The impact of fear of pain on the temporal processing of emotional faces: modulation of attentional resources.

Ahead of Print

Publisher: Springer Verlag Country of Publication: Germany NLM ID: 101177984 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1612-4790 (Electronic) Linking ISSN: 16124782 NLM ISO Abbreviation: Cogn Process Subsets: MEDLINE

Publication: <2004->: Heidelburg : Springer Verlag
Original Publication: Lengerich : Pabst Science, 2000-

Recent research has focused on the spatial attention bias toward pain-related cues in individuals with fear of pain (FOP), but our understanding of its temporal attention features, particularly regarding emotional faces, is limited. To address this gap, 39 individuals with high fear of pain (H-FOP) and 37 with low fear of pain (L-FOP) completed a rapid serial visual presentation dual task. Participants viewed a series of rapidly presented pictures, first identified neutral building images as the first target (T1) and then emotional faces (painful, neutral, and happy) as the second target (T2). T1 and T2 presented at time intervals of 232 ms (lag 2) and 696 ms (lag 6), respectively. Results indicate that H-FOP group members were less accurate in recognizing faces at lag 2 shortly after correctly identifying T1 compared to those L-FOP group members. Notably, all participants were more accurate in recognizing painful faces at lag 2 than in identifying neutral and happy faces, suggesting a negative bias toward pain stimuli when attentional resources were limited. In contrast, at lag 6, when attentional resources were more abundant, participants showed greater accuracy in recognizing neutral faces than emotional faces. These findings underscore the influence of fear of pain and available cognitive resources on the attentional processing of emotional faces over time, providing insights into how fear of pain affects the temporal dynamics of emotional face recognition and the role of attentional resources.
(© 2024. The Author(s), under exclusive licence to Marta Olivetti Belardinelli.)

Anderson A, Britton K (2019) On the automaticity of attentional orienting to threatening stimuli. Emotion 20(6):1190.
Bar-Haim Y, Lamy D, Pergamin L, Bakermans-Kranenburg M, van Ijzendoorn M (2007) Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study. Psychol Bull 133(1):1–24. (PMID: 1720156810.1037/0033-2909.133.1.1)
Barnhart W, Buelow M, Trost Z (2019) Effects of acute pain and pain-related fear on risky decision-making and effort during cognitive tests. J Clin Exp Neuropsychol 41(10):1033–1047. (PMID: 3136627510.1080/13803395.2019.1646711)
Baum C, Schneider R, Keogh E, Lautenbacher S (2013) Different stages in attentional processing of facial expressions of pain: a dot-probe task modification. J Pain 14(3):223–232. (PMID: 2329499610.1016/j.jpain.2012.11.001)
Belopolsky V, Devue C, Theeuwes J (2011) Angry faces hold the eyes. Vis Cogn 19(1):27–36. https://doi.org/10.1080/13506285.2010.536186. (PMID: 10.1080/13506285.2010.536186)
Bushnell M, Čeko M, Low L (2013) Cognitive and emotional control of pain and its disruption in chronic pain. Nat Rev Neurosci 14(7):502–511. (PMID: 23719569446535110.1038/nrn3516)
Carleton R, Park I, Asmundson GJ (2006) The illness/injury sensitivity index: an examination of construct validity. Depress Anxiety 23(6):340–346. (PMID: 1668873510.1002/da.20138)
Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Routledge, London.
Corti E, Gasson N, Loftus A (2021) Cognitive profile and mild cognitive impairment in people with chronic lower back pain. Brain Cogn 151:105737. (PMID: 3394594010.1016/j.bandc.2021.105737)
Crombez G, Eccleston C, Baeyens F, Eelen P (1998) When somatic information threatens, catastrophic thinking enhances attentional interference. Pain 75(2):187–198. (PMID: 958375410.1016/S0304-3959(97)00219-4)
Crombez G, Eccleston C, Van den Broeck A, Goubert L, Van Houdenhove B (2004) Hypervigilance to pain in fibromyalgia: the mediating role of pain intensity and catastrophic thinking about pain. Clin J Pain 20(2):98–102. (PMID: 1477004910.1097/00002508-200403000-00006)
Crombez G, Van Damme S, Eccleston C (2005) Hypervigilance to pain: an experimental and clinical analysis. Pain 116(1):4–7. (PMID: 1592738710.1016/j.pain.2005.03.035)
De Martino B, Kalisch R, Rees G, Dolan R (2009) Enhanced processing of threat stimuli under limited attentional resources. Cereb Cortex 19(1):127–133. (PMID: 1844845310.1093/cercor/bhn062)
Dux P, Marois R (2009) The attentional blink: a review of data and theory. Atten Percept Psychophys 71(8):1683–1700. (PMID: 19933555291590410.3758/APP.71.8.1683)
Faul F, Erdfelder E, Buchner A, Lang A-G (2009) Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behav Res Methods 41(4):1149–1160. (PMID: 1989782310.3758/BRM.41.4.1149)
Fox E, Russo R, Georgiou G (2005) Anxiety modulates the degree of attentive resources required to process emotional faces. Cogn Affect Behav Neurosci 5(4):396–404. (PMID: 16541810190337310.3758/CABN.5.4.396)
Fritz J, George S, Delitto A (2001) The role of fear-avoidance beliefs in acute low back pain: relationships with current and future disability and work status. Pain 94(1):7–15. (PMID: 1157674010.1016/S0304-3959(01)00333-5)
Gao X, Deng X, Chen N, Luo W, Hu L, Jackson T, Chen H (2011) Attentional biases among body-dissatisfied young women: an ERP study with rapid serial visual presentation. Int J Psychophysiol 82(2):133–142. (PMID: 2187150310.1016/j.ijpsycho.2011.07.015)
Grynberg D, Maurage P (2014) Pain and empathy: the effect of self-oriented feelings on the detection of painful facial expressions. PLoS ONE 9(7):e100434. (PMID: 24983356407764810.1371/journal.pone.0100434)
Harker K, Klein R, Dick B, Verrier M, Rashiq S (2011) Exploring attentional disruption in fibromyalgia using the attentional blink. Psychol Health 26(7):915–929. (PMID: 2159818710.1080/08870446.2010.525639)
Higgins D, Martin A, Baker D, Vasterling J, Risbrough V (2018) The relationship between chronic pain and neurocognitive function: a systematic review. Clin J Pain 34(3):262–275. (PMID: 28719507577198510.1097/AJP.0000000000000536)
International Association for the Study of Pain (IASP) Pain IASP Taxonomy (2015). Available online: http://www.iasppain.org/Education/Content.aspx?ItemNumber=1698&navItemNumber=576.
Jackson T, Su L, Wang Y (2018) Effects of higher versus lower threat contexts on pain-related visual attention biases: an eye-tracking study of chronic pain. J Pain 19(6):649–659. (PMID: 2945231210.1016/j.jpain.2018.01.011)
Jones S, Walsh J (2021) The disruptive effects of pain on the early allocation of attentional resources: an attentional blink study. Eur J Pain 25(10):2202–2211. (PMID: 3418435310.1002/ejp.1833)
Lee S, Kang Y, Cho S-J (2017) Subjective cognitive decline in patients with migraine and its relationship with depression, anxiety, and sleep quality. J Headache Pain 18(1):77. (PMID: 28744704552682710.1186/s10194-017-0779-1)
Leeuw M, Goossens M, Linton S, Crombez G, Boersma K, Vlaeyen J (2007) The fear-avoidance model of musculoskeletal pain: current state of scientific evidence. J Behav Med 30(1):77–94. (PMID: 1718064010.1007/s10865-006-9085-0)
Ling Y, Yang Z, Jackson T (2019) Visual attention to pain cues for impending touch versus impending pain: an eye tracking study. Eur J Pain 23(8):1527–1537. (PMID: 3111231610.1002/ejp.1428)
Markfelder T, Pauli P (2020) Fear of pain and pain intensity: meta-analysis and systematic review. Psychol Bull 146:411–450. (PMID: 3221274510.1037/bul0000228)
Martens S, Wyble B (2010) The attentional blink: past, present, and future of a blind spot in perceptual awareness. Neurosci Biobehav Rev 34(6):947–957. (PMID: 2002590210.1016/j.neubiorev.2009.12.005)
Martinez-Calderon J, Flores-Cortes M, Morales-Asencio JM, Luque-Suarez A (2019) Pain-related fear, pain intensity and function in individuals with chronic musculoskeletal pain: a systematic review and meta-analysis. J Pain 20(12):1394–1415. (PMID: 3106387410.1016/j.jpain.2019.04.009)
McNeil D, Rainwater A (1998) Development of the fear of pain questionnaire-III. J Behav Med 21(4):389–410. (PMID: 978916810.1023/A:1018782831217)
Mishra M, Ray S, Srinivasan N (2017) Effect of emotions on temporal attention. Prog Brain Res 236:287–309. (PMID: 2915741710.1016/bs.pbr.2017.08.014)
Moriarty O, McGuire BE, Finn DP (2011) The effect of pain on cognitive function: a review of clinical and preclinical research. Prog Neurobiol 93(3):385–404. (PMID: 2121627210.1016/j.pneurobio.2011.01.002)
Öhman A (2005) The role of the amygdala in human fear: automatic detection of threat. Psychoneuroendocrinology 30(10):953–958. (PMID: 1596365010.1016/j.psyneuen.2005.03.019)
Pedale T, Basso D, Santangelo V (2017) Processing of negative stimuli facilitates event-based prospective memory only under low memory load. J Cogn Psychol 29(8):920–928. https://doi.org/10.1080/20445911.2017.1329204. (PMID: 10.1080/20445911.2017.1329204)
Pessoa L, Japee S, Ungerleider G (2005) Visual awareness and the detection of fearful faces. Emotion 5(2):243–247. https://doi.org/10.1037/1528-3542.5.2.243. (PMID: 10.1037/1528-3542.5.2.24315982091)
Peters ML, Vlaeyen JWS, Kunnen AMW (2002) Is pain-related fear a predictor of somatosensory hypervigilance in chronic low back pain patients? Behav Res Ther 40(1):85–103. (PMID: 1176476110.1016/S0005-7967(01)00005-5)
Raymond JE, Shapiro KL, Arnell KM (1992) Temporary suppression of visual processing in an RSVP task: an attentional blink? J Exp Psychol Hum Percept Perform 18:849–860. (PMID: 150088010.1037/0096-1523.18.3.849)
Rogers AH, Farris SG (2022) A meta-analysis of the associations of elements of the fear-avoidance model of chronic pain with negative affect, depression, anxiety, pain-related disability and pain intensity. Eur J Pain 26(8):1611–1635. (PMID: 35727200954189810.1002/ejp.1994)
Scherer KR (2001) Appraisal considered as a process of multilevel sequential checking. Appraisal processes in emotion: theory, methods, research. Oxford University Press, New York, pp 92–120. (PMID: 10.1093/oso/9780195130072.003.0005)
Schmidt LJ, Belopolsky AV, Theeuwes J (2015) Potential threat attracts attention and interferes with voluntary saccades. Emotion 15(3):329–338. https://doi.org/10.1037/emo0000041. (PMID: 10.1037/emo000004125527964)
Shafer AT, Matveychuk D, Penney T, O’Hare AJ, Stokes J, Dolcos F (2012) Processing of emotional distraction is both automatic and modulated by attention: evidence from an event-related fMRI investigation. J Cogn Neurosci 24(5):1233–1252. https://doi.org/10.1162/jocn_a_00206. (PMID: 10.1162/jocn_a_00206223328054491634)
Sharpe L, Brookes M, Jones E, Gittins C, Wufong E, Nicholas MK (2017) Threat and fear of pain induces attentional bias to pain words: an eye-tracking study. Eur J Pain 21(2):385–396. (PMID: 2777468010.1002/ejp.936)
Suhr J, Spickard B (2012) Pain-related fear is associated with cognitive task avoidance: exploration of the cogniphobia construct in a recurrent headache sample. Clin Neuropsychol 26(7):1128–1141. (PMID: 2292864310.1080/13854046.2012.713121)
Sun M, Liu F, Cui L, Wei P, Zhang Q (2021) The effect of fearful faces on the attentional blink is modulated by emotional task relevance: an event-related potential study. Neuropsychologia 162:108043. (PMID: 3460089210.1016/j.neuropsychologia.2021.108043)
Tesio V, Torta DM, Colonna F, Leombruni P, Ghiggia A, Fusaro E, Castelli L (2015) Are fibromyalgia patients cognitively impaired? Objective and subjective neuropsychological evidence. Arthritis Care Res 67(1):143–150. (PMID: 10.1002/acr.22403)
Thomas JS, France CR (2007) Pain-related fear is associated with avoidance of spinal motion during recovery from low back pain. Spine 32(16):E460–E466. (PMID: 1763238510.1097/BRS.0b013e3180bc1f7b)
Trippe RH, Hewig J, Heydel C, Hecht H, Miltner W (2007) Attentional blink to emotional and threatening pictures in spider phobics: electrophysiology and behavior. Brain Res 1148:149–160. (PMID: 1736776510.1016/j.brainres.2007.02.035)
Van Damme S, Crombez G, Eccleston C (2002) Retarded disengagement from pain cues: the effects of pain catastrophizing and pain expectancy. Pain 100(1):111–118. (PMID: 1243546410.1016/S0304-3959(02)00290-7)
Van Damme S, Crombez G, Eccleston C (2004) Disengagement from pain: the role of catastrophic thinking about pain. Pain 107(1):70–76. (PMID: 1471539110.1016/j.pain.2003.09.023)
Vermeulen N, Godefroid J, Mermillod M (2009) Emotional modulation of attention: fear increases but disgust reduces the attentional blink. PLoS ONE 4(11):e7924. (PMID: 19936235277563010.1371/journal.pone.0007924)
Vlaeyen JWS, Linton SJ (2000) Fear-avoidance and its consequences in chronic musculoskeletal pain: a state of the art. Pain 85(3):317–332. (PMID: 1078190610.1016/S0304-3959(99)00242-0)
Vuilleumier P, Armony JL, Driver J, Dolan RJ (2001) Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron 30(3):829–841. (PMID: 1143081510.1016/S0896-6273(01)00328-2)
Yang Z, Bateer, (2020) Identifying pain perceptual biases related to fear of pain and threat in a pain-free sample. Eur J Pain 24(6):1084–1093. (PMID: 3213370510.1002/ejp.1553)
Yang Z, Jackson T, Gao X, Chen H (2012) Identifying selective visual attention biases related to fear of pain by tracking eye movements within a dot-probe paradigm. Pain 153(8):1742–1748. (PMID: 2271710110.1016/j.pain.2012.05.011)
Zale EL, Lange KL, Fields SA, Ditre JW (2013) The relation between pain-related fear and disability: a meta-analysis. J Pain 14(10):1019–1030. (PMID: 23850095379116710.1016/j.jpain.2013.05.005)
Zheng C, Wang J-Y, Luo F (2015) Painful faces-induced attentional blink modulated by top–down and bottom–up mechanisms. PLoS ONE 6:695.
Zheng P, Lyu Z, Jackson T (2018) Fear of pain and event-related potentials during exposure to image-cued somatosensory stimulation. Brain Res 1695:91–101. (PMID: 2985213710.1016/j.brainres.2018.05.042)
Zheng P, Lyu Z, Jackson T (2019) Effects of trait fear of pain on event-related potentials during word cue presentations that signal potential pain. Eur J Neurosci 50(8):3365–3379. (PMID: 3122037710.1111/ejn.14495)
Zivony A, Lamy D (2022) What processes are disrupted during the attentional blink? An integrative review of event-related potential research. Psychon Bull Rev 29(2):394–414. (PMID: 3429143010.3758/s13423-021-01973-2)

B/2021/01/65 Education Science Planning Project of Jiangsu Province

Keywords: Attentional blink; Attentional resources; Emotional faces; Fear of pain; Rapid serial visual presentation

Date Created: 20241105 Latest Revision: 20241105

20241106

10.1007/s10339-024-01243-8

39499392