Advertisement

Adolescent Psychopathic Traits Negatively Relate to Hemodynamic Activity within the Basal Ganglia during Error-Related Processing

  • J. Michael MaurerEmail author
  • Vaughn R. Steele
  • Gina M. Vincent
  • Vikram Rao
  • Vince D. Calhoun
  • Kent A. Kiehl
Article

Abstract

Youth with elevated psychopathic traits exhibit a number of comparable neurocognitive deficits as adult psychopathic offenders, including error-related processing deficits. Subregions of the basal ganglia play an important, though indirect, role in error-related processing through connections with cortical areas including the anterior cingulate cortex. A number of recent structural and functional magnetic resonance imaging (s/fMRI) studies have associated basal ganglia dysfunction in youth with elevated psychopathic traits, but these studies have not examined whether dysfunction occurring within subregions of the basal ganglia help contribute to error-related processing deficits previously observed in such at-risk youth. Here, we investigated error-related processing using a response inhibition Go/NoGo fMRI experimental paradigm in a large sample of incarcerated male adolescent offenders (n = 182). In the current report, psychopathy scores (measured via the Psychopathy Checklist: Youth Version (PCL:YV)) were negatively related to hemodynamic activity within input nuclei of the basal ganglia (i.e., the caudate and nucleus accumbens), as well as intrinsic/output nuclei (i.e., the globus pallidus and substantia nigra) and related nuclei (i.e., the subthalamic nucleus) during error-related processing. This is the first evidence to suggest that error-related dysfunction previously observed in youth with elevated psychopathic traits may be related to underlying abnormalities occurring within subregions of the basal ganglia.

Keywords

Juvenile delinquency Callous-unemotional traits Functional magnetic resonance imaging Error-related processing Basal ganglia 

Notes

Acknowledgments

This study was funded by the National Institute of Mental Health (NIMH) grant R01 MH071896 (PI: Kiehl), the National Institute of Child Health and Human Development (NICHD) grant R01 HD082257 (PI: Kiehl), the National Institute on Drug Abuse (NIDA) K01 DA026502 (PI: Vincent), and the National Institute of General Medical Sciences (NIGMS) P20 GM103472 (PI: Calhoun). JMM is supported by NIDA through grant number F31 DA043328. VRS is supported by the Intramural Research Program of NIDA, National Institutes of Health, Baltimore, Maryland. We are grateful to the staff and clients (and parents) at the Youth Diagnostic and Development Center and the New Mexico Children, Youth, and Families Department for their support and assistance in making this research possible. The authors thank Prashanth Nyalakanti for his assistance in data analysis.

Compliance with Ethical Standards

Conflict of Interest

The authors report no biomedical financial interests or potential conflicts of interest.

Ethical Approval

All research protocols were approved by Ethical and Independent Review Services (E &I), the Office for Human Research Protections (OHRP), and the juvenile detention center where data collection occurred.

Informed Consent

Informed consent was obtained from all individual participants included in the study.

References

  1. Anderson, N. E., Steele, V. R., Maurer, J. M., Bernat, E. M., & Kiehl, K. A. (2015). Psychopathy, attention, and oddball target detection: New insights from PCL-R facet scores. Psychophysiology, 52(9), 1194–1204.Google Scholar
  2. Blair, R. J. R. (2013). Psychopathy: Cognitive and neural dysfunction. Dialogues in Clinical Neuroscience, 15(2), 181–190.Google Scholar
  3. Botvinick, M. M., Braver, T. S., Barch, D. M., Carter, C. S., & Cohen, J. D. (2001). Conflict monitoring and cognitive control. Psychological Review, 108(3), 624–652.Google Scholar
  4. Brazil, I. A., de Bruijn, E. R., Bulten, B. H., von Borries, A. K., van Lankveld, J. J., Buitelaar, J. K., & Verkes, R. J. (2009). Early and late components of error monitoring in violent offenders with psychopathy. Biological Psychiatry, 65(2), 137–143.Google Scholar
  5. Budhani, S., & Blair, R. J. R. (2005). Response reversal and children with psychopathic tendencies: Success is a function of salience of contingency change. Journal of Child Psychology and Psychiatry, 46(9), 972–981.Google Scholar
  6. Bunzeck, N., & Duzel, E. (2006). Absolute coding of stimulus novelty in the human substantia nigra/VTA. Neuron, 51(369–379), 369.Google Scholar
  7. Burgaleta, M., MacDonald, P. A., Martínez, K., Román, F. J., Álvarez-Linera, J., Ramos González, A., . . . Colom, R. (2014). Subcortical regional morphology correlates with fluid and spatial intelligence. Human Brain Mapping, 35(5), 1957–1968.Google Scholar
  8. Caldwell, M. F. (2011). Treatment-related changes in behavioral outcomes of psychopathy facets in adolescent offenders. Law and Human Behavior, 35(4), 275–187.Google Scholar
  9. Caldwell, M. F., McCormick, D. J., Umstead, D., & Van Rybroek, G. J. (2007). Evidence of treatment progress and therapeutic outcomes among adolescents with psychopathic features. Criminal Justice and Behavior, 34(5), 573–587.Google Scholar
  10. Calhoun, V. D., Stevens, M., Pearlson, G. D., & Kiehl, K. A. (2004). fMRI analysis with the general linear model: Removal of latency-induced amplitude bias by incorporation of hemodynamic derivative terms. NeuroImage, 22, 252–257.Google Scholar
  11. Calhoun, V. D., Wager, T. D., Krishnan, A., Rosch, K. S., Seymour, K. E., Nebel, M. B., . . . Kiehl, K. A. (2017). The impact of T1 versus EPI spatial normalization templates for fMRI data analysis. Human Brain Mapping, 38(11), 5331–5342.Google Scholar
  12. Cavanagh, J. F., Sanguinetti, J. L., Allen, J. J. B., Sherman, S. J., & Frank, M. J. (2014). The subthalamic nucleus contributes to post-error slowing. The Journal of Neuroscience, 26(11), 2637–2644.Google Scholar
  13. Cope, L. M., Vincent, G. M., Jobelius, J. L., Nyalakanti, P., Calhoun, V. D., & Kiehl, K. A. (2014). Psychopathic traits modulate brain responses to drug cues in incarcerated offenders. Frontiers in Human Neuroscience, 8(87), 1–18.Google Scholar
  14. Dadds, M. R., Perry, Y., Hawes, D. J., Merz, S., Riddell, A. C., Haines, D. J., . . . Abeygunawardane, A. I. (2006). Attention to the eyes and fear-recognition deficits in child psychopathy. The British Journal of Psychiatry, 189(3), 280–281.Google Scholar
  15. Dalley, J. W., Fryer, T. D., Brichard, L., Robinson, E. S., Theobald, D. E., Lääne, K., . . . Robbins, T. W. (2007). Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science, 315(5816), 1267–1270.Google Scholar
  16. Danielmeier, C., & Ullsperger, M. (2011). Post-error adjustments. Frontiers in Psychology, 2(233), 1–10.Google Scholar
  17. Doppelmayr, M., Klimesch, W., Sauseng, P., Hodlmoser, K., Stadler, W., & Hanslmayr, S. (2005). Intelligence related differences in EEG badpower. Neuroscience Letters, 381(3), 309–313.Google Scholar
  18. Edens, J. F., Campbell, J. S., & Weir, J. M. (2007). Youth psychopathy and criminal recidivism: A meta-analysis of the psychopathy checklist measures. Law and Human Behavior, 31(1), 53–75.Google Scholar
  19. Edwards, B. G., Calhoun, V. D., & Kiehl, K. A. (2012). Joint ICA of ERP and fMRI during error-monitoring. NeuroImage, 59(2), 1896–1903.Google Scholar
  20. Egner, T. (2009). Prefrontal cortex and cognitive control: Motivating functional hierarchies. Nature Neuroscience, 12, 821–822.Google Scholar
  21. Finger, E. C., Marsh, A. A., Mitchell, D. G., Reid, M. E., Sims, C., Budhani, S., . . . Blair, J. R. (2008). Abnormal ventromedial prefrontal cortex function in children with psychopathic traits during reversal learning. Archives in General Psychiatry, 65(5), 586–594.Google Scholar
  22. Finger, E. C., Marsh, A. A., Blair, K. S., Reid, M. E., Sims, C., Ng, P., . . . Blair, R. J. (2011). Disrupted reinforcement signaling in the orbitofrontal cortex and caudate in youths with conduct disorder or oppositional defiant disorder and a high level of psychopathic traits. American Journal of Psychiatry, 168(2), 152–162.Google Scholar
  23. Foley, R. M. (2001). Academic characteristics of incarcerated youth and correctional educational programs: A literature review. Journal of Emotional and Behavioral Disorders, 9(4), 248–259.Google Scholar
  24. Forth, A. E., Kosson, D. S., & Hare, R. D. (2003). The Psychopathy Checklist: Youth Version. Toronto: Multi-Health Systems.Google Scholar
  25. Freire, L., & Mangin, J. F. (2001). Motion correction algorithms may create spurious brain activations in the absence of subject motion. NeuroImage, 14, 709–722.Google Scholar
  26. Freire, L., Roche, A., & Mangin, J. F. (2002). What is the best similarity measure for motion correction in fMRI time series? IEEE Transactions on Medical Imaging, 21, 470–484.Google Scholar
  27. Frick, P. J., Cornell, A. H., Bodin, S. D., Dane, H. E., Barry, C. T., & Loney, B. R. (2003). Callous-unemotional traits and developmental pathways to severe conduct problems. Developmental Psychology, 39(2), 246–260.Google Scholar
  28. Grazioplene, R. G., Ryman, S. G., Gray, J. R., Rustichini, A., Jung, R. E., & DeYoung, C. G. (2015). Subcortical intelligence: Caudate volume predicts IQ in healthy adults. Human Brain Mapping, 36(4), 1407–1416.Google Scholar
  29. Haber, S. N., & Knutson, B. (2010). The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology, 35(1), 4–26.Google Scholar
  30. Haier, R. J., Siegel, B. V., Nuechterlein, K. H., Hazlett, E., Wu, J. C., & Paek, J. (1992). Cortical glucose metabolic rate correlates of abstract reasoning and attention studied with positron emission tomography. Intelligence, 12, 199–217.Google Scholar
  31. Ham, T., Leff, A., de Boissezon, X., Joffe, A., & Sharp, D. J. (2013). Cognitive control and the salience network: An investigation of error processing and effective connectivity. Journal of Neuroscience, 33(16), 7091–7098.Google Scholar
  32. Hare, R. D. (1991). The Hare psychopathy checklist - revised manual. Toronto: Multi-Health Systems.Google Scholar
  33. Hare, R. D. (2003). Manual for the Hare Psychopathy Checklist - Revised (2nd ed.). Toronto: Multi-Health Systems.Google Scholar
  34. Harsay, H. A., Spaan, M., Wijnen, J. G., & Ridderinkhof, K. R. (2012). Error awareness and salience processing in the oddball task: Shared neural mechanisms. Frontiers in Human Neuroscience, 6(246), 1–20.Google Scholar
  35. Hawes, S. W., Byrd, A. L., Kelley, S. E., Gonzalez, R., Edens, J. F., & Pardini, D. A. (2018). Psychopathic features across development: Assessing longitudinal invariance among Caucasian and African American youths. Journal of Research in Personality,  73, 180-188.Google Scholar
  36. Hemphälä, M., Kosson, D. S., Westerman, J., & Hodgins, S. (2015). Stability and predictors of psychopathic traits from mid-adolescence through early adulthood. Scandanavian Journal of Psychology, 56(6), 649–658.Google Scholar
  37. Hemphill, J. F., Hare, R. D., & Wong, S. (1998). Psychopathy and recidivism: A review. Legal and Criminological Psychology, 3(1), 139–170.Google Scholar
  38. Hermann, M. J., Rommler, J., Ehlis, A. C., Heidrich, A., & Fallgatter, A. J. (2004). Source localization (LORETA) of the error-related negativity (ERN/ne) and positivity (Pe). Cognitive Brain Research, 20(2), 294–299.Google Scholar
  39. Holroyd, C. B., & Coles, M. G. H. (2002). The neural basis of human error processing: Reinforcement learning, dopamine, and the error-related negativity. Psychological Review, 109(4), 679–709.Google Scholar
  40. Juarez, M., Kiehl, K. A., & Calhoun, V. D. (2013). Intrinsic limbic and paralimbic networks are associated with criminal psychopathy. Human Brain Mapping, 34(8), 1921–1930.Google Scholar
  41. Kaufman, J., Birmaher, B., & Brent, D. (1997). Schedule for affective disorders and schizophrenia for school-aged children: Present and lifetime version (K-SADS-PL): Initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry, 37(7), 980–988.Google Scholar
  42. Kennealy, P. J., Hicks, B. M., & Patrick, C. J. (2007). Validity of factors of the psychopathy checklist-revised in female prisoners: Discriminant relations with antisocial behavior, substance abuse, and personality. Assessment, 14(4), 323–340.Google Scholar
  43. Kennerley, S. W., Walton, M. E., Behrens, T. E. J., Buckley, M. J., & Rushworth, M. F. S. (2006). Optimal decision making and the anterior cingulate cortex. Nature Neuroscience, 9, 940–947.Google Scholar
  44. Kiehl, K. A., Liddle, P. F., & Hopfinger, J. B. (2000). Error processing and the rostral anterior cingulate: An event-related fMRI study. Psychophysiology, 37(2), 216–223.Google Scholar
  45. Lanciego, J. L., Luquin, N., & Obeso, J. A. (2012). Functional neuroanatomy of the basal ganglia. Cold Spring Harbor Perspectives in Medicine, 5, 1–20.Google Scholar
  46. Lee, Z., Klaver, J. R., Hart, S. D., Moretti, M. M., & Douglas, K. S. (2009). Short-term stability of psychopathic traits in adolescent offenders. Journal of Clinical Child and Adolescent Psychology, 38(5), 595–605.Google Scholar
  47. Lynam, D. R., Caspi, A., Moffitt, T. E., Loeber, R., & Stouthamer-Loeber, M. (2007). Longitudinal evidence that psychopathy scores in early adolescence predict adult psychopathy. Journal of Abnormal Psychology, 116, 155–165.Google Scholar
  48. Mailloux, D. L., Forth, A. E., & Kroner, D. G. (1997). Psychopathy and substance use in adolescent male offenders. Psychological Reports, 81(2), 529–530.Google Scholar
  49. Maldjian, J. A., Laurienti, P. J., Kraft, R. A., & Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage, 19(3), 1233–1239.Google Scholar
  50. Maldjian, J. A., Laurienti, P. J., & Burdette, J. H. (2004). Precentral gyrus discrepency in electronic versions of the Talairach atlas. NeuroImage, 21(1), 450–455.Google Scholar
  51. Marsh, A. A., Finger, E. C., Fowler, K. A., Adalio, C. J., Jurkowitz, I. T., Schechter, J. C., . . . Blair, R. J. (2013). Empathic responsiveness in amygdala and anterior cingulate cortex in youths with psychopathic traits. Journal of Child Psychology and Psychiatry, 54(8), 900–910.Google Scholar
  52. Mathalon, D. H., Whitfield, S. L., & Ford, J. M. (2003). Anatomy of an error: ERP and fMRI. Biological Psychology, 64(1–2), 119–141.Google Scholar
  53. Maurer, J. M., Steele, V. R., Cope, L. M., Vincent, G. M., Stephen, J. M., Calhoun, V. D., & Kiehl, K. A. (2016a). Dysfunctional error-related processing in incarcerated youth with elevated psychopathic traits. Developmental Cognitive Neuroscience, 19, 70–77.Google Scholar
  54. Maurer, J. M., Steele, V. R., Edwards, B. G., Bernat, E. M., Calhoun, V. D., & Kiehl, K. A. (2016b). Dysfunctional error-related processing in female psychopathy. Social Cognitive and Affective Neuroscience, 11(7), 1059–1068.Google Scholar
  55. Middleton, F. A., & Strick, P. L. (2000). Basal ganglia and cerebellar loops: Motor and cognitive circuits. Brain Research Reviews, 31(2–3), 236–250.Google Scholar
  56. Neubauer, A. C., & Fink, A. (2009). Intelligence and neural efficiency. Neuroscience & Biobehavioral Reviews, 33(1004–1023), 1004–1023.Google Scholar
  57. Neumann, C. S., & Hare, R. D. (2008). Psychopathic traits in a large community sample: Links to violence, alcohol use, and intelligence. Journal of Consulting and Clinical Psychology, 76(5), 893–899.Google Scholar
  58. Neumann, C. S., Kosson, D. S., Forth, A. E., & Hare, R. D. (2006). Factor structure of the Hare psychopathy checklist: Youth version (PCL:YV) in incarcerated adolescents. Psychological Assessment, 18(2), 142–154.Google Scholar
  59. Newman, J. P., & Baskin-Sommers, A. R. (2012). Early selective attention abnormalities in psychopathy: Implications for self-regulation. In M. I. Posner (Ed.), Cognitive neuroscience of attention (2nd ed., pp. 421–439). United States of America: The Guilford Press.Google Scholar
  60. Nys, G. M. S., van Zandvoort, M. J. E., van der Worp, H. B., Kappelle, L. J., & de Haan, E. H. F. (2006). Neuropsychological and neuroanatomical correlates of perseverative responses in subacute stroke. Brain, 129, 2148–2157.Google Scholar
  61. Overbeek, T. J. M., Nieuwenhuis, S., & Ridderinkhof, K. R. (2005). Dissociable components of error processing. Journal of Psychophysiology, 19(4), 319–329.  https://doi.org/10.1027/0269-8803.19.4.319.Google Scholar
  62. Patrick, C. J., Bradley, M. M., & Lang, P. J. (1993). Emotion in the criminal psychopath: Startle reflex modulation. Journal of Abnormal Psychology, 102(1), 82–92.Google Scholar
  63. Philippi, C. L., Pujara, M. S., Motzkin, J. C., Newman, J., Kiehl, K. A., & Koenigs, M. (2015). Altered resting-state functional connectivity in cortical networks in psychopathy. The Journal of Neuroscience, 35(15), 6068–6078.Google Scholar
  64. Rabbit, P. M. A. (1981). Sequential reactions. In D. Holding (Ed.), Human Skills (pp. 153–175). New York: Wiley.Google Scholar
  65. Ravizza, S. M., & Ciranni, M. A. (2002). Contributions of the prefrontal cortex and basal ganglia to set shifting. Journal of Cognitive Neuroscience, 14(3), 472–483.Google Scholar
  66. Rice, M. E., & Harris, G. T. (1997). Cross-validation and extension of the violence risk appraisal guide for child molestors and rapists. Law and Human Behavior, 21(2), 231–241.Google Scholar
  67. Roussy, S., & Toupin, J. (2000). Behavioral inhibition deficits in juvenile psychopaths. Aggressive Behavior, 26(6), 413–424.Google Scholar
  68. Rubia, K., Russell, T., Overmeyer, S., Brammer, M. J., Bullmore, E. T., Sharma, T., . . . Taylor, E. (2001). Mapping motor inhibition: Conjunctive brain activations across different versions of go/no-go and stop tasks. NeuroImage, 13(2), 250–261.Google Scholar
  69. Siegert, S., Herrojo Ruiz, M., Brucke, C., Huebl, J., Schneider, G.-H., Ullsperger, M., & Kuhn, A. A. (2014). Error signals in the subthalamic nucleus are related to post-error slowing in patients with Parkinson's disease. Cortex, 60, 103–120.Google Scholar
  70. Steele, V. R., Claus, E. D., Aharoni, E., Harenski, C., Calhoun, V. D., Pearlson, G. D., & Kiehl, K. A. (2014). A large scale (n = 102) functional neuroimaging study of error processing in a go/NoGo task. Behavioural Brain Science, 268, 127–138.Google Scholar
  71. Steele, V. R., Anderson, N. E., Claus, E. D., Bernat, E. M., Rao, V., Assaf, M., . . . Kiehl, K. A. (2016a). Neuroimaging measures of error-processing: Extracting reliable signals from event-related potentials and functional magnetic resonance imaging. NeuroImage, 132, 247–260.Google Scholar
  72. Steele, V. R., Maurer, J. M., Bernat, E. M., Calhoun, V. D., & Kiehl, K. A. (2016b). Error-related processing in adult males with elevated psychopathic traits. Personality Disorders: Theory, Research, and Treatment, 7(1), 80–90.Google Scholar
  73. Ullsperger, M., Harsay, H. A., Wessel, J. R., & Ridderinkhof, K. R. (2010). Conscious perception of errors and its relation to the anterior insula. Brain Structure & Function, 214(5–6), 629–643.  https://doi.org/10.1007/s00429-010-0261-1.Google Scholar
  74. Uslaner, J. M., & Robinson, T. E. (2006). Subthalamic nucleus lesions increase impulsive action and decrease impulsive choice - mediation by enchanced incentive motivation? European Journal of Neuroscience, 24(8), 2345–2354.Google Scholar
  75. van Veen, V., & Carter, C. S. (2002). The timing of action-monitoring processes in the anterior cingulate cortex. Journal of Cognitive Neuroscience, 14(4), 593–602.Google Scholar
  76. Vijayaraghavan, L., Vaidya, J. G., Humphreys, C. T., Beglinger, L. J., & Paradoso, S. (2008). Emotional and motivational changes after bilateral lesions of the globus pallidus. Neuropsychology, 22, 412–418.Google Scholar
  77. Vincent, G. M., Cope, L. M., King, J., Nyalakanti, P., & Kiehl, K. A. (2017). Callous-unemotional traits modulate brain drug craving response in high-risk young offenders. Journal of Abnormal Child Psychology, 1–17.Google Scholar
  78. Wasserman, G. A., McReynolds, L. S., Lucas, C. P., Fisher, P., & Santos, L. (2002). The voice DISC-IV with incarcerated male youths: Prevalence of disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 41(3), 314–321.Google Scholar
  79. Wechsler, D. (1997). WAIS-III: Wechsler Adult Intelligence Scale (3rd Edition). San Antonio, TX: The Psychological Corporation.Google Scholar
  80. Wechsler, D. (2003). Wechsler Intelligence Scale for Children (4th ed.). San Antonio: Harcourt Assessment.Google Scholar
  81. Weissman, D. G., Schriber, R. A., Fassbender, C., Atherton, O., Krafft, C., Robins, R. W., . . . Guyer, A. E. (2015). Earlier adolescent substance use onset predicts stronger connectivity between reward and cognitive control brain networks. Developmental Cognitive Neuroscience, 16, 121–129.Google Scholar
  82. Yang, Y., Narr, K. L., Baker, L. A., Joshi, S. H., Jahanshad, N., Raine, A., & Thompson, P. M. (2015). Frontal and striatal alterations associated with psychopathic traits in adolescence. Psychiatry Research: Neuroimaging, 231(3), 333–340.Google Scholar
  83. Yin, H. H., & Knowlton, B. J. (2006). The role of the basal ganglia in habit formation. Nature Reviews Neuroscience, 7, 464–476.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of New MexicoAlbuquerqueUSA
  2. 2.The Mind Research Network (MRN) & Lovelace Biomedical and Environmental Research Institute (LBERI)AlbuquerqueUSA
  3. 3.Neuroimaging Research Branch, National Institute on Drug Abuse, Intramural Research ProgramNational Institutes of HealthBaltimoreUSA
  4. 4.Department of PsychiatryUniversity of Massachusetts Medical SchoolWorcesterUSA
  5. 5.Department of Neuro-OncologyMD Anderson Cancer CenterHoustonUSA
  6. 6.Department of Electrical and Computer EngineeringUniversity of New MexicoAlbuquerqueUSA

Personalised recommendations