BACKGROUND: Maladaptive behaviors and interpersonal difficulties in patients with borderline personality disorder (BPD) seem connected to biased facial emotion processing. This bias is often accompanied by heightened amygdala activity in patients with BPD as compared to healthy controls. However, functional magnetic resonance imaging (fMRI) studies exploring differences between patients and healthy controls in facial emotion processing have produced divergent results. The current study explored fMRI and heart rate variability (HRV) correlates of negative facial emotion processing in patients with BPD and healthy controls. METHODS: The study included 30 patients with BPD (29 females; age: M = 24.22, SD = 5.22) and 30 healthy controls (29 females; M = 24.66, SD = 5.28). All participants underwent the "faces" task, an emotional face perception task, in an fMRI session simultaneously with ECG. In this task, participants are presented with emotional expressions of disgust, sadness, and fear (as a negative condition) and with the same pictures in a scrambled version (as a neutral condition). RESULTS: We found no differences in brain activity between patients with BPD and healthy controls when processing negative facial expressions as compared to neutral condition. We observed activation in large-scale brain areas in both groups when presented with negative facial expressions as compared to neutral condition. Patients with BPD displayed lower HRV than healthy controls in both conditions. However, there were no significant associations between HRV and amygdala activity and BPD symptoms. CONCLUSION: The results of this study indicate no abnormal brain activity during emotional facial processing in patients with BPD. This result contrasts with previous studies and more studies are needed to clarify the relationship between facial emotion processing and brain activity in patients with BPD. Possible reasons for the absence of brain activity differences are discussed in the study. Consistent with previous findings, patients showed lower HRV than healthy controls. However, HRV was not associated with amygdala activity and BPD symptoms.

Brain and Mind Research Program Central European Institute of Technology Masaryk University Brno Czech Republic

Department of Psychiatry University Hospital Brno and Faculty of Medicine Masaryk University Jihlavská 340 20 Brno 625 00 Czech Republic

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Bertsch K, Hillmann K, Herpertz SC. Behavioral and neurobiological correlates of disturbed emotion processing in borderline personality disorder. Psychopathology. 2018;51:76–82. doi: 10.1159/000487363. PubMed DOI

Sanislow CA, Grilo CM, Morey LC, Bender DS, Skodol AE, Gunderson JG, et al. Confirmatory factor analysis of DSM-IV criteria for borderline personality disorder: findings from the collaborative longitudinal personality disorders study. Am J Psychiatr. 2002;159:284–290. doi: 10.1176/appi.ajp.159.2.284. PubMed DOI

Putnam KM, Silk KR. Emotion dysregulation and the development of borderline personality disorder. Dev Psychopathol. 2005;17:899–925. doi: 10.1017/S0954579405050431. PubMed DOI

Blair RJR. Facial expressions, their communicatory functions and neuro-cognitive substrates. Philos Trans R Soc Lond, B, Biol Sci. 2003;358:561–572. doi: 10.1098/rstb.2002.1220. PubMed DOI PMC

Mitchell AE, Dickens GL, Picchioni MM. Facial emotion processing in borderline personality disorder: a systematic review and meta-analysis. Neuropsychol Rev. 2014;24:166–184. doi: 10.1007/s11065-014-9254-9. PubMed DOI

Unoka Z, Fogd D, Füzy M, Csukly G. Misreading the facial signs: specific impairments and error patterns in recognition of facial emotions with negative valence in borderline personality disorder. Psychiatry Res. 2011;189:419–425. doi: 10.1016/j.psychres.2011.02.010. PubMed DOI

Bland AR, Williams CA, Scharer K, Manning S. Emotion processing in borderline personality disorders. Issues Ment Health Nurs. 2004;25:655–672. doi: 10.1080/01612840490486692. PubMed DOI

Guitart-Masip M, Pascual JC, Carmona S, Hoekzema E, Bergé D, Pérez V, et al. Neural correlates of impaired emotional discrimination in borderline personality disorder: an fMRI study. Prog Neuro-Psychopharmacol Biol Psychiatry. 2009;33:1537–1545. doi: 10.1016/j.pnpbp.2009.08.022. PubMed DOI

Domes G, Grabe HJ, Czieschnek D, Heinrichs M, Herpertz SC. Alexithymic traits and facial emotion recognition in borderline personality disorder. Psychother Psychosom. 2011;80:383–385. doi: 10.1159/000325828. PubMed DOI

Dyck M, Habel U, Slodczyk J, Schlummer J, Backes V, Schneider F, et al. Negative bias in fast emotion discrimination in borderline personality disorder. Psychol Med. 2009;39:855–864. doi: 10.1017/S0033291708004273. PubMed DOI

Minzenberg MJ, Poole JH, Vinogradov S. Adult social attachment disturbance is related to childhood maltreatment and current symptoms in borderline personality disorder. J Nerv Ment Dis. 2006;194:341–348. doi: 10.1097/01.nmd.0000218341.54333.4e. PubMed DOI

Cullen KR, LaRiviere LL, Vizueta N, Thomas KM, Hunt RH, Miller MJ, et al. Brain activation in response to overt and covert fear and happy faces in women with borderline personality disorder. Brain Imaging Behav. 2016;10:319–331. doi: 10.1007/s11682-015-9406-4. PubMed DOI PMC

D’Argembeau A, Van der Linden M. Facial expressions of emotion influence memory for facial identity in an automatic way. Emotion. 2007;7:507–515. doi: 10.1037/1528-3542.7.3.507. PubMed DOI

Vuilleumier P, Pourtois G. Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia. 2007;45:174–194. doi: 10.1016/j.neuropsychologia.2006.06.003. PubMed DOI

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

Schulze L, Schulze A, Renneberg B, Schmahl C, Niedtfeld I. Neural correlates of affective disturbances: a comparative Meta-analysis of negative affect processing in borderline personality disorder, major depressive disorder, and posttraumatic stress disorder. Biol Psychiatry Cogn Neurosci Neuroimaging. 2019;4:220–232. doi: 10.1016/j.bpsc.2018.11.004. PubMed DOI

Wrege JS, Ruocco AC, Carcone D, Lang UE, Lee ACH, Walter M. Facial emotion perception in borderline personality disorder: differential neural activation to ambiguous and threatening expressions and links to impairments in self and interpersonal functioning. J Affect Disord. 2021;284:126–135. doi: 10.1016/j.jad.2021.01.042. PubMed DOI

Lamers A, Toepper M, Fernando SC, Schlosser N, Bauer E, Woermann F, et al. Nonacceptance of negative emotions in women with borderline personality disorder: association with neuroactivity of the dorsal striatum. J Psychiatry Neurosci. 2019;44:303–312. doi: 10.1503/jpn.180077. PubMed DOI PMC

Donegan NH, Sanislow CA, Blumberg HP, Fulbright RK, Lacadie C, Skudlarski P, et al. Amygdala hyperreactivity in borderline personality disorder: implications for emotional dysregulation. Biol Psychiatry. 2003;54:1284–1293. doi: 10.1016/S0006-3223(03)00636-X. PubMed DOI

Minzenberg MJ, Fan J, New AS, Tang CY, Siever LJ. Fronto-limbic dysfunction in response to facial emotion in borderline personality disorder: an event-related fMRI study. Psychiatry Res Neuroimaging. 2007;155:231–243. doi: 10.1016/j.pscychresns.2007.03.006. PubMed DOI PMC

Baskin-Sommers AR, Hooley JM, Dahlgren MK, Gönenc A, Yurgelun-Todd DA, Gruber SA. Elevated Preattentive affective processing in individuals with borderline personality disorder: a preliminary fMRI study. Front Psychol. 2015:6. 10.3389/fpsyg.2015.01866. PubMed PMC

Lamers A, Toepper M, Fernando SC, Schlosser N, Lenz E, Woermann F, et al. Caudate hyperactivation during the processing of happy faces in borderline personality disorder. Neuropsychologia. 2021:163. 10.1016/j.neuropsychologia.2021.108086. PubMed

Ellenbroek BA, Kidwell M, Colussi-Mas J, Youn J. Heart rate variability as a translational biomarker for emotional and cognitive deficits. Handb Behav Neurosci. 2019;29:199–212. doi: 10.1016/B978-0-12-803161-2.00013-8. DOI

Cattaneo LA, Franquillo AC, Grecucci A, Beccia L, Caretti V, Dadomo H. Is low heart rate variability associated with emotional dysregulation, psychopathological dimensions, and prefrontal dysfunctions? An integrative view. J Pers Med. 2021:11. 10.3390/jpm11090872. PubMed PMC

Chang C, Metzger CD, Glover GH, Duyn JH, Heinze HJ, Walter M. Association between heart rate variability and fluctuations in resting-state functional connectivity. Neuroimage. 2013;68:93–104. doi: 10.1016/j.neuroimage.2012.11.038. PubMed DOI PMC

Sakaki M, Yoo HJ, Nga L, Lee TH, Thayer JF, Mather M. Heart rate variability is associated with amygdala functional connectivity with MPFC across younger and older adults. Neuroimage. 2016;139:44–52. doi: 10.1016/j.neuroimage.2016.05.076. PubMed DOI PMC

Mulcahy JS, Larsson DEO, Garfinkel SN, Critchley HD. Heart rate variability as a biomarker in health and affective disorders: a perspective on neuroimaging studies. Neuroimage. 2019:202. 10.1016/j.neuroimage.2019.116072. PubMed

Duggento A, Bianciardi M, Passamonti L, Wald LL, Guerrisi M, Barbieri R, et al. Globally conditioned granger causality in brain-brain and brain-heart interactions: a combined heart rate variability/ultra-high-field (7 T) functional magnetic resonance imaging study. Philos Trans R Soc A Math Phys Eng Sci. 2016:374. 10.1098/rsta.2015.0185. PubMed PMC

Schulz SM. Neural correlates of heart-focused interoception: a functional magnetic resonance imaging meta-analysis. Philos Trans R Soc Lond, B, Biol Sci. 2016:371. 10.1098/rstb.2016.0018. PubMed PMC

Steinfurth ECK, Wendt J, Geisler F, Hamm AO, Thayer JF, Koenig J. Resting state vagally-mediated heart rate variability is associated with neural activity during explicit emotion regulation. Front Neurosci. 2018:12. 10.3389/fnins.2018.00794. PubMed PMC

Miller JG, Xia G, Hastings PD. Resting heart rate variability is negatively associated with mirror neuron and limbic response to emotional faces. Biol Psychol. 2019:146. 10.1016/j.biopsycho.2019.107717. PubMed PMC

Koenig J, Kemp AH, Feeling NR, Thayer JF, Kaess M. Resting state vagal tone in borderline personality disorder: a meta-analysis. Prog Neuro-Psychopharmacol Biol Psychiatry. 2016;64:18–26. doi: 10.1016/j.pnpbp.2015.07.002. PubMed DOI

Koenig J, Rinnewitz L, Parzer P, Resch F, Thayer JF, Kaess M. Resting cardiac function in adolescent non-suicidal self-injury: the impact of borderline personality disorder symptoms and psychosocial functioning. Psychiatry Res. 2017;248:117–120. doi: 10.1016/j.psychres.2016.12.024. PubMed DOI

Wainsztein AE, Abulafia C, Goldberg X, Camacho-Téllez V, Vulcano M, Vigo DE, et al. Diurnal variation of heart rate variability as a physiological index of mood and emotion regulation processes in major depression and borderline personality disorder. Pers Med Psychiatry. 2020;23:100065. doi: 10.1016/j.pmip.2020.100065. DOI

Weise S, Parzer P, Zimmermann R, Fürer L, Resch F, Kaess M, et al. Emotion dysregulation and resting-state autonomic function in adolescent borderline personality disorder-a multimodal assessment approach. Personal Disord Theory Res Treat. 2020;11:46–53. doi: 10.1037/per0000367. PubMed DOI

Maiß C, Engemann L, Kern K, Flasbeck V, Mügge A, Lücke T, et al. Cardiac parasympathetic activity in female patients with borderline personality disorder predicts approach/avoidance behavior towards angry faces. Biol Psychol. 2021:163. 10.1016/j.biopsycho.2021.108146. PubMed

Paret C, Niedtfeld I, Lotter T, Wunder A, Grimm S, Mennes M, et al. Single-dose effects of citalopram on neural responses to affective stimuli in borderline personality disorder: a randomized clinical trial. Biol Psychiatry Cogn Neurosci Neuroimaging. 2021;6:837–845. doi: 10.1016/j.bpsc.2021.02.002. PubMed DOI

Anderson IM, Del-Ben CM, Mckie S, Richardson P, Williams SR, Elliott R, Deakin JW. Citalopram modulation of neuronal responses to aversive face emotions: a functional MRI study. Neuroreport. 2007;18:1351–1355. doi: 10.1097/WNR.0b013e3282742115. PubMed DOI

Bartečků E, Hořínková J, Křenek P, Damborská A, Tomandl J, Tomandlová M, et al. Osteocalcin levels decrease during the treatment of an acute depressive episode. Front Psychiatry. 2022;13:893012. doi: 10.3389/fpsyt.2022.893012. PubMed DOI PMC

Fertuck EA, Karan E, Stanley B. The specificity of mental pain in borderline personality disorder compared to depressive disorders and healthy controls. Borderline Personal Disord Emot Dysregul. 2016:3. 10.1186/s40479-016-0036-2. PubMed PMC

Bridler R, Häberle A, Müller ST, Cattapan K, Grohmann R, Toto S, et al. Psychopharmacological treatment of 2195 in-patients with borderline personality disorder: a comparison with other psychiatric disorders. Eur Neuropsychopharmacol. 2015;25:763–772. doi: 10.1016/j.euroneuro.2015.03.017. PubMed DOI

Stoffers-Winterling J, Storebø OJ, Lieb K. Pharmacotherapy for borderline personality disorder: an update of published, unpublished and ongoing studies. Curr Psychiatry Rep. 2020;22:1–10. doi: 10.1007/s11920-020-01164-1. PubMed DOI PMC

Chandler GM, Iosifescu DV, Pollack MH, Targum SD, Fava M. Validation of the Massachusetts general hospital antidepressant treatment history questionnaire (ATRQ) CNS Neurosci Ther. 2010;16:322–325. doi: 10.1111/j.1755-5949.2009.00102.x. PubMed DOI PMC

Wang S-M, Han C, Lee S-J, Jun T-Y, Patkar AA, Masand PS, et al. Second generation antipsychotics in the treatment of major depressive disorder: an update. Chonnam Med J. 2016;52:159. doi: 10.4068/cmj.2016.52.3.159. PubMed DOI PMC

Látalová A, Radimecká M, Lamoš M, Jáni M, Damborská A, Theiner P, et al. Neural correlates of social exclusion and overinclusion in patients with borderline personality disorder: an fMRI study. Borderline Personal Disord Emot Dysregul. 2023:10. 10.1186/s40479-023-00240-1. PubMed PMC

First MB, Williams JB, Benjamin LS, Spitzer RL. Structured clinical interview for DSM-5 personality disorders: SCID-5-PD. Washington: American Psychiatric Association Publishing; 2016.

Bohus M, Limberger MF, Frank U, Chapman AL, Kühler T, Stieglitz R-D. Psychometric properties of the borderline symptom list (BSL) Psychopathology. 2007;40:126–132. doi: 10.1159/000098493. PubMed DOI

Radimecká M, Jeřábková P, Látalová A, Linhartová P. Psychometric properties of the Czech version of borderline symptom list 23 (BSL-23) Psychoterapie. 2022;16:85–101.

Kaufman EA, Xia M, Fosco G, Yaptangco M, Skidmore CR, Crowell SE. The difficulties in emotion regulation scale short form (DERS-SF): validation and replication in adolescent and adult samples. J Psychopathol Behav Assess. 2016;38:443–455. doi: 10.1007/s10862-015-9529-3. DOI

Benda J. Krátká forma škály potíží v regulaci emocí: pilotní studie české verze. E-psychologie. 2017;11:1–15.

Berenson KR, Gyurak A, Downey G, Ayduk O, Bradley K. Instrument title: rejection sensitivity RS-adult questionnaire (A-RSQ). Measurement instrument database for the social science 2013.

Briere J, Weathers FW, Runtz M. Is dissociation a multidimensional construct? Data from the multiscale dissociation inventory. J Trauma Stress. 2005;18:221–231. doi: 10.1002/jts.20024. PubMed DOI

Bernstein DP, Fink L, Handelsman L, Foote J, Lovejoy M, Wenzel K, et al. Initial reliability and validity of a new retrospective measure of child abuse and neglect. Am J Psychiatry. 1994;151:1132–1136. doi: 10.1176/ajp.151.8.1132. PubMed DOI

Kascakova N, Furstova J, Šolcová IP. Psychometric analysis of the Czech version of childhood trauma questionnaire (CTQ) with the sociodemografic differences in traumatization of Czech adults. Ceskoslovenska Psychologie. 2018;62(212):30.

Kundu P, Voon V, Balchandani P, Lombardo MV, Poser BA, Bandettini PA. Multi-echo fMRI: a review of applications in fMRI denoising and analysis of BOLD signals. Neuroimage. 2017;154:59–80. doi: 10.1016/j.neuroimage.2017.03.033. PubMed DOI

Allen PJ, Josephs O, Turner R. A method for removing imaging artifact from continuous EEG recorded during functional MRI. Neuroimage. 2000;12:230–239. doi: 10.1006/nimg.2000.0599. PubMed DOI

Corp IBM. IBM SPSS statistics for windows. Armonk, NY: IBM Corp; 2017.

Glover GH, Li TQ, Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn Reson Med. 2000;44:162–167. doi: 10.1002/1522-2594(200007)44:1<162::aid-mrm233.0.co;2-e. PubMed DOI

Kovářová A, Gajdoš M, Rektor I, Mikl M. Contribution of the multi-echo approach in accelerated functional magnetic resonance imaging multiband acquisition. Hum Brain Mapp. 2022;43:955–973. doi: 10.1002/hbm.25698. PubMed DOI PMC

Poser BA, Versluis MJ, Hoogduin JM, Norris DG. BOLD contrast sensitivity enhancement and artifact reduction with multiecho EPI: parallel-acquired inhomogeneity-desensitized fMRI. Magn Reson Med. 2006;55:1227–1235. doi: 10.1002/mrm.20900. PubMed DOI

Gajdoš M, Mikl M, Mareček R. Mask_explorer: a tool for exploring brain masks in fMRI group analysis. Comput Methods Prog Biomed. 2016;134:155–163. doi: 10.1016/j.cmpb.2016.07.015. PubMed DOI

Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage. 2012;59:2142–2154. doi: 10.1016/j.neuroimage.2011.10.018. PubMed DOI PMC

MATLAB . R2021a. Natick, Massachusetts: The MathWorks Inc.; 2021.

xjView. https://www.alivelearn.net/xjview. Accessed 20 July 2023.

Peters AC, Blechert J, Sämann PG, Eidner I, Czisch M, Spoormaker VI. One night of partial sleep deprivation affects habituation of hypothalamus and skin conductance responses. J Neurophysiol. 2014;112:1267–1276. doi: 10.1152/jn.00657.2013.-Sleep. PubMed DOI

BrainVision analyzer (version 2). Gilching, Germany: Brain Products GmbH; 2021. Accessed 16 August 2023.

Bilek E, Itz ML, Stößel G, Ma R, Berhe O, Clement L, et al. Deficient amygdala habituation to threatening stimuli in borderline personality disorder relates to adverse childhood experiences. Biol Psychiatry. 2019;86:930–938. doi: 10.1016/j.biopsych.2019.06.008. PubMed DOI

Goldstein KE, Feinberg A, Corniquel MB, Szeszko JR, et al. Anomalous amygdala habituation to unpleasant stimuli among unmedicated individuals with borderline personality disorder and a history of self-harming behavior. J Personal Disord. 2021;35:618–631. doi: 10.1521/pedi_2020_34_495. PubMed DOI

Radaelli D, Poletti S, Dallaspezia S, Colombo C, Smeraldi E, Benedetti F. Neural responses to emotional stimuli in comorbid borderline personality disorder and bipolar depression. Psychiatry Res Neuroimaging. 2012;203:61–66. doi: 10.1016/j.pscychresns.2011.09.010. PubMed DOI

Frick C, Lang S, Kotchoubey B, Sieswerda S, Dinu-Biringer R, Berger M, et al. Hypersensitivity in borderline personality disorder during mindreading. PLoS One. 2012;7:e41650. doi: 10.1371/journal.pone.0041650. PubMed DOI PMC

Mier D, Lis S, Esslinger C, Sauer C, Hagenhoff M, Ulferts J, et al. Neuronal correlates of social cognition in borderline personality disorder. Soc Cogn Affect Neurosci. 2013;8:531–537. doi: 10.1093/scan/nss028. PubMed DOI PMC

Schulze L, Schmahl C, Niedtfeld I. Neural correlates of disturbed emotion processing in borderline personality disorder: a multimodal Meta-analysis. Biol Psychiatry. 2016;79:97–106. doi: 10.1016/j.biopsych.2015.03.027. PubMed DOI

Krause-Utz A, Walther J-C, Lis S, Schmahl C, Bohus M. Heart rate variability during a cognitive reappraisal task in female patients with borderline personality disorder: the role of comorbid posttraumatic stress disorder and dissociation. Psychol Med. 2019;49:1810–1821. doi: 10.1017/S0033291718002489. PubMed DOI PMC

Krause-Utz A, Walther JC, Kyrgiou AI, Hoogenboom W, Alampanou M, Bohus M, et al. Severity of childhood maltreatment predicts reaction times and heart rate variability during an emotional working memory task in borderline personality disorder. Eur J Psychotraumatol. 2022:13. 10.1080/20008198.2022.2093037. PubMed PMC

Khalili-Mahani N, Chang C, van Osch MJ, Veer IM, van Buchem MA, Dahan A, et al. The impact of “physiological correction” on functional connectivity analysis of pharmacological resting state fMRI. Neuroimage. 2013;65:499–510. doi: 10.1016/j.neuroimage.2012.09.044. PubMed DOI