Abstract
Empathy for pain is at the basis of altruistic behaviors and is known to be modulated by variables such as group membership, pleasantness or unpleasantness of situations and social relationships. Also, face attractiveness and aesthetic judgment might play a role when observing a person in painful conditions, by increasing individuals’ empathic responsiveness. Indeed, physical attractiveness can modify both the perception of the face itself and its reception in a social context. In the present study, we aimed to assess cortical activity when attention is focused on the aesthetic features of an individual showing painful feelings. Brain activity (optical imaging: functional near-infrared spectroscopy, fNIRS), considered in its hemodynamic components (oxygenated [oxy-Hb] and deoxygenated hemoglobin [deoxy-Hb]) was monitored when 22 subjects (Mage = 24.9; SD = 3.6) observed faces (attractive; unattractive) that received painful stimulations (pain; no pain) and were asked to judge the attractiveness and pain condition of the face. Specifically, we targeted the left and right inferior frontal gyrus (IFG), sensory cortex, and temporo-parietal junction (TPJ). Analyses revealed significant lower oxy-Hb levels in left IFG compared to right hemispheric channels when asking participants to rate faces attractiveness independently from the stimulus features. Besides, lower levels of deoxy-Hb were detected in the right TPJ for unattractive faces compared to attractive faces. Overall, present findings highlighted that the formulation of an aesthetic judgment and face attractiveness plays a relevant role in empathic concerns and this seems to be able to overlay painful appraisal.
Article Highlights
-
The aesthetic judgment of face stimuli overlays the evaluation of pain conditions.
-
A hemispheric lateralization effect related to emotion was found for right IFG.
-
Bilateral preparietal somatosensory association areas are involved in aesthetic judgment.
-
Unattractive faces triggered a cognitive empathic response modulated by the right TPJ.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated for this study are available on request to the corresponding author.
References
Aharon I, Etcoff N, Ariely D et al (2001) Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron 32:537–551. https://doi.org/10.1016/S0896-6273(01)00491-3
Allison T, Puce A, Mccarthy G (2000) Social perception from visual cues: role of the STS region. Trends Cogn Sci 4:267–278
Balconi M, Ferrari C (2013) Repeated transcranial magnetic stimulation on dorsolateral prefrontal cortex improves performance in emotional memory retrieval as a function of level of anxiety and stimulus valence. Psychiatry Clin Neurosci 67:210–218. https://doi.org/10.1111/pcn.12041
Balconi M, Mazza G (2010) Lateralisation effect in comprehension of emotional facial expression: a comparison between EEG alpha band power and behavioural inhibition (BIS) and activation (BAS) systems. Laterality Asymmetries Body. Brain Cogn 15:361–384. https://doi.org/10.1080/13576500902886056
Balconi M, Pozzoli U (2003) Face-selective processing and the effect of pleasant and unpleasant emotional expressions on ERP correlates. Int J Psychophysiol 49:67–74. https://doi.org/10.1016/S0167-8760(03)00081-3
Balconi M, Vanutelli ME (2016) Hemodynamic (fNIRS) and EEG (N200) correlates of emotional inter-species interactions modulated by visual and auditory stimulation. Sci Rep. https://doi.org/10.1038/srep23083
Balconi M, Brambilla E, Falbo L (2009) BIS/BAS, cortical oscillations and coherence in response to emotional cues. Brain Res Bull 80:151–157. https://doi.org/10.1016/j.brainresbull.2009.07.001
Balconi M, Grippa E, Vanutelli ME (2015) What hemodynamic (fNIRS), electrophysiological (EEG) and autonomic integrated measures can tell us about emotional processing. Brain Cogn 95:67–76. https://doi.org/10.1016/j.bandc.2015.02.001
Batson D (2014) The altruism question. Toward a social-psychological answer. Psychology Press, New York
Borod JC, Cicero BA, Obler LK et al (1998) Right hemisphere emotional perception: evidence across multiple channels. Neuropsychology 12:446–458. https://doi.org/10.1037//0894-4105.12.3.446
Botvinick M, Jha AP, Bylsma LM et al (2005) Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain. Neuroimage 25:312–319. https://doi.org/10.1016/j.neuroimage.2004.11.043
Calvo-Merino B, Urgesi C, Orgs G et al (2010) Extrastriate body area underlies aesthetic evaluation of body stimuli. Exp Brain Res 204:447–456. https://doi.org/10.1007/s00221-010-2283-6
Chatterjee A, Thomas A, Smith SE, Aguirre GK (2009) The neural response to facial attractiveness. Neuropsychology 23:135–143. https://doi.org/10.1037/a0014430
Craig K, Prkachin K, Grunau R (2001) The facial expression of pain. In: Turk D, Melzack R (eds) Handbook of pain assessment, 2nd edn. Guilford Press, New York, pp 153–169
Cui X, Bray S, Reiss AL (2010) Functional near infrared spectroscopy (NIRS) signal improvement based on negative correlation between oxygenated and deoxygenated hemoglobin dynamics. Neuroimage 49:3039–3046. https://doi.org/10.1016/j.neuroimage.2009.11.050
Davis MH (1980) A mulitdimensional approach to individual differences in empathy. J Pers Soc Psychol. https://doi.org/10.1037/0022-3514.44.1.113
de Waal FBM (2008) Putting the altruism back into altruism: the evolution of empathy. Annu Rev Psychol 59:279–300. https://doi.org/10.1146/annurev.psych.59.103006.093625
Dixson AF, Halliwell G, East R et al (2003) Masculine somatotype and hirsuteness as determinants of sexual attractiveness to women. Arch Sex Behav 32:29–39. https://doi.org/10.1023/A:1021889228469
Fan Y, Han S (2008) Temporal dynamic of neural mechanisms involved in empathy for pain: an event-related brain potential study. Neuropsychologia 46:160–173. https://doi.org/10.1016/j.neuropsychologia.2007.07.023
Frith U, Frith CD (2003) Development and neurophysiology of mentalizing. Philos Trans Biol Sci. https://doi.org/10.1098/rstb.2002.1218
Fu G, Mondloch C, Ding XP et al (2014) The neural correlates of the face attractiveness aftereffect: a functional near-infrared spectroscopy (fNIRS) study. Neuroimage 85:1–7. https://doi.org/10.1038/jid.2014.371
Fusar-poli P, Placentino A, Carletti F et al (2009) Laterality effect on emotional faces processing: ALE meta-analysis of evidence. Neurosci Lett 452:262–267. https://doi.org/10.1016/j.neulet.2009.01.065
Grecucci A, Giorgetta C, Bonini N, Sanfey AG (2013) Reappraising social emotions: the role of inferior frontal gyrus, temporo-parietal junction and insula in interpersonal emotion regulation. Front Hum Neurosci 7:1–12. https://doi.org/10.3389/fnhum.2013.00523
Gu X, Han S (2007) Attention and reality constraints on the neural processes of empathy for pain. Neuroimage 36:256–267. https://doi.org/10.1016/j.neuroimage.2007.02.025
Han S, Fan Y, Xu X et al (2009) Empathic neural responses to others’ pain are modulated by emotional contexts. Hum Brain Mapp 30:3227–3237. https://doi.org/10.1002/hbm.20742
Haxby JV, Hoffman EA, Gobbini MI (2000) The distributed human neural system for face perception. Trends Cogn Sci 4:223–233. https://doi.org/10.1016/S1364-6613(00)01482-0
Hoaglin DC, Iglewicz B, Hoaglin DC, Iglewicz B (1987) Fine-tuning some resistant rules for outlier labeling. J Am Stat Assoc 82:1147–1149
Hornstein HA (1972) Promotive tension: the basis of prosocial behavior from a lewinian perspective. J Soc Issues 28:191–218. https://doi.org/10.1111/j.1540-4560.1972.tb00039.x
Ishai A (2007) Sex, beauty and the orbitofrontal cortex. Int J Psychophysiol 63:181–185. https://doi.org/10.1016/j.ijpsycho.2006.03.010
Ishizu T, Zeki S (2013) The brain’s specialized systems for aesthetic and perceptual judgment. Eur J Neurosci 37:1413–1420. https://doi.org/10.1111/ejn.12135
Jackson PL, Meltzoff AN, Decety J (2005) How do we perceive the pain of others? A window into the neural processes involved in empathy. Neuroimage 24:771–779. https://doi.org/10.1016/j.neuroimage.2004.09.006
Jankowiak-Siuda K, Rymarczyk K, Żurawski Ł et al (2015) Physical attractiveness and sex as modulatory factors of empathic brain responses to pain. Front Behav Neurosci 9:1–11. https://doi.org/10.3389/fnbeh.2015.00236
Johnson JD, Simmons CH, Jordav A et al (2002) Rodney King and O.J. Revisited: the impact of race and defendant empathy induction on judicial decisions. J Appl Soc Psychol 32:1208–1223. https://doi.org/10.1111/j.1559-1816.2002.tb01432.x
Junghöfer M, Bradley MM, Elbert TR, Lang PJ (2001) Fleeting images: a new look at early emotion discrimination. Psychophysiology 38:175–178. https://doi.org/10.1017/S0048577201000762
Kirsch LP, Urgesi C, Cross ES (2016) Neuroscience and biobehavioral reviews shaping and reshaping the aesthetic brain: emerging perspectives on the neurobiology of embodied aesthetics. Neurosci Biobehav Rev 62:56–68. https://doi.org/10.1016/j.neubiorev.2015.12.005
Lamm C, Singer T (2010) The role of anterior insular cortex in social emotions. Brain Struct Funct 214:579–591. https://doi.org/10.1007/s00429-010-0251-3
Liang X, Zebrowitz LA, Zhang Y (2010) Neural activation in the “reward circuit” shows a nonlinear response to facial attractiveness. Soc Neurosci 5:320–334. https://doi.org/10.1080/17470911003619916
Ma DS, Correll J, Wittenbrink B (2015) The Chicago face database: a free stimulus set of faces and norming data. Behav Res Methods 47:1122–1135. https://doi.org/10.3758/s13428-014-0532-5
Martin-Loeches M, Hernandez-Tamames JA, Martin A, Urrutia M (2014) Beauty and ugliness in the bodies and faces of others: an fMRI study of person esthetic judgement. Neuroscience 277:486–497
Mehrabian A, Blum JS (1997) Physical appearance, attractiveness, and the mediating role of emotions. Curr Psychol 16:20–42. https://doi.org/10.4324/9781351309561-1
Mehrabian A, Epstein N (1972) A measure of emotional empathy. J Pers 40:525–543
Morita Y, Morita K, Yamamoto M et al (2001) Effects of facial affect recognition on the auditory P300 in healthy subjects. Neurosci Res 41:89–95. https://doi.org/10.1016/S0168-0102(01)00248-6
O’Doherty J, Winston J, Critchley H et al (2003) Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness. Neuropsychologia 41:147–155. https://doi.org/10.1016/S0028-3932(02)00145-8
Preston SD, de Waal FBM (2002) Empathy: its ultimate and proximate bases. Behav Brain Sci 25:1–72. https://doi.org/10.1017/S0140525X02000018
Rhodes GI, Jeffery L, Watson TL et al (2003) Face attractiveness aftereffects: fitting the mind to the world. Psychol Sci 14:558–566. https://doi.org/10.1167/3.9.298
Saarela MV, Hlushchuk Y, Williams ACDC et al (2007) The compassionate brain: humans detect intensity of pain from another’s face. Cereb Cortex 17:230–237. https://doi.org/10.1093/cercor/bhj141
Saxe R, Kanwisher N (2003) People thinking about thinking people: the role of the temporo-parietal junction in “theory of mind”. Neuroimage 19:1835–1842. https://doi.org/10.1016/S1053-8119(03)00230-1
Schwartz GE, Davidson RJ, Maer F (1975) Right hemisphere lateralization for emotion in the human brain: Interactions with cognition. Science (–80) 190:286–288. https://doi.org/10.1126/science.1179210
Shamay-tsoory S (2015) The neuropsychology of empathy: evidence from lesion studies. Rev Neuropsychol 7:237–243. https://doi.org/10.1684/nrp.2015.0356
Sheng F, Han S (2012) Manipulations of cognitive strategies and intergroup relationships reduce the racial bias in empathic neural responses. Neuroimage 61:786–797. https://doi.org/10.1016/j.neuroimage.2012.04.028
Simon D, Craig KD, Miltner WHR, Rainville P (2006) Brain responses to dynamic facial expressions of pain. Pain 126:309–318. https://doi.org/10.1016/j.pain.2006.08.033
Singer T, Seymour B, O’Doherty J et al (2004) Empathy for pain involves the affective but not sensory components of pain. Science 80(303):1157–1162. https://doi.org/10.1126/science.1093535
Singer T, Seymour B, O’Doherty JP et al (2006) Empathic neural responses are modulated by the perceived fairness of others. Nature 439:466–469. https://doi.org/10.1038/nature04271
Van Overwalle F (2009) Social cognition and the brain: a meta-analysis. Hum Brain Mapp 30:829–858. https://doi.org/10.1002/hbm.20547
Wedding D, Stalans L (1985) Hemispheric differences in the perception of positive and negative faces. Int J Neurosci 27:277–281
Xu X, Zuo X, Wang X, Han S (2009) Do you feel my pain? Racial group membership modulates empathic neural responses. J Neurosci 29:8525–8529. https://doi.org/10.1523/JNEUROSCI.2418-09.2009
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Additional information
Communicated by Melvyn A. Goodale.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Balconi, M., Kopis, N. & Angioletti, L. Does aesthetic judgment on face attractiveness affect neural correlates of empathy for pain? A fNIRS study. Exp Brain Res 238, 2067–2076 (2020). https://doi.org/10.1007/s00221-020-05867-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-020-05867-y