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Sex-Related Differences in Emotion Recognition in Multi-concussed Athletes

Published online by Cambridge University Press:  15 December 2016

Edith Léveillé ,
Samuel Guay ,
Caroline Blais ,
Peter Scherzer  and
Louis De Beaumont
Edith Léveillé
Affiliation:
Département de psychologie, Université du Québec à Montréal, Montréal, Québec, Canada Hôpital du Sacré-Cœur de Montréal, Montréal, Québec, Canada
Samuel Guay
Affiliation:
Département de psychologie, Université du Québec à Trois-Rivières, Trois-Rivières, Québec, Canada
Caroline Blais
Affiliation:
Département de psychoéducation et de psychologie, Université du Québec en Outaouais, Gatineau, Québec, Canada
Peter Scherzer
Affiliation:
Département de psychologie, Université du Québec à Montréal, Montréal, Québec, Canada
Louis De Beaumont*
Affiliation:
Hôpital du Sacré-Cœur de Montréal, Montréal, Québec, Canada Département de psychologie, Université du Québec à Trois-Rivières, Trois-Rivières, Québec, Canada
*
Correspondence and reprint requests to: Louis De Beaumont, Département de Psychologie, Université du Québec à Trois-Rivières, C.P. 5000, Trois-Rivières (Québec) Canada, G9A 5H7. E-mail: [email protected]
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Abstract

Objectives: Concussion is defined as a complex pathophysiological process affecting the brain. Although the cumulative and long-term effects of multiple concussions are now well documented on cognitive and motor function, little is known about their effects on emotion recognition. Recent studies have suggested that concussion can result in emotional sequelae, particularly in females and multi-concussed athletes. The objective of this study was to investigate sex-related differences in emotion recognition in asymptomatic male and female multi-concussed athletes. Methods: We tested 28 control athletes (15 males) and 22 multi-concussed athletes (10 males) more than a year since the last concussion. Participants completed the Post-Concussion Symptom Scale, the Beck Depression Inventory-II, the Beck Anxiety Inventory, a neuropsychological test battery and a morphed emotion recognition task. Pictures of a male face expressing basic emotions (anger, disgust, fear, happiness, sadness, surprise) morphed with another emotion were randomly presented. After each face presentation, participants were asked to indicate the emotion expressed by the face. Results: Results revealed significant sex by group interactions in accuracy and intensity threshold for negative emotions, together with significant main effects of emotion and group. Conclusions: Male concussed athletes were significantly impaired in recognizing negative emotions and needed more emotional intensity to correctly identify these emotions, compared to same-sex controls. In contrast, female concussed athletes performed similarly to same-sex controls. These findings suggest that sex significantly modulates concussion effects on emotional facial expression recognition. (JINS, 2017, 23, 65–77)

Keywords

SportConcussionEmotional facial expressionGender differencesAnxietyDepression
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 23 , Issue 1 , January 2017 , pp. 65 - 77
Copyright
Copyright © The International Neuropsychological Society 2016 

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References

REFERENCES

Adolphs, R. (1999a). The human amygdala and emotion. The Neuroscientist, 5(2), 125–137. doi: 10.1177/107385849900500216 CrossRefGoogle Scholar
Adolphs, R. (1999b). Social cognition and the human brain. Trends in Cognitive Sciences, 3(12), 469–479.Google Scholar
Adolphs, R. (2001). The neurobiology of social cognition. Current Opinion in Neurobiology, 11(2), 231–239.Google Scholar
Adolphs, R. (2002a). Neural systems for recognizing emotion. Current Opinion in Neurobiology, 12(2), 169–177.Google Scholar
Adolphs, R. (2002b). Recognizing emotion from facial expressions: Psychological and neurological mechanisms. Behavioral and Cognitive Neuroscience Reviews, 1(1), 21–62.Google Scholar
Adolphs, R. (2003). Cognitive neuroscience of human social behaviour. Nature Reviews Neuroscience, 4(3), 165–178. doi: 10.1038/nrn1056 CrossRefGoogle ScholarPubMed
Adolphs, R., Baron-Cohen, S., & Tranel, D. (2002). Impaired recognition of social emotions following amygdala damage. Journal of Cognitive Neuroscience, 14(8), 1264–1274.Google Scholar
Adolphs, R., Damasio, H., Tranel, D., Cooper, G., & Damasio, A.R. (2000). A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. The Journal of Neuroscience, 20(7), 2683–2690.Google Scholar
Adolphs, R., Damasio, H., Tranel, D., & Damasio, A.R. (1996). Cortical systems for the recognition of emotion in facial expressions. The Journal of Neuroscience, 16(23), 7678–7687.CrossRefGoogle ScholarPubMed
Adolphs, R., & Tranel, D. (2004). Impaired judgments of sadness but not happiness following bilateral amygdala damage. Journal of Cognitive Neuroscience, 16(3), 453–462.Google Scholar
Adolphs, R., Tranel, D., Damasio, H., & Damasio, A.R. (1994). Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature, 372(6507), 669–672.CrossRefGoogle Scholar
Adolphs, R., Tranel, D., Hamann, S., Young, A.W., Calder, A.J., Phelps, E.A., & Damasio, A.R. (1999). Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia, 37(10), 1111–1117.Google Scholar
Baker, J.G., Leddy, J.J., Darling, S.R., Shucard, J., Makdissi, M., & Willer, B.S. (2016). Gender differences in recovery from sports-related concussion in adolescents. Clinical Pediatrics, 55(8), 771–775.Google Scholar
Beck, A.T., & Steer, R.A. (1993). Beck Anxiety Inventory manual. San Antonio, TX: PsychCorp/Pearson.Google Scholar
Beck, A.T., Steer, R.A., & Brown, G.K. (1996). Beck Depression Inventory-II. San Antonio, TX: PsychCorp/Pearson.Google Scholar
Bigler, E.D. (2001a). The lesion (s) in traumatic brain injury: Implications for clinical neuropsychology. Archives of Clinical Neuropsychology, 16(2), 95–131.Google Scholar
Bigler, E.D. (2001b). Quantitative magnetic resonance imaging in traumatic brain injury. The Journal of Head Trauma Rehabilitation, 16(2), 117–134.Google Scholar
Bigler, E.D. (2007). Anterior and middle cranial fossa in traumatic brain injury: Relevant neuroanatomy and neuropathology in the study of neuropsychological outcome. Neuropsychology, 21(5), 515–531.Google Scholar
Bigler, E.D., Johnson, S.C., Anderson, C.V., Blatter, D.D., Gale, S.D., Russo, A.A., & Hopkins, R.O. (1996). Traumatic brain injury and memory: The role of hippocampal atrophy. Neuropsychology, 10(3), 333–342.Google Scholar
Bishop, S.J., Aguirre, G.K., Nunez-Elizalde, A.O., & Toker, D. (2015). Seeing the world through non rose-colored glasses: Anxiety and the amygdala response to blended expressions. Frontiers in Human Neuroscience, 9, 152.Google Scholar
Broglio, S.P., Eckner, J.T., Paulson, H.L., & Kutcher, J.S. (2012). Cognitive decline and aging: The role of concussive and subconcussive impacts. Exercise and Sport Sciences Reviews, 40(3), 138–144.Google Scholar
Broshek, D.K., Kaushik, T., Freeman, J.R., Erlanger, D., Webbe, F., & Barth, J.T. (2005). Sex differences in outcome following sports-related concussion. Journal of Neurosurgery, 102(5), 856–863.Google Scholar
Brown, D.A., Elsass, J.A., Miller, A.J., Reed, L.E., & Reneker, J.C. (2015). Differences in symptom reporting between males and females at baseline and after a sports-related concussion: A systematic review and meta-analysis. Sports Medicine, 45(7), 1027–1040.CrossRefGoogle ScholarPubMed
Bryant, R.A., O’Donnell, M.L., Creamer, M., McFarlane, A.C., Clark, C.R., & Silove, D. (2010). The psychiatric sequelae of traumatic injury. American Journal of Psychiatry, 167(3), 312–320.Google Scholar
Callahan, B.L., Ueda, K., Sakata, D., Plamondon, A., & Murai, T. (2011). Liberal bias mediates emotion recognition deficits in frontal traumatic brain injury. Brain and Cognition, 77(3), 412–418. doi: 10.1016/j.bandc.2011.08.017 Google Scholar
Campbell, R., Elgar, K., Kuntsi, J., Akers, R., Terstegge, J., Coleman, M., & Skuse, D. (2002). The classification of ‘fear’ from faces is associated with face recognition skill in women. Neuropsychologia, 40(6), 575–584.Google Scholar
Chamard, E., Lassonde, M., Henry, L., Tremblay, J., Boulanger, Y., De Beaumont, L., & Theoret, H. (2013). Neurometabolic and microstructural alterations following a sports-related concussion in female athletes. Brain Injury, 27(9), 1038–1046. doi: 10.3109/02699052.2013.794968 Google Scholar
Chappell, M.H., Ulug, A.M., Zhang, L., Heitger, M.H., Jordan, B.D., Zimmerman, R.D., & Watts, R. (2006). Distribution of microstructural damage in the brains of professional boxers: A diffusion MRI study. Journal of Magnetic Resonance Imaging, 24(3), 537–542. doi: 10.1002/jmri.20656 Google Scholar
Chayer, C., & Freedman, M. (2001). Frontal lobe functions. Current Neurology and Neuroscience Reports, 1(6), 547–552.Google Scholar
Collins, M.W., Lovell, M.R., Iverson, G.L., Cantu, R.C., Maroon, J.C., & Field, M. (2002). Cumulative effects of concussion in high school athletes. Neurosurgery, 51(5), 1175–1181.Google Scholar
Colvin, A.C., Mullen, J., Lovell, M.R., West, R.V., Collins, M.W., & Groh, M. (2009). The role of concussion history and gender in recovery from soccer-related concussion. The American Journal of Sports Medicine, 37(9), 1699–1704.Google Scholar
Covassin, T., Elbin, R., Bleecker, A., Lipchik, A., & Kontos, A.P. (2013). Are there differences in neurocognitive function and symptoms between male and female soccer players after concussions? The American Journal of Sports Medicine, 41(12), 2890–2895.Google Scholar
Covassin, T., Swanik, C.B., Sachs, M., Kendrick, Z., Schatz, P., Zillmer, E., & Kaminaris, C. (2006). Sex differences in baseline neuropsychological function and concussion symptoms of collegiate athletes. British Journal of Sports Medicine, 40(11), 923–927.Google Scholar
Covassin, T., Swanik, C.B., & Sachs, M.L. (2003). Sex differences and the incidence of concussions among collegiate athletes. Journal of Athletic Training, 38(3), 238–244.Google Scholar
Croker, V., & McDonald, S. (2005). Recognition of emotion from facial expression following traumatic brain injury. Brain Injury, 19(10), 787–799. doi: 10.1080/02699050500110033 CrossRefGoogle ScholarPubMed
De Beaumont, L., Beauchemin, M., Beaulieu, C., & Jolicoeur, P. (2013). Long-term attenuated electrophysiological response to errors following multiple sports concussions. Journal of Clinical and Experimental Neuropsychology, 35(6), 596–607. doi: 10.1080/13803395.2013.800023 Google Scholar
De Beaumont, L., Brisson, B., Lassonde, M., & Jolicoeur, P. (2007). Long-term electrophysiological changes in athletes with a history of multiple concussions. Brain Injury, 21(6), 631–644. doi: 10.1080/02699050701426931 Google Scholar
De Beaumont, L., Henry, L.C., & Gosselin, N. (2012). Long-term functional alterations in sports concussion. Neurosurgical Focus, 33(6), E8: 1–7. doi: 10.3171/2012.9.FOCUS12278 Google Scholar
De Beaumont, L., Lassonde, M., Leclerc, S., & Theoret, H. (2007). Long-term and cumulative effects of sports concussion on motor cortex inhibition. Neurosurgery, 61(2), 329–336; discussion 336–337. doi: 10.1227/01.NEU.0000280000.03578.B6 Google Scholar
De Beaumont, L., Mongeon, D., Tremblay, S., Messier, J., Prince, F., Leclerc, S., & Théoret, H. (2011). Persistent motor system abnormalities in formerly concussed athletes. Journal of Athletic Training, 46(3), 234–240.Google Scholar
De Beaumont, L., Theoret, H., Mongeon, D., Messier, J., Leclerc, S., Tremblay, S., & Lassonde, M. (2009). Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood. Brain, 132(3), 695–708. doi: 10.1093/brain/awn347 Google Scholar
Deb, S., Lyons, I., & Koutzoukis, C. (1999). Neurobehavioural symptoms one year after a head injury. The British Journal of Psychiatry, 174(4), 360–365.CrossRefGoogle ScholarPubMed
Deb, S., Lyons, I., Koutzoukis, C., Ali, I., & McCarthy, G. (1999). Rate of psychiatric illness 1 year after traumatic brain injury. American Journal of Psychiatry, 156(3), 374–378.CrossRefGoogle ScholarPubMed
Decq, P., Gault, N., Blandeau, M., Kerdraon, T., Berkal, M., ElHelou, A., & Peyrin, J.-C. (2016). Long-term consequences of recurrent sports concussion. Acta Neurochirurgica, 158(2), 289–300.Google Scholar
Derntl, B., Kryspin-Exner, I., Fernbach, E., Moser, E., & Habel, U. (2008). Emotion recognition accuracy in healthy young females is associated with cycle phase. Hormones and Behavior, 53(1), 90–95.Google Scholar
Derntl, B., Windischberger, C., Robinson, S., Lamplmayr, E., Kryspin-Exner, I., Gur, R.C., & Habel, U. (2008). Facial emotion recognition and amygdala activation are associated with menstrual cycle phase. Psychoneuroendocrinology, 33(8), 1031–1040.CrossRefGoogle ScholarPubMed
Deschênes, A., Forget, H., Daudelin-Peltier, C., Fiset, D., & Blais, C. (2015). Facial expression recognition impairment following acute social stress. Journal of Vision, 15(12), 1383–1383.CrossRefGoogle Scholar
Dick, R. (2009). Is there a gender difference in concussion incidence and outcomes? British Journal of Sports Medicine, 43(Suppl 1), i46–i50.Google Scholar
Didehbani, N., Cullum, C.M., Mansinghani, S., Conover, H., & Hart, J. (2013). Depressive symptoms and concussions in aging retired NFL players. Archives of Clinical Neuropsychology, 28(5), 418–424.Google Scholar
Dupuis, F., Johnston, K.M., Lavoie, M., Lepore, F., & Lassonde, M. (2000). Concussions in athletes produce brain dysfunction as revealed by event‐related potentials. Neuroreport, 11(18), 4087–4092.Google Scholar
Echemendia, R.J., & Julian, L.J. (2001). Mild traumatic brain injury in sports: Neuropsychology’s contribution to a developing field. Neuropsychology Review, 11(2), 69–88.Google Scholar
Echemendia, R.J., Putukian, M., Mackin, R.S., Julian, L., & Shoss, N. (2001). Neuropsychological test performance prior to and following sports-related mild traumatic brain injury. Clinical Journal of Sport Medicine, 11(1), 23–31.Google Scholar
Ellis, M.J., Ritchie, L.J., Koltek, M., Hosain, S., Cordingley, D., Chu, S., & Russell, K. (2015). Psychiatric outcomes after pediatric sports-related concussion. Journal of Neurosurgery: Pediatrics, 16(6), 709–718.Google Scholar
Farace, E., & Alves, W.M. (2000). Do women fare worse: A metaanalysis of gender differences in traumatic brain injury outcome. Journal of Neurosurgery, 93(4), 539–545.CrossRefGoogle ScholarPubMed
Fenton, G., McClelland, R., Montgomery, A., MacFlynn, G., & Rutherford, W. (1993). The postconcussional syndrome: Social antecedents and psychological sequelae. The British Journal of Psychiatry, 162(4), 493–497.Google Scholar
Fleminger, S. (2008). Long-term psychiatric disorders after traumatic brain injury. European Journal of Anaesthesiology, 25(S42), 123–130.Google Scholar
Gaetz, M., Goodman, D., & Weinberg, H. (2000). Electrophysiological evidence for the cumulative effects of concussion. Brain Injury, 14(12), 1077–1088.Google Scholar
Gale, S., Burr, R., Bigler, E.D., & Blatter, D. (1993). Fornix degeneration and memory in traumatic brain injury. Brain Research Bulletin, 32(4), 345–349.Google Scholar
Gessel, L.M., Collins, C.L., & Dick, R.W. (2007). Concussions among United States high school and collegiate athletes. Journal of Athletic Training, 42(4), 495–503.Google Scholar
Green, R., Turner, G.R., & Thompson, W.F. (2004). Deficits in facial emotion perception in adults with recent traumatic brain injury. Neuropsychologia, 42(2), 133–141. doi: 10.1016/j.neuropsychologia.2003.07.005 Google Scholar
Guapo, V.G., Graeff, F.G., Zani, A.C.T., Labate, C.M., dos Reis, R.M., & Del-Ben, C.M. (2009). Effects of sex hormonal levels and phases of the menstrual cycle in the processing of emotional faces. Psychoneuroendocrinology, 34(7), 1087–1094.Google Scholar
Guskiewicz, K.M., Marshall, S.W., Bailes, J., McCrea, M., Cantu, R.C., Randolph, C., & Jordan, B.D. (2005). Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery, 57(4), 719–726. doi: 10.1227/01.neu.0000175725.75780.dd Google Scholar
Guskiewicz, K.M., Marshall, S.W., Bailes, J., McCrea, M., Harding, H.P., Matthews, A., & Cantu, R.C. (2007). Recurrent concussion and risk of depression in retired professional football players. Medicine & Science in Sports & Exercise, 39(6), 903–909.Google Scholar
Guskiewicz, K.M., McCrea, M., Marshall, S.W., Cantu, R.C., Randolph, C., Barr, W., & Kelly, J.P. (2003). Cumulative effects associated with recurrent concussion in collegiate football players: The NCAA Concussion Study. Journal of the American Medical Association, 290(19), 2549–2555.Google Scholar
Guskiewicz, K.M., Ross, S.E., & Marshall, S.W. (2001). Postural stability and neuropsychological deficits after concussion in collegiate athletes. Journal of Athletic Training, 36(3), 263–273.Google Scholar
Guskiewicz, K.M., Weaver, N.L., Padua, D.A., & Garrett, W.E. (2000). Epidemiology of concussion in collegiate and high school football players. The American Journal of Sports Medicine, 28(5), 643–650.Google Scholar
Hall, J.A., & Matsumoto, D. (2004). Gender differences in judgments of multiple emotions from facial expressions. Emotion, 4(2), 201–206.Google Scholar
Hampson, E., van Anders, S.M., & Mullin, L.I. (2006). A female advantage in the recognition of emotional facial expressions: Test of an evolutionary hypothesis. Evolution and Human Behavior, 27(6), 401–416.Google Scholar
Harmer, C.J., Grayson, L., & Goodwin, G.M. (2002). Enhanced recognition of disgust in bipolar illness. Biological Psychiatry, 51(4), 298–304.Google Scholar
Henry, J.D., Phillips, L.H., Crawford, J.R., Ietswaart, M., & Summers, F. (2006). Theory of mind following traumatic brain injury: The role of emotion recognition and executive dysfunction. Neuropsychologia, 44(10), 1623–1628. doi: 10.1016/j.neuropsychologia.2006.03.020 Google Scholar
Henry, L.C., Tremblay, J., Tremblay, S., Lee, A., Brun, C., Lepore, N., & Lassonde, M. (2011). Acute and chronic changes in diffusivity measures after sports concussion. Journal of Neurotrauma, 28(10), 2049–2059. doi: 10.1089/neu.2011.1836 Google Scholar
Henry, L.C., Tremblay, S., Boulanger, Y., Ellemberg, D., & Lassonde, M. (2010). Neurometabolic changes in the acute phase after sports concussions correlate with symptom severity. Journal of Neurotrauma, 27(1), 65–76.Google Scholar
Henry, L.C., Tremblay, S., Leclerc, S., Khiat, A., Boulanger, Y., Ellemberg, D., & Lassonde, M. (2011). Metabolic changes in concussed American football players during the acute and chronic post-injury phases. BMC Neurology, 11, 105. doi: 10.1186/1471-2377-11-105 Google Scholar
Hopkins, M.J., Dywan, J., & Segalowitz, S.J. (2002). Altered electrodermal response to facial expression after closed head injury. Brain Injury, 16(3), 245–257. doi: 10.1080/02699050110103346 Google Scholar
Humphreys, K., Minshew, N., Leonard, G.L., & Behrmann, M. (2007). A fine-grained analysis of facial expression processing in high-functioning adults with autism. Neuropsychologia, 45(4), 685–695.Google Scholar
Ietswaart, M., Milders, M., Crawford, J.R., Currie, D., & Scott, C.L. (2008). Longitudinal aspects of emotion recognition in patients with traumatic brain injury. Neuropsychologia, 46(1), 148–159. doi: 10.1016/j.neuropsychologia.2007.08.002 Google Scholar
Iverson, G.L., Brooks, B.L., Lovell, M.R., & Collins, M.W. (2006). No cumulative effects for one or two previous concussions. British Journal of Sports Medicine, 40(1), 72–75. doi: 10.1136/bjsm.2005.020651 Google Scholar
Iverson, G.L., Gaetz, M., Lovell, M.R., & Collins, M.W. (2004). Cumulative effects of concussion in amateur athletes. Brain Injury, 18(5), 433–443. doi: 10.1080/02699050310001617352 Google Scholar
Johnson, S.C., Pinkston, J.B., Bigler, E.D., & Blatter, D.D. (1996). Corpus callosum morphology in normal controls and traumatic brain injury: Sex differences, mechanisms of injury, and neuropsychological correlates. Neuropsychology, 10(3), 408–415.Google Scholar
Koponen, S., Taiminen, T., Hiekkanen, H., & Tenovuo, O. (2011). Axis I and II psychiatric disorders in patients with traumatic brain injury: A 12-month follow-up study. Brain Injury, 25(11), 1029–1034. doi: 10.3109/02699052.2011.607783 Google Scholar
Koponen, S., Taiminen, T., Portin, R., Himanen, L., Isoniemi, H., Heinonen, H., & Tenovuo, O. (2002). Axis I and II psychiatric disorders after traumatic brain injury: A 30-year follow-up study. The American Journal of Psychiatry, 159(8), 1315–1321.Google Scholar
Kosaka, B. (2006). Neuropsychological assessment in mild traumatic brain injury: A clinical overview. British Columbia Medical Journal, 48(9), 447–452.Google Scholar
Kutcher, J.S., & Eckner, J.T. (2010). At-risk populations in sports-related concussion. Current Sports Medicine Reports, 9(1), 16–20.Google Scholar
Langner, O., Dotsch, R., Bijlstra, G., Wigboldus, D.H., Hawk, S.T., & van Knippenberg, A. (2010). Presentation and validation of the Radboud Faces Database. Cognition and Emotion, 24(8), 1377–1388.Google Scholar
Larson-Dupuis, C., Chamard, E., Falardeau, V., Frasnelli, J., Beaulieu, C., Poirier, J., & De Beaumont, L. (2015). Impact of BDNF Val66Met polymorphism on olfactory functions of female concussed athletes. Brain Injury, 29(7-8), 963–970. doi: 10.3109/02699052.2015.1016452 Google Scholar
Lincoln, A.E., Caswell, S.V., Almquist, J.L., Dunn, R.E., Norris, J.B., & Hinton, R.Y. (2011). Trends in concussion incidence in high school sports a prospective 11-year study. The American Journal of Sports Medicine, 39(5), 958–963.Google Scholar
Lovell, M.R. (2004). Grade 1 or “Ding” concussions in high school athletes. The American Journal of Sports Medicine, 32(1), 47–54. doi: 10.1177/0363546503260723 Google Scholar
Lovell, M.R., Collins, M.W., Iverson, G.L., Field, M., Maroon, J.C., Cantu, R., & Fu, F.H. (2003). Recovery from mild concussion in high school athletes. Journal of Neurosurgery, 98(2), 296–301.Google Scholar
Marar, M., McIlvain, N.M., Fields, S.K., & Comstock, R.D. (2012). Epidemiology of concussions among United States high school athletes in 20 sports. The American Journal of Sports Medicine, 40(4), 747–755.Google Scholar
Marečková, K., Perrin, J.S., Khan, I.N., Lawrence, C., Dickie, E., McQuiggan, D.A., & Consortium, I. (2012). Hormonal contraceptives, menstrual cycle and brain response to faces. Social Cognitive & Affective Neuroscience, 9(2), 191–200.Google Scholar
Maroon, J.C., Lovell, M.R., Norwig, J., Podell, K., Powell, J.W., & Hartl, R. (2000). Cerebral concussion in athletes: Evaluation and neuropsychological testing. Neurosurgery, 47(3), 659–672.Google Scholar
McCrea, M., Barr, W.B., Guskiewicz, K.M., Randolph, C., Marshall, S.W., Cantu, R., & Kelly, J.P. (2005). Standard regression-based methods for measuring recovery after sport-related concussion. Journal of the International Neuropsychological Society, 11(1), 58–69.Google Scholar
McCrea, M., Guskiewicz, K.M., Marshall, S.W., Barr, W., Randolph, C., Cantu, R.C., & Kelly, J.P. (2003). Acute effects and recovery time following concussion in collegiate football players: The NCAA Concussion Study. Journal of the American Medical Association, 290(19), 2556–2563.Google Scholar
McCrory, P.R., Meeuwisse, W.H., Aubry, M., Cantu, B., Dvorak, J., Echemendia, R.J., & Turner, M (2013). Consensus statement on concussion in sport: The 4th International Conference on Concussion in Sport held in Zurich, November 2012. British Journal of Sports Medicine, 47(5), 250–258. doi: 10.1136/bjsports-2013-092313 Google Scholar
McDonald, S., & Flanagan, S. (2004). Social perception deficits after traumatic brain injury: Interaction between emotion recognition, mentalizing ability, and social communication. Neuropsychology, 18(3), 572–579. doi: 10.1037/0894-4105.18.3.572 Google Scholar
McDonald, S., Flanagan, S., Rollins, J., & Kinch, J. (2003). TASIT: A new clinical tool for assessing social perception after traumatic brain injury. The Journal of Head Trauma Rehabilitation, 18(3), 219–238.Google Scholar
McDonald, S., Li, S., De Sousa, A., Rushby, J., Dimoska, A., James, C., & Tate, R.L. (2011). Impaired mimicry response to angry faces following severe traumatic brain injury. Journal of Clinical and Experimental Neuropsychology, 33(1), 17–29. doi: 10.1080/13803391003761967 CrossRefGoogle ScholarPubMed
Milders, M., Ietswaart, M., Crawford, J.R., & Currie, D. (2008). Social behavior following traumatic brain injury and its association with emotion recognition, understanding of intentions, and cognitive flexibility. Journal of the International Neuropsychological Society, 14(2), 318–326.Google Scholar
Montagne, B., Kessels, R.P., Frigerio, E., de Haan, E.H., & Perrett, D.I. (2005). Sex differences in the perception of affective facial expressions: Do men really lack emotional sensitivity? Cognitive Processing, 6(2), 136–141.Google Scholar
Pearson, R., & Lewis, M.B. (2005). Fear recognition across the menstrual cycle. Hormones and Behavior, 47(3), 267–271.Google Scholar
Phillips, M.L., Drevets, W.C., Rauch, S.L., & Lane, R. (2003). Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry, 54(5), 504–514. doi: 10.1016/s0006-3223(03)00168-9 Google Scholar
Rahman, Q., Wilson, G.D., & Abrahams, S. (2004). Sex, sexual orientation, and identification of positive and negative facial affect. Brain and Cognition, 54(3), 179–185.Google Scholar
Rapcsak, S.Z., Galper, S., Comer, J., Reminger, S., Nielsen, L., Kaszniak, A.W., & Cohen, R. (2000). Fear recognition deficits after focal brain damage: A cautionary note. Neurology, 54(3), 575–581.Google Scholar
Richards, A., French, C.C., Calder, A.J., Webb, B., Fox, R., & Young, A.W. (2002). Anxiety-related bias in the classification of emotionally ambiguous facial expressions. Emotion, 2(3), 273–287.Google Scholar
Rosenberg, H., Dethier, M., Kessels, R.P., Westbrook, R.F., & McDonald, S. (2015). Emotion perception after moderate-severe traumatic brain injury: The valence effect and the role of working memory, processing speed, and nonverbal reasoning. Neuropsychology, 29(4), 509–521. doi: 10.1037/neu0000171 Google Scholar
Schatz, P., Moser, R.S., Covassin, T., & Karpf, R. (2011). Early indicators of enduring symptoms in high school athletes with multiple previous concussions. Neurosurgery, 68(6), 1562–1567.Google Scholar
Slobounov, S., Slobounov, E., Sebastianelli, W., Cao, C., & Newell, K. (2007). Differential rate of recovery in athletes after first and second concussion episodes. Neurosurgery, 61(2), 338–344; discussion 344. doi: 10.1227/01.NEU.0000280001.03578.FF Google Scholar
Smith, M.L., Cottrell, G.W., Gosselin, F., & Schyns, P.G. (2005). Transmitting and decoding facial expressions. Psychological Science, 16(3), 184–189.Google Scholar
Solomon, G.S., Kuhn, A.W., & Zuckerman, S.L. (2015). Depression as a modifying factor in sport-related concussion: A critical review of the literature. The Physician and Sportsmedicine, 44(1), 14–19.Google Scholar
Squire, L.R., Stark, C.E., & Clark, R.E. (2004). The medial temporal lobe*. Annual Review of Neuroscience, 27, 279–306.Google Scholar
Squire, L.R., & Zola-Morgan, S. (1991). The medial temporal lobe memory system. Science, 253(5026), 1380–1386.Google Scholar
Stuss, D.T., Alexander, M.P., & Benson, D.F. (1997). Frontal lobe functions. In M.R. Trimble & J.L. Cummings (Eds.), Contemporary behavioral neurology Vol. 16, pp. 348). Woburn, MA: Butterworth-Heinemann.Google Scholar
Tardif, J., Fiset, D., & Blais, C. (2014). Narcissistic personality differences in facial emotional expression categorization. Journal of Vision, 14(10), 1444–1444.Google Scholar
Tardif, J., Hébert, K., Blais, C., Fiset, D., Mercier, K., Brunet, J.-F., & Forest, G. (2014). The impact of sleep deprivation on the ability to recognize blended human emotions. Sleep, A89.Google Scholar
Tate, D.F., & Bigler, E.D. (2000). Fornix and hippocampal atrophy in traumatic brain injury. Learning & Memory, 7(6), 442–446.Google Scholar
Thayer, J., & Johnsen, B.H. (2000). Sex differences in judgement of facial affect: A multivariate analysis of recognition errors. Scandinavian Journal of Psychology, 41(3), 243–246.Google Scholar
Theriault, M., De Beaumont, L., Gosselin, N., Filipinni, M., & Lassonde, M. (2009). Electrophysiological abnormalities in well functioning multiple concussed athletes. Brain Injury, 23(11), 899–906. doi: 10.1080/02699050903283189 Google Scholar
Theriault, M., De Beaumont, L., Tremblay, S., Lassonde, M., & Jolicoeur, P. (2011). Cumulative effects of concussions in athletes revealed by electrophysiological abnormalities on visual working memory. Journal of Clinical and Experimental Neuropsychology, 33(1), 30–41. doi: 10.1080/13803391003772873 CrossRefGoogle ScholarPubMed
Tremblay, S., De Beaumont, L., Henry, L.C., Boulanger, Y., Evans, A.C., Bourgouin, P., & Lassonde, M. (2013). Sports concussions and aging: A neuroimaging investigation. Cerebral Cortex, 23(5), 1159–1166. doi: 10.1093/cercor/bhs102 Google Scholar
Trojian, T. (2016). Depression is under-recognised in the sport setting: Time for primary care sports medicine to be proactive and screen widely for depression symptoms. British Journal of Sports Medicine, 50(3), 137–139.Google Scholar
Vagnozzi, R., Signoretti, S., Cristofori, L., Alessandrini, F., Floris, R., Isgro, E., & Lazzarino, G. (2010). Assessment of metabolic brain damage and recovery following mild traumatic brain injury: A multicentre, proton magnetic resonance spectroscopic study in concussed patients. Brain, 133(11), 3232–3242. doi: 10.1093/brain/awq200 Google Scholar
Vagnozzi, R., Signoretti, S., Tavazzi, B., Floris, R., Ludovici, A., Marziali, S., & Delfini, R. (2008). Temporal window of metabolic brain vulnerability to concussion: A pilot 1H‐magnetic resonance spectroscopic study in concussed athletes—Part III. Neurosurgery, 62(6), 1286–1296.Google Scholar
Vargas, G., Rabinowitz, A., Meyer, J., & Arnett, P.A. (2015). Predictors and prevalence of postconcussion depression symptoms in collegiate athletes. Journal of Athletic Training, 50(3), 250–255.Google Scholar
Williams, C., & Wood, R.L. (2010). Impairment in the recognition of emotion across different media following traumatic brain injury. Journal of Clinical and Experimental Neuropsychology, 32(2), 113–122. doi: 10.1080/13803390902806543 Google Scholar
Wunderle, K., Hoeger, K.M., Wasserman, E., & Bazarian, J.J. (2014). Menstrual phase as predictor of outcome after mild traumatic brain injury in women. The Journal of Head Trauma Rehabilitation, 29(5), E1–E8.Google Scholar
Yang, J., Peek-Asa, C., Covassin, T., & Torner, J.C. (2015). Post-concussion symptoms of depression and anxiety in division I collegiate athletes. Developmental Neuropsychology, 40(1), 18–23. doi: 10.1080/87565641.2014.973499 Google Scholar
Young, A.W., Rowland, D., Calder, A.J., Etcoff, N.L., Seth, A., & Perrett, D.I. (1997). Facial expression megamix: Tests of dimensional and category accounts of emotion recognition. Cognition, 63(3), 271–313.Google Scholar
Zhang, K., Johnson, B., Pennell, D., Ray, W., Sebastianelli, W., & Slobounov, S. (2010). Are functional deficits in concussed individuals consistent with white matter structural alterations: Combined FMRI & DTI study. Experimental Brain Research, 204(1), 57–70. doi: 10.1007/s00221-010-2294-3 Google Scholar
Zhang, L., Heier, L., Zimmerman, R., Jordan, B., & Uluğ, A. (2006). Diffusion anisotropy changes in the brains of professional boxers. AJNR American Journal of Neuroradiology, 27(9), 2000–2004.Google Scholar
Zuckerman, S.L., Apple, R.P., Odom, M.J., Lee, Y.M., Solomon, G.S., & Sills, A.K. (2014). Effect of sex on symptoms and return to baseline in sport-related concussion: Clinical article. Journal of Neurosurgery: Pediatrics, 13(1), 72–81.Google Scholar