Abstract
Using a rapid serial visual presentation paradigm, we previously showed that the average amplitudes of six event-related potential (ERP) components were affected by different categories of emotional faces. In the current study, we investigated the six discriminating components on a single-trial level to clarify whether the amplitude difference between experimental conditions results from a difference in the real variability of single-trial amplitudes or from latency jitter across trials. It is found that there were consistent amplitude differences in the single-trial P1, N170, VPP, N3, and P3 components, demonstrating that a substantial proportion of the average amplitude differences can be explained by the pure variability in amplitudes on a single-trial basis between experimental conditions. These single-trial results verified the three-stage scheme of facial expression processing beyond multitrial ERP averaging, and showed the three processing stages of “fear popup”, “emotional/unemotional discrimination”, and “complete separation” based on the single-trial ERP dynamics.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Haxby J V, Hoffman E A, GobbiniM I. The distributed human neural system for face perception. Trends Cogn Sci, 2000, 4: 223–233
Adolphs R. Recognizing emotion from facial expressions: psychological and neurological mechanisms. Behav Cogn Neurosci Rev, 2002: 1, 21–62
Calder A J, Young A W. Understanding the recognition of facial identity and facial expression. Nat Rev Neurosc, 2005, 6: 641–651
Esslen M, Pascual-Marqui R D, Hell D, et al. Brain areas and time course of emotional processing. Neuroimage, 2004, 21: 1189–1203
Eimer M, Holmes A. Event-related brain potential correlates of emotional face processing. Neuropsychologia, 2007, 45: 15–31
Palermo R, Rhodes G. Are you always on my mind? A review of how face perception and attention interact. Neuropsychologia, 2007, 45: 75–92
Utama N P, Takemoto A, Koike Y, et al. Phased processing of facial emotion: an ERP study. Neurosci Res, 2009, 64: 30–40
Pessoa L, McKenna M, Gutierrez E, et al. Neural processing of emotional faces requires attention. Proc Natl Acad Sci USA, 2002, 99: 11458–11463
Schupp H T, Stockburger J, Codispoti M, et al. Selective visual attention to emotion. J Neurosci, 2007, 27: 1082–1089
Flaisch T, Junghöfer M, Bradley M M, et al. Rapid picture processing: affective primes and targets. Psychophysiology, 2008, 45: 1–10
Luo W, Feng W, He W, et al. Three stages of facial expression processing: ERP study with rapid serial visual presentation. Neuroimage, 2010, 49: 1857–1867
Jung T P, Makeig S, Westerfield M, et al. Analysis and visualization of single-trial event-related potentials. Hum Brain Mapp, 2001, 14: 166–185
Limpiti T, Van Veen B D, Wakai, R T. A spatiotemporal framework for MEG/EEG evoked response amplitude and latency variability estimation. IEEE Trans Biomed Eng, 2010, 57: 616–625
Blankertz B, Lemm S, Treder M, et al. Single-trial analysis and classification of ERP components-a tutorial. Neuroimage, 2011, 56: 814–825
Unsal A, Segalowitz S J. Sources of P300 attenuation after head injury: single-trial amplitude, latency jitter, and EEG power. Psychophysiology, 1995, 32: 249–256
Walhovd K B, Rosquist H, Fjell A M. P300 amplitude age reductions are not caused by latency jitter. Psychophysiology, 2008, 45: 545–553
Rousselet G A, Husk J S, Bennett P J, et al. Single-trial EEG dynamics of object and face visual processing. Neuroimage, 2007, 36: 843–862
Ford J M, White P, Lim K O, et al. Schizophrenics have fewer and smaller P300s: a single-trial analysis. Biol Psychia, 1994, 35: 96–103
Spencer K M. Averaging, detection, and classification of single-trial ERPs. In: Handy T C, ed. Event-Related Potentials: a Method Handbook. London: The MIT Press, 2005. 209–227
Williams L M, Palmer D, Liddell B J, et al. The ‘when’ and ‘where’ of perceiving signals of threat versus non-threat. Neuroimage, 2006, 31: 458–467
Jaśkowski P, Verleger R. Amplitudes and latencies of single-trial ERP’s estimated by a maximum-likelihood method. IEEE Trans Biomed Eng, 1999, 46: 987–993
Jaśkowski P, Verleger R. An evaluation of methods for single-trial estimation of P3 latency. Psychophysiology, 2000, 37: 153–162
Pham D T, Möcks J, Köhler W, et al. Variable latencies of noisy signals: estimation and testing in brain potential data. Biometrika, 1987, 74: 525–533
Möcks J, Köhler W, Gasser T, et al. Novel approaches to the problem of latency jitter. Psychophysiology, 1988, 25: 217–226
Rousselet G A, Pernet C R, Bennett P J, et al. Parametric study of EEG sensitivity to phase noise during face processing. BMC Neurosci, 2008, 9: 1–22
Adolphs R, Tranel D, Damasio H, et al. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature, 1994, 372: 613–614
Adolphs R, Tranel D, Damasio H, et al. Fear and the human amygdala. J Neurosci, 1995, 15: 5879–5891
LeDoux J. Fear and the brain: where have we been, and where are we going? Biol Psychiatry, 1998, 44: 1229–1238
Rotshtein P, Richardson M P, Winston J S, et al. Amygdala damage affects event-related potentials for fearful faces at specific time windows. Hum Brain Mapp, 2010, 31: 1089–1105
Kawasaki H, Kaufman O, Damasio H, et al. Single-neuron responses to emotional visual stimuli recorded in human ventral prefrontal cortex. Nat Neurosci, 2001, 4: 15–16
Meeren H K, van Heijnsbergen C C, de Gelder B. Rapid perceptual integration of facial expression and emotional body language. Proc Natl Acad Sci USA, 2005, 102: 16518–16523
Vuilleumier P, Pourtois G. Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia, 2007, 45: 174–194
Eimer M, Holmes A. An ERP study on the time course of emotional face processing. Neuroreport, 2002, 13: 427–431
Eger E, Jedynak A, Iwaki T, et al. Rapid extraction of emotional expression: evidence from evoked potential fields during brief presentation of face stimuli. Neuropsychologia, 2003, 41: 808–817
Pourtois G, Grandjean D, Sander D, et al. Electrophysiological correlates of rapid spatial orienting towards fearful faces. Cereb Cortex, 2004, 14: 619–633
Pourtois G, Dan E S, Grandjean D, et al. Enhanced extrastriate visual response to bandpass spatial frequency filtered fearful faces: time course and topographic evoked-potentials mapping. Hum Brain Mapp, 2005, 26: 65–79
Ito T A, Larsen J T, Smith N K, et al. Negative information weighs more heavily on the brain: the negativity bias in evaluative categorizations. J Pers Soc Psychol, 1998, 75: 887–900
Cacioppo J T, Gardner W L. Emotion. Annu Rev Psychol, 1999, 50: 191–214
Krolak-Salmon P, Fischer C, Vighetto A, et al. Processing of facial emotional expression: spatio-temporal data as assessed by scalp event-related potentials. Eur J Neurosci, 2001, 13: 987–994
Campanella S, Quinet P, Bruyer R, et al. Categorical perception of happiness and fear facial expressions: an ERP study. J Cogn Neurosci, 2002, 14: 210–227
Batty M, Taylor M J. Early processing of the six basic facial emotional expressions. Cognitive Brain Res, 2003, 17: 613–620
Jiang Y, Shannon R W, Vizueta N, et al. Dynamics of processing invisible faces in the brain: automatic neural encoding of facial expression information. Neuroimage, 2009, 44: 1171–1177
Carretié L, Iglesias J. An ERP study on the specificity of facial expression processing. Int J Psychophysiol, 1995, 19: 183–192
Schyns P G, Petro L S, Smith M L. Dynamics of visual information integration in the brain for categorizing facial expressions. Curr Biol, 2007, 17: 1580–1585
Smith M L, Fries P, Gosselin F, et al. Inverse mapping the neuronal substrates of face categorizations. Cereb Cortex, 2009, 19: 2428–2438
Makeig S, Debener S, Onton J, et al. Mining event-related brain dynamics. Trends Cogn Sci, 2004, 8: 204–210
Klimesch W, Sauseng P, Hanslmayr S, et al. Event-related phase reorganization may explain evoked neural dynamics. Neurosci Biobehav R, 2007, 31: 1003–1016
Sauseng P, Klimesch W, Gruber W R, et al. Are event-related potential components generated by phase resetting of brain oscillations? A critical discussion. Neuroscience, 2007, 146: 1435–1444
Rossion B, Jacques C. Does physical interstimulus variance account for early electrophysiological face sensitive responses in the human brain? Ten lessons on the N170. Neuroimage, 2008, 39: 1959–1979
Kuefner D, de Heering A, Jacques C, et al. Early visually evoked electrophysiological responses over the human brain (P1, N170) show stable patterns of face-sensitivity from 4 years to adulthood. Front Hum Neurosci, 2010, 3: 67
Quian Quiroga R. Obtaining single stimulus evoked potentials with wavelet denoising. Physica D, 2010, 145: 278–292
Botzel K, Schulze S, Stodieck S R. Scalp topography and analysis of intracranial sources of face-evoked potentials. Exp Brain Res, 1995, 104: 135–143
Author information
Authors and Affiliations
Corresponding authors
Additional information
This article is published with open access at Springerlink.com
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 2.0 International License (https://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
About this article
Cite this article
Zhang, D., Luo, W. & Luo, Y. Single-trial ERP evidence for the three-stage scheme of facial expression processing. Sci. China Life Sci. 56, 835–847 (2013). https://doi.org/10.1007/s11427-013-4527-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-013-4527-8