Skip to main content

Gender Differences in Preattentive Processing of Facial Expressions: An ERP Study

Brain Topography volume 26, pages 488–500 (2013)Cite this article

Abstract

To investigate gender differences in pre-attentive processing of facial expressions we recorded the expression mismatch negativity (EMMN) in the deviant-standard-reverse oddball paradigm. For female participants, sad faces elicited larger EMMN than happy faces, but this difference disappeared in the left hemisphere. For male participants, EMMN was not modulated by facial expressions, regardless of in the left or right hemispheres. While the source analysis indicated that for both genders prefrontal activations were observed for sad EMMN, more sources were involved for male than female participants. For happy EMMN, the current sources were located in the occipital lobe and parietal lobe for females and the temporal lobe and the frontal lobe for males. The present findings emphasized the importance of considering gender as a factor in the study of the pre-attentive processing of facial expressions.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Adolphs R (2002) Recognizing emotion from facial expressions: psychological and neurological mechanisms. Behav Cogn Neurosci Rev 1(1):21–62. doi:10.1177/1534582302001001003

    Article  PubMed  Google Scholar 

  • Adolphs R (2003) Cognitive neuroscience of human social behaviour. Nat Rev Neurosci 4(3):165–178. doi:10.1038/nrn1056

    Article  PubMed  CAS  Google Scholar 

  • Astikainen P, Hietanen JK (2009) Event-related potentials to task-irrelevant changes in facial expressions. Behav Brain Funct 5(1):30

    Article  PubMed  Google Scholar 

  • Astikainen P, Ruusuvirta T, Wikgren J, Korhonen T (2004) The human brain processes visual changes that are not cued by attended auditory stimulation. Neurosci Lett 368(2):231–234

    Article  PubMed  CAS  Google Scholar 

  • Astikainen P, Lillstrang E, Ruusuvirta T (2008) Visual mismatch negativity for changes in orientation: a sensory memory-dependent response. Eur J Neurosci 28(11):2319–2324

    Article  PubMed  Google Scholar 

  • Baumeister RF, Bratslavsky E, Finkenauer C, Vohs KD (2001) Bad is stronger than good. Rev General Psychol 5(4):323–370

    Article  Google Scholar 

  • Bentin S, Allison T, Puce A, Perez E, McCarthy G (1996) Electrophysiological studies of face perception in humans. J Cogn Neurosci 8(6):551–565

    Article  PubMed  Google Scholar 

  • Bentin S, Taylor MJ, Rousselet GA, Itier RJ, Caldara R, Schyns PG, Rossion B (2007) Controlling interstimulus perceptual variance does not abolish N170 face sensitivity. Nat Neurosci 10(7):801–802

    Article  PubMed  CAS  Google Scholar 

  • Cacioppo JT, Berntson GG (1994) Relationship between attitudes and evaluative space: a critical review with emphasis on the separability of positive and negative substrates. Psychol Bull 115(3):401–423

    Article  Google Scholar 

  • Cacioppo JT, Gardner WL, Berntson GG (1997) Beyond bipolar conceptualizations and measures: the case of attitudes and evaluative space. Pers Soc Psychol Rev 1(1):3–25

    Article  PubMed  CAS  Google Scholar 

  • Caharel S, Courtay N, Bernard C, Lalonde R, Rebaï M (2005) Familiarity and emotional expression influence an early stage of face processing: an electrophysiological study. Brain Cogn 59(1):96–100. doi:10.1016/j.bandc.2005.05.005

    Article  PubMed  Google Scholar 

  • Campanella S, Rossignol M, Mejias S, Joassin F, Maurage P, Debatisse D, Guérit JM (2004) Human gender differences in an emotional visual oddball task: an event-related potentials study. Neurosci Lett 367(1):14–18

    Article  PubMed  CAS  Google Scholar 

  • Campanella S, Falbo L, Rossignol M, Grynberg D, Balconi M, Verbanck P, Maurage P (2012) Sex differences on emotional processing are modulated by subclinical levels of alexithymia and depression: a preliminary assessment using event-related potentials. Psychiatry Res 197(1–2):145–153. doi:10.1016/j.psychres.2011.12.026

    Article  PubMed  Google Scholar 

  • Chang Y, Xu J, Shi N, Zhang B, Zhao L (2010) Dysfunction of processing task-irrelevant emotional faces in major depressive disorder patients revealed by expression-related visual MMN. Neurosci Lett 472(1):33–37

    Article  PubMed  CAS  Google Scholar 

  • Czigler I, Balázs L, Winkler I (2002) Memory-based detection of task-irrelevant visual changes. Psychophysiology 39(6):869–873

    Article  PubMed  Google Scholar 

  • Czigler I, Balázs L, Pató LG (2004) Visual change detection: event-related potentials are dependent on stimulus location in humans. Neurosci Lett 364(3):149–153. doi:10.1016/j.neulet.2004.04.048

    Article  PubMed  CAS  Google Scholar 

  • Eger E, Jedynak A, Iwaki T, Skrandies W (2003) Rapid extraction of emotional expression: evidence from evoked potential fields during brief presentation of face stimuli. Neuropsychologia 41(7):808–817. doi:10.1016/s0028-3932(02)00287-7

    Article  PubMed  CAS  Google Scholar 

  • Eimer M, Holmes A (2007) Event-related brain potential correlates of emotional face processing. Neuropsychologia 45(1):15–31

    Article  PubMed  Google Scholar 

  • Fuchs M, Kastner J, Wagner M, Hawes S, Ebersole JS (2002) A standardized boundary element method volume conductor model. Clin Neurophysiol 113(5):702–712

    Article  PubMed  Google Scholar 

  • Fusar-Poli P, Placentino A, Carletti F, Landi P, Allen P, Surguladze S, Politi P (2009) Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci 34(6):418–432

    PubMed  Google Scholar 

  • Goffaux V, Gauthier I, Rossion B (2003) Spatial scale contribution to early visual differences between face and object processing. Cogn Brain Res 16(3):416–424. doi:10.1016/s0926-6410(03)00056-9

    Article  Google Scholar 

  • Grimshaw GM, Bulman-Fleming MB, Ngo C (2004) A signal-detection analysis of sex differences in the perception of emotional faces. Brain Cogn 54(3):248–250

    Article  PubMed  Google Scholar 

  • Hall JA, Matsumoto D (2004) Gender differences in judgments of multiple emotions from facial expressions. Emotion 4(2):201–206

    Article  PubMed  Google Scholar 

  • Hoffmann H, Kessler H, Eppel T, Rukavina S, Traue HC (2010) Expression intensity, gender and facial emotion recognition: women recognize only subtle facial emotions better than men. Acta Psychol 135(3):278–283

    Article  Google Scholar 

  • Ikezawa S, Nakagome K, Mimura M, Shinoda J, Itoh K, Homma I, Kamijima K (2008) Gender differences in lateralization of mismatch negativity in dichotic listening tasks. Int J Psychophysiol 68(1):41–50

    Article  PubMed  Google Scholar 

  • Jarros RB, Salum GA, da Belem Silva CT, Toazza R, Abreu Costa M, de Fumagalli Salles J, Manfro GG (2012) Anxiety disorders in adolescence are associated with impaired facial expression recognition to negative valence. J Psychiatr Res 46(2):147–151

    Article  PubMed  Google Scholar 

  • Jurcak V, Tsuzuki D, Dan I (2007) 10/20, 10/10, and 10/5 systems revisited: their validity as relative head-surface-based positioning systems. Neuroimage 34(4):1600–1611

    Article  PubMed  Google Scholar 

  • Kasai K, Nakagome K, Iwanami A, Fukuda M, Itoh K, Koshida I, Kato N (2002) No effect of gender on tonal and phonetic mismatch negativity in normal adults assessed by a high-resolution EEG recording. Cogn Brain Res 13(3):305–312

    Article  Google Scholar 

  • Kesler-West ML, Andersen AH, Smith CD, Avison MJ, Davis CE, Kryscio RJ, Blonder LX (2001) Neural substrates of facial emotion processing using fMRI. Cogn Brain Res 11(2):213–226

    Article  CAS  Google Scholar 

  • Kimura M, Katayama Ji, Murohashi H (2006) An ERP study of visual change detection: effects of magnitude of spatial frequency changes on the change-related posterior positivity. Int J Psychophysiol 62(1):14–23

    Article  PubMed  Google Scholar 

  • Kimura M, Katayama Ji, Ohira H, Schröger E (2009) Visual mismatch negativity: new evidence from the equiprobable paradigm. Psychophysiology 46(2):402–409

    Article  PubMed  Google Scholar 

  • Kimura M, Ohira H, Schröger E (2010a) Localizing sensory and cognitive systems for pre-attentive visual deviance detection: an sLORETA analysis of the data of Kimura et al. (2009). Neurosci Lett 485(3):198–203

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Schröger E, Czigler I, Ohira H (2010b) Human visual system automatically encodes sequential regularities of discrete events. J Cogn Neurosci 22(6):1124–1139

    Article  PubMed  Google Scholar 

  • Kimura M, Widmann A, Schröger E (2010c) Human visual system automatically represents large-scale sequential regularities. Brain Res 1317:165–179

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Kondo H, Ohira H, Schröger E (2011) Unintentional temporal context–based prediction of emotional faces: an electrophysiological study. Cereb Cortex. doi:10.1093/cercor/bhr244

    PubMed  Google Scholar 

  • Kret ME, De Gelder B (2012) A review on sex differences in processing emotional signals. Neuropsychologia 50(7):1211–1221. doi:10.1016/j.neuropsychologia.2011.12.022

    Article  PubMed  CAS  Google Scholar 

  • Krombholz A, Schaefer F, Boucsein W (2007) Modification of N170 by different emotional expression of schematic faces. Biol Psychol 76(3):156–162

    Article  PubMed  Google Scholar 

  • Lee TMC, Liu HL, Hoosain R, Liao WT, Wu CT, Yuen KSL, Gao JH (2002) Gender differences in neural correlates of recognition of happy and sad faces in humans assessed by functional magnetic resonance imaging. Neurosci Lett 333(1):13–16

    Article  PubMed  CAS  Google Scholar 

  • Lee SH, Kim EY, Kim S, Bae SM (2010) Event-related potential patterns and gender effects underlying facial affect processing in schizophrenia patients. Neurosci Res 67(2):172–180

    Article  PubMed  Google Scholar 

  • Li H, Yuan J, Lin C (2008) The neural mechanism underlying the female advantage in identifying negative emotions: an event-related potential study. Neuroimage 40(4):1921–1929

    Article  PubMed  Google Scholar 

  • Li X, Lu Y, Sun G, Gao L, Zhao L (2012) Visual mismatch negativity elicited by facial expressions: new evidence from the equiprobable paradigm. Behav Brain Funct 8(1):7. doi:10.1186/1744-9081-8-7

    Article  PubMed  Google Scholar 

  • Liddell BJ, Williams LM, Rathjen J, Shevrin H, Gordon E (2004) A temporal dissociation of subliminal versus supraliminal fear perception: an event-related potential study. J Cogn Neurosci 16:479–486

    Article  PubMed  Google Scholar 

  • Lithari C, Frantzidis C, Papadelis C, Vivas A, Klados M, Kourtidou-Papadeli C, Bamidis P (2010) Are females more responsive to emotional stimuli? A neurophysiological study across arousal and valence dimensions. Brain Topogr 23(1):27–40. doi:10.1007/s10548-009-0130-5

    Article  PubMed  CAS  Google Scholar 

  • Lithari C, Klados MA, Papadelis C, Pappas C, Albani M, Bamidis PD (2012) How does the metric choice affect brain functional connectivity networks? Biomed Signal Process Control 7(3):228–236. doi:10.1016/j.bspc.2011.05.004

    Article  Google Scholar 

  • Maxwell JS, Shackman AJ, Davidson RJ (2005) Unattended facial expressions asymmetrically bias the concurrent processing of nonemotional information. J Cogn Neurosci 17:1386–1395

    Article  PubMed  Google Scholar 

  • Montagne B, Kessels R, Frigerio E, de Haan E, Perrett D (2005) Sex differences in the perception of affective facial expressions: do men really lack emotional sensitivity? Cogn Process 6(2):136–141

    Article  PubMed  Google Scholar 

  • Morris JS, Öhman A, Dolan RJ (1999) A subcortical pathway to the right amygdala mediating “unseen” fear. Proc Natl Acad Sci USA 96(4):1680–1685. doi:10.1073/pnas.96.4.1680

    Article  PubMed  CAS  Google Scholar 

  • Näätänen R, Pakarinen S, Rinne T, Takegata R (2004) The mismatch negativity (MMN): towards the optimal paradigm. Clin Neurophysiol 115(1):140–144

    Article  PubMed  Google Scholar 

  • Olofsson JK, Polich J (2007) Affective visual event-related potentials: arousal, repetition, and time-on-task. Biol Psychol 75(1):101–108. doi:10.1016/j.biopsycho.2006.12.006

    Article  PubMed  Google Scholar 

  • Palermo R, Rhodes G (2007) Are you always on my mind? A review of how face perception and attention interact. Neuropsychologia 45(1):75–92

    Article  PubMed  Google Scholar 

  • Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24D:5–12

    Google Scholar 

  • Pazo-Alvarez P, Amenedo E, Cadaveira F (2004) Automatic detection of motion direction changes in the human brain. Eur J Neurosci 19(7):1978–1986

    Article  PubMed  CAS  Google Scholar 

  • Rahko J, Paakki J–J, Starck T, Nikkinen J, Remes J, Hurtig T, Kiviniemi V (2010) Functional mapping of dynamic happy and fearful facial expression processing in adolescents. Brain Imaging Behav 4(2):164–176

    Article  PubMed  Google Scholar 

  • Rahman Q, Wilson GD, Abrahams S (2004) Sex, sexual orientation, and identification of positive and negative facial affect. Brain Cogn 54(3):179–185

    Article  PubMed  Google Scholar 

  • Rossion B, Jacques C (2008) Does physical interstimulus variance account for early electrophysiological face sensitive responses in the human brain? Ten lessons on the N170. Neuroimage 39(4):1959–1979. doi:10.1016/j.neuroimage.2007.10.011

    Article  PubMed  Google Scholar 

  • Rozenkrants B, Olofsson JK, Polich J (2008) Affective visual event-related potentials: arousal, valence, and repetition effects for normal and distorted pictures. Int J Psychophysiol 67(2):114–123. doi:10.1016/j.ijpsycho.2007.10.010

    PubMed  Google Scholar 

  • Sagiv N, Bentin S (2001) Structural encoding of human and schematic faces: holistic and part-based processes. J Cogn Neurosci 13(7):937–951. doi:10.1162/089892901753165854

    Article  PubMed  CAS  Google Scholar 

  • Sato W, Kubota Y, Okada T, Murai T, Yoshikawa S, Sengoku A (2002) Seeing happy emotion in fearful and angry faces: qualitative analysis of facial expression recognition in a bilateral amygdala-damaged patient. Cortex 38(5):727–742

    Article  PubMed  Google Scholar 

  • Schirmer A, Kotz SA, Friederici AD (2002) Sex differentiates the role of emotional prosody during word processing. Cogn Brain Res 14(2):228–233

    Article  Google Scholar 

  • Schirmer A, Striano T, Friederici AD (2005) Sex differences in the preattentive processing of vocal emotional expressions. Neuroreport 16(6):635–639

    Article  PubMed  Google Scholar 

  • Semlitsch HV, Anderer P, Schuster P, Presslich O (1986) A solution for reliable and valid reduction of ocular artifacts, applied to the P300 ERP. Psychophysiology 23(6):695–703. doi:10.1111/j.1469-8986.1986.tb00696.x

    Article  PubMed  CAS  Google Scholar 

  • Stefanics G, Csukly G, Komlósi S, Czobor P, Czigler I (2012) Processing of unattended facial emotions: a visual mismatch negativity study. Neuroimage 59(3):3042–3049

    Article  PubMed  Google Scholar 

  • Susac A, Ilmoniemi RJ, Pihko E, Supek S (2004) Neurodynamic studies on emotional and inverted faces in an oddball paradigm. Brain Topogr 16(4):265–268

    Article  PubMed  Google Scholar 

  • Urakawa T, Inui K, Yamashiro K, Kakigi R (2010) Cortical dynamics of the visual change detection process. Psychophysiology 47(5):905–912

    PubMed  Google Scholar 

  • Wagner M, Fuchs M, Kastner J (2004) Evaluation of sLORETA in the presence of noise and multiple sources. Brain Topogr 16(4):277–280

    Article  PubMed  Google Scholar 

  • Weymar M, Löw A, Öhman A, Hamm AO (2011) The face is more than its parts: brain dynamics of enhanced spatial attention to schematic threat. Neuroimage 58(3):946–954

    Article  PubMed  Google Scholar 

  • Wright CI, Martis B, Shin LM, Fischer H, Rauch SL (2002) Enhanced amygdala responses to emotional versus neutral schematic facial expressions. Neuroreport 13(6):785–790

    Article  PubMed  Google Scholar 

  • Yucel G, McCarthy G, Belger A (2007) fMRI reveals that involuntary visual deviance processing is resource limited. Neuroimage 34(3):1245–1252

    Article  PubMed  Google Scholar 

  • Zhao L, Li J (2006) Visual mismatch negativity elicited by facial expressions under non-attentional condition. Neurosci Lett 410(2):126–131

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Psychology and Cognitive Science, East China Normal University, Shanghai, China

    Qiang Xu

  2. Department of Psychology, Ningbo University, Ningbo, China

    Yaping Yang

  3. Department of Psychology, Shanghai Normal University, Shanghai, China

    Pei Wang

  4. Department of Medical Imaging, Jinan Military General Hospital, Jinan, China

    Gang Sun & Lun Zhao

Authors
  1. Qiang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yaping Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gang Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lun Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Pei Wang or Lun Zhao.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Xu, Q., Yang, Y., Wang, P. et al. Gender Differences in Preattentive Processing of Facial Expressions: An ERP Study. Brain Topogr 26, 488–500 (2013). https://doi.org/10.1007/s10548-013-0275-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-013-0275-0

Keywords

  • Gender differences
  • Pre-attentive processes
  • EMMN