
DOI: 10.11648/j.jgo.20180603.14      View  1433      Downloads  132
Exercise benefits our emotional function, particularly frontal lobe-mediated cognitive processes. Recent studies have indicated that affective neural circuits are modulated by premenstrual syndrome (PMS). Meanwhile, observational studies have reported that physical activity can promote PMS remission. Nonetheless, few studies have investigated the effect of physical activity on sad emotion recognition from a neurobiological perspective. Our objective was to explore the relationships between exercise and high order sad emotion cognitive processing in women with PMS. We conducted a sad facial emotion recognition task to examine the effects of aerobic exercise on activity in central frontal regions with electroencephalography in 31 participants. Participants were divided into a high (HPMS) or low severity PMS (LPMS) group according to self-reported PMS scores. We then analyzed cortical activity in response to sad cues, comparing such activity between the groups. Repeated ANOVA and pooled t statistics were used for statistical analysis. We observed a significant reduction in the N250 wave evoked by sad emotions after exercise compared with baseline at most channels in HPMS (P < 0.05), but not in LPMS. There was also a significant post-exercise prolongation of N250 latency at F3 and C3 in HPMS. There were no differences in N250 activation between the groups at baseline but significantly lower activation was noted in the lateral prefrontal cortex (PFC: F7 and F8) of HPMS compared with LPMS after exercise. Furthermore, higher PMS scores were significantly associated with greater PFC-N250 amplitude before exercise, but this was not observed after exercise. Acute exercise induced significant brain activity changes in response to sad cues in the HPMS group only. Furthermore, significantly lower activation of the lateral PFC was found after exercise in HPMS compared with LPMS. Given our results, we discuss the potential efficacy of exercise to modulate emotional context or sad emotion regulatory capabilities in women with PMS.
Exercise, Premenstrual Syndrome, Brain, Sad Emotion, Electroencephalography
To cite this article
Ren-Jen Hwang, Hsin-Ju Chen, Zhan-Xian Guo, Yu-Sheun Lee, Yueh-O Chuang, Physical Activity and Neural Correlates of Sad Facial Expressions in Premenstrual Syndrome, Journal of Gynecology and Obstetrics. Vol. 6, No. 3, 2018, pp. 56-66. doi: 10.11648/j.jgo.20180603.14
Copyright © 2018 Authors retain the copyright of this article.
This article is an open access article distributed under the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Dimmock PW, Wyatt KM, Jones PW, O'Brien PM: Efficacy of selective serotonin-reuptake inhibitors in premenstrual syndrome: a systematic review. Lancet 2000, 356 (9236): 1131-1136.
A DM, K S, A D, Sattar K: Epidemiology of Premenstrual Syndrome (PMS)-A Systematic Review and Meta-Analysis Study. Journal of clinical and diagnostic research: JCDR 2014, 8 (2): 106-109.
Freeman EW, Rickels K, Schweizer E, Ting T: Relationships between age and symptom severity among women seeking medical treatment for premenstrual symptoms. Psychol Med 1995, 25 (2): 309-315.
Roca CA, Schmidt PJ, Altemus M, Deuster P, Danaceau MA, Putnam K, Rubinow DR: Differential menstrual cycle regulation of hypothalamic-pituitary-adrenal axis in women with premenstrual syndrome and controls. J Clin Endocrinol Metab 2003, 88 (7): 3057-3063.
Duenas JL, Lete I, Bermejo R, Arbat A, Perez-Campos E, Martinez-Salmean J, Serrano I, Doval JL, Coll C: Prevalence of premenstrual syndrome and premenstrual dysphoric disorder in a representative cohort of Spanish women of fertile age. European journal of obstetrics, gynecology, and reproductive biology 2011, 156 (1): 72-77.
Shah NR, Jones JB, Aperi J, Shemtov R, Karne A, Borenstein J: Selective serotonin reuptake inhibitors for premenstrual syndrome and premenstrual dysphoric disorder: a meta-analysis. Obstetrics and gynecology 2008, 111 (5): 1175-1182.
Liao H, Pang Y, Liu P, Liu H, Duan G, Liu Y, Tang L, Tao J, Wen D, Li S et al: Abnormal Spontaneous Brain Activity in Women with Premenstrual Syndrome Revealed by Regional Homogeneity. Frontiers in human neuroscience 2017, 11: 62.
Liu Q, Li R, Zhou R, Li J, Gu Q: Abnormal Resting-State Connectivity at Functional MRI in Women with Premenstrual Syndrome. PloS one 2015, 10 (9): e0136029.
Ochsner KN, Gross JJ: The cognitive control of emotion. Trends in cognitive sciences 2005, 9 (5): 242-249.
Miller EK, Cohen JD: An integrative theory of prefrontal cortex function. Annual review of neuroscience 2001, 24: 167-202.
Heijnen S, Hommel B, Kibele A, Colzato LS: Neuromodulation of Aerobic Exercise-A Review. Frontiers in psychology 2015, 6: 1890.
Kelly ME, Loughrey D, Lawlor BA, Robertson IH, Walsh C, Brennan S: The impact of exercise on the cognitive functioning of healthy older adults: a systematic review and meta-analysis. Ageing Res Rev 2014, 16: 12-31.
Wogensen E, Mala H, Mogensen J: The Effects of Exercise on Cognitive Recovery after Acquired Brain Injury in Animal Models: A Systematic Review. Neural plasticity 2015, 2015: 830871.
Hillman CH, Kamijo K, Scudder M: A review of chronic and acute physical activity participation on neuroelectric measures of brain health and cognition during childhood. Preventive medicine 2011, 52 Suppl 1: S21-28.
Hillman CH, Snook EM, Jerome GJ: Acute cardiovascular exercise and executive control function. International journal of psychophysiology: official journal of the International Organization of Psychophysiology 2003, 48 (3): 307-314.
Mata J, Hogan CL, Joormann J, Waugh CE, Gotlib IH: Acute exercise attenuates negative affect following repeated sad mood inductions in persons who have recovered from depression. J Abnorm Psychol 2013, 122 (1): 45-50.
Thayer RE, Newman JR, McClain TM: Self-regulation of mood: strategies for changing a bad mood, raising energy, and reducing tension. Journal of personality and social psychology 1994, 67 (5): 910-925.
Daley A: Exercise and premenstrual symptomatology: a comprehensive review. Journal of women's health 2009, 18 (6): 895-899.
Levesque J, Eugene F, Joanette Y, Paquette V, Mensour B, Beaudoin G, Leroux JM, Bourgouin P, Beauregard M: Neural circuitry underlying voluntary suppression of sadness. Biological psychiatry 2003, 53 (6): 502-510.
Galdo Alvarez S, Lindin Novo M, Diaz Fernandez F: Naming faces: a multidisciplinary and integrated review. Psicothema 2009, 21 (4): 521-527.
Chammat M, Foucher A, Nadel J, Dubal S: Reading sadness beyond human faces. Brain research 2010, 1348: 95-104.
Dennis TA, Chen CC: Emotional face processing and attention performance in three domains: neurophysiological mechanisms and moderating effects of trait anxiety. International journal of psychophysiology: official journal of the International Organization of Psychophysiology 2007, 65 (1): 10-19.
Nasr S, Esteky H: A study of N250 event-related brain potential during face and non-face detection tasks. Journal of vision 2009, 9 (5): 5, 1-14.
Wijers AA, Van Besouw NJ, Mulder G: Selective attention to a facial feature with and without facial context: an ERP-study. International journal of psychophysiology: official journal of the International Organization of Psychophysiology 2002, 44 (1): 13-35.
Streit M, Wolwer W, Brinkmeyer J, Ihl R, Gaebel W: EEG-correlates of facial affect recognition and categorisation of blurred faces in schizophrenic patients and healthy volunteers. Schizophrenia research 2001, 49 (1-2): 145-155.
Wynn JK, Lee J, Horan WP, Green MF: Using event related potentials to explore stages of facial affect recognition deficits in schizophrenia. Schizophrenia bulletin 2008, 34 (4): 679-687.
Streit M, Wolwer W, Brinkmeyer J, Ihl R, Gaebel W: Electrophysiological correlates of emotional and structural face processing in humans. Neurosci Lett 2000, 278 (1-2): 13-16.
Luo W, Feng W, He W, Wang NY, Luo YJ: Three stages of facial expression processing: ERP study with rapid serial visual presentation. NeuroImage 2010, 49 (2): 1857-1867.
Balconi M, Pozzoli U: Event-related oscillations (ERO) and event-related potentials (ERP) in emotional face recognition. The International journal of neuroscience 2008, 118 (10): 1412-1424.
Carretie L, Martin-Loeches M, Hinojosa JA, Mercado F: Emotion and attention interaction studied through event-related potentials. Journal of cognitive neuroscience 2001, 13 (8): 1109-1128.
Streit M, Ioannides AA, Liu L, Wolwer W, Dammers J, Gross J, Gaebel W, Muller-Gartner HW: Neurophysiological correlates of the recognition of facial expressions of emotion as revealed by magnetoencephalography. Brain research Cognitive brain research 1999, 7 (4): 481-491.
Wolwer W, Brinkmeyer J, Stroth S, Streit M, Bechdolf A, Ruhrmann S, Wagner M, Gaebel W: Neurophysiological correlates of impaired facial affect recognition in individuals at risk for schizophrenia. Schizophrenia bulletin 2012, 38 (5): 1021-1029.
Raichlen DA, Alexander GE: Adaptive Capacity: An Evolutionary Neuroscience Model Linking Exercise, Cognition, and Brain Health. Trends in neurosciences 2017, 40 (7): 408-421.
Matta Mello Portugal E, Cevada T, Sobral Monteiro-Junior R, Teixeira Guimaraes T, da Cruz Rubini E, Lattari E, Blois C, Camaz Deslandes A: Neuroscience of exercise: from neurobiology mechanisms to mental health. Neuropsychobiology 2013, 68 (1): 1-14.
Breiter HC, Etcoff NL, Whalen PJ, Kennedy WA, Rauch SL, Buckner RL, Strauss MM, Hyman SE, Rosen BR: Response and habituation of the human amygdala during visual processing of facial expression. Neuron 1996, 17 (5): 875-887.
Steiner M, Macdougall M, Brown E: The premenstrual symptoms screening tool (PSST) for clinicians. Archives of women's mental health 2003, 6 (3): 203-209.
Kerestes R, Labuschagne I, Croft RJ, O'Neill BV, Bhagwagar Z, Phan KL, Nathan PJ: Evidence for modulation of facial emotional processing bias during emotional expression decoding by serotonergic and noradrenergic antidepressants: an event-related potential (ERP) study. Psychopharmacology 2009, 202 (4): 621-634.
Liu T, Pinheiro A, Zhao Z, Nestor PG, McCarley RW, Niznikiewicz MA: Emotional cues during simultaneous face and voice processing: electrophysiological insights. PloS one 2012, 7 (2): e31001.
Fox KR: The influence of physical activity on mental well-being. Public Health Nutr 1999, 2 (3A): 411-418.
Kramer AF, Erickson KI: Capitalizing on cortical plasticity: influence of physical activity on cognition and brain function. Trends in cognitive sciences 2007, 11 (8): 342-348.
Bernstein EE, McNally RJ: Acute aerobic exercise helps overcome emotion regulation deficits. Cognition & emotion 2017, 31 (4): 834-843.
Crabbe JB, Smith JC, Dishman RK: Emotional & electroencephalographic responses during affective picture viewing after exercise. Physiology & behavior 2007, 90 (2-3): 394-404.
Korzekwa MI, Steiner M: Premenstrual syndromes. Clinical obstetrics and gynecology 1997, 40 (3): 564-576.
Kraemer GR, Kraemer RR: Premenstrual syndrome: diagnosis and treatment experiences. J Womens Health 1998, 7 (7): 893-907.
Roy EJ, Wilson MA, Kelley DB: Estrogen-induced progestin receptors in the brain and pituitary of the South African clawed frog, Xenopus laevis. Neuroendocrinology 1986, 42 (1): 51-56.
Huppertz C, Bartels M, Groen-Blokhuis MM, Dolan CV, de Moor MH, Abdellaoui A, van Beijsterveldt CE, Ehli EA, Hottenga JJ, Willemsen G et al: The dopaminergic reward system and leisure time exercise behavior: a candidate allele study. BioMed research international 2014, 2014: 591717.
Tsuchiya N, Iwase M, Izumizaki M, Homma I: Dopaminergic modulation of exercise hyperpnoea via D (2) receptors in mice. Experimental physiology 2012, 97 (2): 228-238.
Baj G, D'Alessandro V, Musazzi L, Mallei A, Sartori CR, Sciancalepore M, Tardito D, Langone F, Popoli M, Tongiorgi E: Physical exercise and antidepressants enhance BDNF targeting in hippocampal CA3 dendrites: further evidence of a spatial code for BDNF splice variants. Neuropsychopharmacology 2012, 37 (7): 1600-1611.
Ma Q: Beneficial effects of moderate voluntary physical exercise and its biological mechanisms on brain health. Neuroscience bulletin 2008, 24 (4): 265-270.
Moon HY, Kim SH, Yang YR, Song P, Yu HS, Park HG, Hwang O, Lee-Kwon W, Seo JK, Hwang D et al: Macrophage migration inhibitory factor mediates the antidepressant actions of voluntary exercise. Proceedings of the National Academy of Sciences of the United States of America 2012, 109 (32): 13094-13099.
Wu G, Feder A, Cohen H, Kim JJ, Calderon S, Charney DS, Mathe AA: Understanding resilience. Frontiers in behavioral neuroscience 2013, 7: 10.
Baratta MV, Rozeske RR, Maier SF: Understanding stress resilience. Frontiers in behavioral neuroscience 2013, 7: 158.
Gross JJT, R. A.: Emotion regulation: Conceptual foundations. In JJ Gross (Ed), Handbook of emotion regulation (pp 3-26) New York: The Guilford Press 2007.
Lane AM, Beedie CJ, Jones MV, Uphill M, Devonport TJ: The BASES expert statement on emotion regulation in sport. Journal of sports sciences 2012, 30 (11): 1189-1195.
Dietrich A: Transient hypofrontality as a mechanism for the psychological effects of exercise. Psychiatry Res 2006, 145 (1): 79-83.
Lee YY, Hsieh S: Classifying different emotional states by means of EEG-based functional connectivity patterns. PloS one 2014, 9 (4): e95415.
Kalisch R, Wiech K, Herrmann K, Dolan RJ: Neural correlates of self-distraction from anxiety and a process model of cognitive emotion regulation. Journal of cognitive neuroscience 2006, 18 (8): 1266-1276.
Berkman ET, Lieberman MD: Approaching the bad and avoiding the good: lateral prefrontal cortical asymmetry distinguishes between action and valence. Journal of cognitive neuroscience 2010, 22 (9): 1970-1979.
Barnes RT, Coombes SA, Armstrong NB, Higgins TJ, Janelle CM: Evaluating attentional and affective changes following an acute exercise bout using a modified dot-probe protocol. Journal of sports sciences 2010, 28 (10): 1065-1076.
Dixon ML: Cognitive control, emotional value, and the lateral prefrontal cortex. Frontiers in psychology 2015, 6: 758.
Kouneiher F, Charron S, Koechlin E: Motivation and cognitive control in the human prefrontal cortex. Nature neuroscience 2009, 12 (7): 939-945.
Morawetz C, Bode S, Baudewig J, Heekeren HR: Effective amygdala-prefrontal connectivity predicts individual differences in successful emotion regulation. Social cognitive and affective neuroscience 2017, 12 (4): 569-585.
Ochsner KN, Bunge SA, Gross JJ, Gabrieli JD: Rethinking feelings: an FMRI study of the cognitive regulation of emotion. Journal of cognitive neuroscience 2002, 14 (8): 1215-1229.
Baxter LR: Brain imaging as a tool in establishing a theory of brain pathology in obsessive compulsive disorder. The Journal of clinical psychiatry 1990, 51 Suppl: 22-25; discussion 26.
LeDoux J, 1996. The Emotional Brain. Touchstone, New York.
Mayberg HS: Limbic-cortical dysregulation: a proposed model of depression. The Journal of neuropsychiatry and clinical neurosciences 1997, 9 (3): 471-481.
Dishman RK: Brain monoamines, exercise, and behavioral stress: animal models. Medicine and science in sports and exercise 1997, 29 (1): 63-74.
Salmon P: Effects of physical exercise on anxiety, depression, and sensitivity to stress: a unifying theory. Clinical psychology review 2001, 21 (1): 33-61.
Browse journals by subject