Brain Structural Correlates of Emotion Recognition in Psychopaths

Vanessa Pera-Guardiola, Oren Contreras-Rodríguez, Iolanda Batalla, David Kosson, José M Menchón, Josep Pifarré, Javier Bosque, Narcís Cardoner, Carles Soriano-Mas, Vanessa Pera-Guardiola, Oren Contreras-Rodríguez, Iolanda Batalla, David Kosson, José M Menchón, Josep Pifarré, Javier Bosque, Narcís Cardoner, Carles Soriano-Mas

Abstract

Individuals with psychopathy present deficits in the recognition of facial emotional expressions. However, the nature and extent of these alterations are not fully understood. Furthermore, available data on the functional neural correlates of emotional face recognition deficits in adult psychopaths have provided mixed results. In this context, emotional face morphing tasks may be suitable for clarifying mild and emotion-specific impairments in psychopaths. Likewise, studies exploring corresponding anatomical correlates may be useful for disentangling available neurofunctional evidence based on the alleged neurodevelopmental roots of psychopathic traits. We used Voxel-Based Morphometry and a morphed emotional face expression recognition task to evaluate the relationship between regional gray matter (GM) volumes and facial emotion recognition deficits in male psychopaths. In comparison to male healthy controls, psychopaths showed deficits in the recognition of sad, happy and fear emotional expressions. In subsequent brain imaging analyses psychopaths with better recognition of facial emotional expressions showed higher volume in the prefrontal cortex (orbitofrontal, inferior frontal and dorsomedial prefrontal cortices), somatosensory cortex, anterior insula, cingulate cortex and the posterior lobe of the cerebellum. Amygdala and temporal lobe volumes contributed to better emotional face recognition in controls only. These findings provide evidence suggesting that variability in brain morphometry plays a role in accounting for psychopaths' impaired ability to recognize emotional face expressions, and may have implications for comprehensively characterizing the empathy and social cognition dysfunctions typically observed in this population of subjects.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. The specific contribution of regional…
Fig 1. The specific contribution of regional GM volumes in the dorsomedial prefrontal cortex (MNI coordinates, x = 17, y = 43, z = 33) to improved sadness recognition in psychopaths was explained by a negative association in this group (red) but a positive association in controls subjects (green).
The plot displays residual values once covariates were controlled for. The sagittal display corresponds to the right hemisphere.
Fig 2
Fig 2
(A) The specific contribution of regional GM volumes in the anterior insula, middle anterior cingulate cortex, orbitofrontal cortex and inferior frontal cortex (Table 3) to improved happiness recognition in psychopaths was explained by a negative association in this group (red) but a positive association in controls subjects (green). (B) Conversely, the specific contribution of regional GM volumes in the amygdalae (Table 3) to improved happiness recognition in control subjects was explained by a negative association in this group (green) but a positive association in psychopaths (red). The plot displays residual values once covariates were controlled for. Images are displayed in neurological convention, therefore the right hemisphere corresponds to the right side in axial and coronal displays. The sagittal display corresponds to the right hemisphere.
Fig 3
Fig 3
(A) The specific contribution of regional GM volumes in the somatosensory cortex (MNI coordinates, x = -26, y = -29, z = 63) to improved fear recognition in psychopaths was explained by a negative association in this group (red) but a positive association in the control subjects (green). (B) Conversely, the specific contribution of regional GM volumes in the temporal cortex (MNI coordinates, x = -48, y = -42, z = 12) to improved fear recognition in controls subjects was explained by a negative association in this group (green) but a positive association in psychopaths (red). Plots display residual values once covariates were controlled for. The sagittal displays correspond to the left hemisphere.

References

    1. Hare RD. The Hare Psychopathy Checklist-Revised. 2nd ed Toronto, Ontario, Canada: Multi-Health Systems; 2003.
    1. Brook M, Brieman CL, Kosson DS. Emotion processing in Psychopathy Checklist-assessed psychopathy: a review of the literature. Clin Psychol Rev. 2013;33: 979–95. 10.1016/j.cpr.2013.07.008
    1. Blair RJR. Responding to the emotions of others: dissociating forms of empathy through the study of typical and psychiatric populations. Conscious Cogn. 2005;14: 698–718. 10.1016/j.concog.2005.06.004
    1. van Honk J, Schutter DJLG. Unmasking feigned sanity: a neurobiological model of emotion processing in primary psychopathy. Cogn Neuropsychiatry. 2006;11: 285–306. 10.1080/13546800500233728
    1. Marsh AA, Blair RJR. Deficits in facial affect recognition among antisocial populations: A meta-analysis. Neurosci Biobehav Rev. 2008;32: 454–465. 10.1016/j.neubiorev.2007.08.003
    1. Dawel A, O’Kearney R, McKone E, Palermo R. Not just fear and sadness: meta-analytic evidence of pervasive emotion recognition deficits for facial and vocal expressions in psychopathy. Neurosci Biobehav Rev. 2012;36: 2288–304. 10.1016/j.neubiorev.2012.08.006
    1. Glass SJ, Newman JP. Recognition of facial affect in psychopathic offenders. J Abnorm Psychol. 2006;115: 815–20. 10.1037/0021-843X.115.4.815
    1. Book A, Quinsey V, Langford D. Psychopathy and the perception of affect and vulnerability. Crim Justice Behav. 2007;34: 531–544.
    1. Sadeh N, Verona E. Visual complexity attenuates emotional processing in psychopathy: implications for fear-potentiated startle deficits. Cogn Affect Behav Neurosci. 2012;12: 346–60. 10.3758/s13415-011-0079-1
    1. Baskin-Sommers AR, Curtin JJ, Newman JP. Emotion-modulated startle in psychopathy: clarifying familiar effects. J Abnorm Psychol. 2013;122: 458–68. 10.1037/a0030958
    1. Deeley Q, Daly E, Surguladze S, Tunstall N, Mezey G, Beer D, et al. Facial emotion processing in criminal psychopathy. Preliminary functional magnetic resonance imaging study. Br J Psychiatry. 2006;189: 533–9. 10.1192/bjp.bp.106.021410
    1. Decety J, Skelly L, Yoder KJ, Kiehl KA. Neural processing of dynamic emotional facial expressions in psychopaths. Soc Neurosci. 2014;9: 36–49. 10.1080/17470919.2013.866905
    1. Contreras-Rodríguez O, Pujol J, Batalla I, Harrison BJ, Bosque J, Ibern-Regàs I, et al. Disrupted neural processing of emotional faces in psychopathy. Soc Cogn Affect Neurosci. 2014;9: 505–12. 10.1093/scan/nst014
    1. Gregory S, ffytche D, Simmons A, Kumari V, Howard M, Hodgins S, et al. The antisocial brain: psychopathy matters. Arch Gen Psychiatry. 2012;69: 962–72. 10.1001/archgenpsychiatry.2012.222
    1. Sethi A, Gregory S, Dell’Acqua F, Periche Thomas E, Simmons A, Murphy DGM, et al. Emotional detachment in psychopathy: Involvement of dorsal default-mode connections. Cortex. 2015;62: 11–9. 10.1016/j.cortex.2014.07.018
    1. De Brito SA, Mechelli A, Wilke M, Laurens KR, Jones AP, Barker GJ, et al. Size matters: increased grey matter in boys with conduct problems and callous-unemotional traits. Brain. 2009;132: 843–52. 10.1093/brain/awp011
    1. Rijsdijk F, Viding E, De Brito S, Forgiarini M, Mechelli A, Jones AP et al. Heritable variations in gray matter concentration as a potential endophenotype for psychopathic traits. Arch Gen Psychiatry. 2010;67: 406–13. 10.1001/archgenpsychiatry.2010.20
    1. Cope LM, Shane MS, Segall JM, Nyalakanti PK, Stevens MC, Pearlson GD, et al. Examining the effect of psychopathic traits on gray matter volume in a community substance abuse sample. Psychiatry Res. 2012;204: 91–100. 10.1016/j.pscychresns.2012.10.004
    1. Yang Y, Raine A, Narr K, Colletti P, Toga A. Localization of deformations within the amygdala in individuals with psychopathy. Arch Gen Psychiatry. 2009;66: 986–94. 10.1001/archgenpsychiatry.2009.110
    1. Yang Y, Raine A, Colletti P, Toga AW, Narr KL. Abnormal temporal and prefrontal cortical gray matter thinning in psychopaths. Mol Psychiatry. 2009;14: 561–2, 555 10.1038/mp.2009.12
    1. Laakso MP, Vaurio O, Koivisto E, Savolainen L, Eronen M, Aronen HJ, et al. Psychopathy and the posterior hippocampus. Behav Brain Res. 2001;118: 187–93. Available:
    1. Cope LM, Ermer E, Nyalakanti PK, Calhoun VD, Kiehl KA. Paralimbic gray matter reductions in incarcerated adolescent females with psychopathic traits. J Abnorm Child Psychol. 2014;42: 659–68. 10.1007/s10802-013-9810-4
    1. Pardini DA, Raine A, Erickson K, Loeber R. Lower amygdala volume in men is associated with childhood aggression, early psychopathic traits, and future violence. Biol Psychiatry. 2014;75: 73–80. 10.1016/j.biopsych.2013.04.003
    1. Contreras-Rodríguez O, Pujol J, Batalla I, Harrison BJ, Soriano-Mas C, Deus J, et al. Functional connectivity bias in the prefrontal cortex of psychopaths. Biol Psychiatry. 2014; 10.1016/j.biopsych.2014.03.007
    1. Blakemore S-J, Choudhury S. Development of the adolescent brain: implications for executive function and social cognition. J Child Psychol Psychiatry. 2006;47: 296–312. 10.1111/j.1469-7610.2006.01611.x
    1. Paus T. Mapping brain maturation and cognitive development during adolescence. Trends Cogn Sci. 2005;9: 60–8. 10.1016/j.tics.2004.12.008
    1. Ashburner J, Friston KJ. Voxel-based morphometry—the methods. Neuroimage. 2000;11: 805–21. 10.1006/nimg.2000.0582
    1. Harmer CJ, Rogers RD, Tunbridge E, Cowen PJ, Goodwin GM. Tryptophan depletion decreases the recognition of fear in female volunteers. Psychopharmacology (Berl). 2003;167: 411–7.
    1. Hayward G, Goodwin GM, Cowen PJ, Harmer CJ. Low-dose tryptophan depletion in recovered depressed patients induces changes in cognitive processing without depressive symptoms. Biol Psychiatry. 2005;57: 517–24. 10.1016/j.biopsych.2004.11.016
    1. Intrator J, Hare R, Stritzke P, Brichtswein K, Dorfman D, Harpur T, et al. A brain imaging (single photon emission computerized tomography) study of semantic and affective processing in psychopaths. Biol Psychiatry. 1997;42: 96–103. 10.1016/S0006-3223(96)00290-9
    1. Kiehl KA, Smith AM, Hare RD, Mendrek A, Forster BB, Brink J, et al. Limbic abnormalities in affective processing by criminal psychopaths as revealed by functional magnetic resonance imaging. Biol Psychiatry. 2001;50: 677–84. Available:
    1. Müller JL, Sommer M, Wagner V, Lange K, Taschler H, Röder CH, et al. Abnormalities in emotion processing within cortical and subcortical regions in criminal psychopaths: evidence from a functional magnetic resonance imaging study using pictures with emotional content. Biol Psychiatry. 2003;54: 152–62. Available:
    1. Glenn AL, Raine A, Schug RA. The neural correlates of moral decision-making in psychopathy. Mol Psychiatry. 2009;14: 5–6. 10.1038/mp.2008.104
    1. Pujol J, Batalla I, Contreras-Rodríguez O, Harrison BJ, Pera V, Hernández-Ribas R, et al. Breakdown in the brain network subserving moral judgment in criminal psychopathy. Soc Cogn Affect Neurosci. 2012;7: 917–23. 10.1093/scan/nsr075
    1. American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5th ed Washington: DC: APA; 2013.
    1. Weschler D. Weschler Adult Intelligence Scale-Third Edition (WAIS-III). San Antonio: The Psychological Corporation; 1997.
    1. Moltó J, Poy R, Torrubia R. Standardization of the Hare Psychopathy Checklist-Revised in a Spanish prison sample. J Pers Disord. 2000;14: 84–96. Available:
    1. Tottenham N, Tanaka JW, Leon AC, McCarry T, Nurse M, Hare TA, et al. The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Res. 2009;168: 242–9. 10.1016/j.psychres.2008.05.006
    1. Ashburner J, Friston K. Unified segmentation. Neuroimage. 2005;26: 839–51.
    1. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage. 2001;14: 21–36. 10.1006/nimg.2001.0786
    1. Soriano-Mas C, Hernández-Ribas R, Pujol J, Urretavizcaya M, Deus J, Harrison BJ, et al. Cross-sectional and longitudinal assessment of structural brain alterations in melancholic depression. Biol Psychiatry. 2011;69: 318–25. 10.1016/j.biopsych.2010.07.029
    1. Thalheimer W, Cook S. How to calculate effect sizes from published research: A simplified methodology. 2002; 1–9. Available:
    1. Song X-W, Dong Z-Y, Long X-Y, Li S-F, Zuo X-N, Zhu C-Z, et al. REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One. Public Library of Science; 2011;6: e25031 10.1371/journal.pone.0025031
    1. Nichols T, Hayasaka S. Controlling the familywise error rate in functional neuroimaging: a comparative review. Stat Methods Med Res. 2003;12: 419–46. Available:
    1. Hayasaka S, Phan KL, Liberzon I, Worsley KJ, Nichols TE. Nonstationary cluster-size inference with random field and permutation methods. Neuroimage. 2004;22: 676–87. 10.1016/j.neuroimage.2004.01.041
    1. Blair RJR, Mitchell DG V, Richell RA, Kelly S, Leonard A, Newman C, et al. Turning a deaf ear to fear: impaired recognition of vocal affect in psychopathic individuals. J Abnorm Psychol. 2002;111: 682–6. Available:
    1. Blair RJR, Mitchell DG V, Peschardt KS, Colledge E, Leonard R a., Shine JH, et al. Reduced sensitivity to others’ fearful expressions in psychopathic individuals. Pers Individ Dif. 2004;37: 1111–1122. 10.1016/j.paid.2003.10.008
    1. Dolan M, Fullam R. Face affect recognition deficits in personality-disordered offenders: association with psychopathy. Psychol Med. 2006;36: 1563–9. 10.1017/S0033291706008634
    1. Iria C, Barbosa F. Perception of facial expressions of fear: Comparative research with criminal and non-criminal psychopaths. J Forens Psychiatry Psychol. 2009;20: 66–73.
    1. Hastings ME, Tangney JP, Stuewig J. Psychopathy and identification of facial expressions of emotion. Pers Individ Dif. 2008;44: 1474–1483. 10.1016/j.paid.2008.01.004
    1. Lykken DT. A study of anxiety in the sociopathic personality. J Abnorm Psychol. 1957;55: 6–10. Available:
    1. Lykken DT. The Antisocial Personalities [Internet]. Hillsdale, New Jersey Hove, UK: Lawrence Erlbaum Associates; 1995. Available:
    1. Patrick CJ, Cuthbert BN, Lang PJ. Emotion in the criminal psychopath: fear image processing. J Abnorm Psychol. 1994;103: 523–34. Available:
    1. Blair RJR. Applying a cognitive neuroscience perspective to the disorder of psychopathy. Dev Psychopathol. 2005;17: 865–91. 10.1017/S0954579405050418
    1. Whalen P. Fear, vigilance, and ambiguity: initial neuroimaging studies of the human amygdale. Curr Dir Psychol Sci. 1998;7: 177–88.
    1. Cleckley H. The Mask of Sanity. An Attempt to Clarify Some Issues About the So-Called Psychopathic Personality. Southern Medical Journal. 1951.
    1. Blair RJ. A cognitive developmental approach to mortality: investigating the psychopath. Cognition. 1995;57: 1–29. 10.1016/0010-0277(95)00676-P
    1. Blair RJ. Neurocognitive models of aggression, the antisocial personality disorders, and psychopathy. J Neurol Neurosurg Psychiatry. 2001;71: 727–731. 10.1136/jnnp.71.6.727
    1. Kosson DS, Suchy Y, Mayer AR, Libby J. Facial affect recognition in criminal psychopaths. Emotion. 2002;2: 398–411. Available:
    1. Decety J, Skelly LR, Kiehl KA. Brain response to empathy-eliciting scenarios involving pain in incarcerated individuals with psychopathy. JAMA psychiatry. 2013;70: 638–45. 10.1001/jamapsychiatry.2013.27
    1. Lorenz AR, Newman JP. Deficient response modulation and emotion processing in low-anxious Caucasian psychopathic offenders: results from a lexical decision task. Emotion. 2002;2: 91–104. Available:
    1. 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.
    1. Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies. Neuroimage. Elsevier Inc.; 2009;44: 489–501. 10.1016/j.neuroimage.2008.08.039
    1. Jones AP, Laurens KR, Herba CM, Barker GJ, Viding E. Amygdala hypoactivity to fearful faces in boys with conduct problems and callous-unemotional traits. Am J Psychiatry. 2009;166: 95–102. 10.1176/appi.ajp.2008.07071050
    1. Gordon HL, Baird A a., End A. Functional differences among those high and low on a trait measure of psychopathy. Biol Psychiatry. 2004;56: 516–521. 10.1016/j.biopsych.2004.06.030
    1. Han T, Alders GL, Greening SG, Neufeld RWJ, Mitchell DG V. Do fearful eyes activate empathy-related brain regions in individuals with callous traits? Soc Cogn Affect Neurosci. 2012;7: 958–68. 10.1093/scan/nsr068
    1. Nacewicz BM, Dalton KM, Johnstone T, Long MT, McAuliff EM, Oakes TR, et al. Amygdala volume and nonverbal social impairment in adolescent and adult males with autism. Arch Gen Psychiatry. 2006;63: 1417–28. 10.1001/archpsyc.63.12.1417
    1. Goghari VM, Macdonald AW, Sponheim SR. Temporal lobe structures and facial emotion recognition in schizophrenia patients and nonpsychotic relatives. Schizophr Bull. 2011;37: 1281–94. 10.1093/schbul/sbq046
    1. Namiki C, Hirao K, Yamada M, Hanakawa T, Fukuyama H, Hayashi T, et al. Impaired facial emotion recognition and reduced amygdalar volume in schizophrenia. Psychiatry Res. 2007;156: 23–32. 10.1016/j.pscychresns.2007.03.004
    1. Onitsuka T, Shenton ME, Kasai K, Nestor PG, Toner SK, Kikinis R, et al. Fusiform gyrus volume reduction and facial recognition in chronic schizophrenia. Arch Gen Psychiatry. 2003;60: 349–55. 10.1001/archpsyc.60.4.349
    1. Phan KL, Wager T, Taylor SF, Liberzon I. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage. 2002;16: 331–348. 10.1006/nimg.2002.1087
    1. Vytal K, Hamann S. Neuroimaging support for discrete neural correlates of basic emotions: a voxel-based meta-analysis. J Cogn Neurosci. 2010;22: 2864–85. 10.1162/jocn.2009.21366
    1. Kober H, Barrett LF, Joseph J, Bliss-Moreau E, Lindquist K, Wager TD. Functional grouping and cortical-subcortical interactions in emotion: A meta-analysis of neuroimaging studies. Neuroimage. 2008;42: 998–1031. 10.1016/j.neuroimage.2008.03.059
    1. Lindquist KA, Kober H, Bliss-moreau E, Barrett LF. The brain basis of emotion: A meta-analytic review. 2012; 121–202.
    1. Sergerie K, Chochol C, Armony JL. The role of the amygdala in emotional processing: A quantitative meta-analysis of functional neuroimaging studies. Neurosci Biobehav Rev. 2008;32: 811–830. 10.1016/j.neubiorev.2007.12.002
    1. Adolphs R. What does the amygdala contribute to social cognition? Ann N Y Acad Sci. 2010;1191: 42–61. 10.1111/j.1749-6632.2010.05445.x
    1. Fitzgerald PB, Oxley TJ, Laird AR, Kulkarni J, Egan GF, Daskalakis ZJ. An analysis of functional neuroimaging studies of dorsolateral prefrontal cortical activity in depression. Psychiatry Res—Neuroimaging. 2006;148: 33–45. 10.1016/j.pscychresns.2006.04.006
    1. Zhao K, Yan W-J, Chen Y-H, Zuo X-N, Fu X. Amygdala volume predicts inter-individual differences in fearful face recognition. PLoS One. 2013;8: e74096 10.1371/journal.pone.0074096
    1. Pham TH, Philippot P. Decoding of facial expression of emotion in criminal psychopaths. J Pers Disord. 2010;24: 445–59. 10.1521/pedi.2010.24.4.445

Source: PubMed

Sponsors en medewerkers

Medische omstandigheden

Geneesmiddelinterventies

3
Abonneren