Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-25T18:53:50.202Z Has data issue: false hasContentIssue false
  • English
  • Français

Impulsivity and aggression in schizophrenia: a neural circuitry perspective with implications for treatment

Published online by Cambridge University Press:  22 April 2015

Matthew J. Hoptman
Matthew J. Hoptman*
Affiliation:
Schizophrenia Research Division, Nathan Kline Institute for Psychiatric Research, Orangeburg, New York, USA; Department of Psychiatry, New York University School of Medicine, New York, New York, USA; Department of Psychology, City University of New York, New York, New York, USA
*
*Address for correspondence, Matthew J. Hoptman, PhD, Nathan Kline Institute, 140 Old Orangeburg Rd., Bldg. 35, Orangeburg, NY 10962, USA. (Email: Hoptman@nki.rfmh.org)
Get access Rights & Permissions [Opens in a new window]

Abstract

Elevations of impulsive behavior have been observed in a number of serious mental illnesses. These phenomena can lead to harmful behaviors, including violence, and thus represent a serious public health concern. Such violence is often a reason for psychiatric hospitalization, and it often leads to prolonged hospital stays, suffering by patients and their victims, and increased stigmatization. Despite the attention paid to violence, little is understood about its neural basis in schizophrenia. On a psychological level, aggression in schizophrenia has been primarily attributed to psychotic symptoms, desires for instrumental gain, or impulsive responses to perceived personal slights. Often, multiple attributions can coexist during a single aggressive incident. In this review, I discuss the neural circuitry associated with impulsivity and aggression in schizophrenia, with an emphasis on implications for treatment. Impulsivity appears to account for a great deal of aggression in schizophrenia, especially in inpatient settings. Urgency, defined as impulsivity in the context of strong emotion, is the primary focus of this article. It is elevated in several psychiatric disorders, and in schizophrenia, it has been related to aggression. Many studies have implicated dysfunctional frontotemporal circuitry in impulsivity and aggression in schizophrenia, and pharmacological treatments may act via that circuitry to reduce urgency and aggressive behaviors; however, more mechanistic studies are critically needed. Recent studies point toward manipulable neurobehavioral targets and suggest that cognitive, pharmacological, neuromodulatory, and neurofeedback treatment approaches can be developed to ameliorate urgency and aggression in schizophrenia. It is hoped that these approaches will improve treatment efficacy.

Keywords

Functional connectivityimpulsivityMRIneuroimagingschizophreniatreatmenturgencyviolenceaggression
Type
Review Articles
Information
CNS Spectrums , Volume 20 , Special Issue 3: Violence in the Psychiatric Setting , June 2015 , pp. 280 - 286
Copyright
© Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

I wish to thank Karen A. Nolan, PhD, and Amanda R. McGovern, PhD, for their helpful comments on prior drafts of this article.

This article draws on work supported in part by the National Institute of Mental Health (M.J.H., grant numbers R01MH064783 and R21MH0804031) and NARSAD (M.J.H., Young Investigator Award).

References

1. McEvoy, JP. The costs of schizophrenia. J Clin Psychiatry. 2007; 68(Suppl 14): 4–7.Google ScholarPubMed
2. Torrey, EF. Stigma and violence: isn’t it time to connect the dots? Schizophr Bull. 2011; 37(5): 892–896.CrossRefGoogle ScholarPubMed
3. Volavka, J, Citrome, L. Heterogeneity of violence in schizophrenia and implications for long-term treatment. Int J Clin Pract. 2008; 62(8): 1237–1245.Google Scholar
4. Stahl, SM. Deconstructing violence as a medical syndrome: mapping psychotic, impulsive, and predatory subtypes to malfunctioning brain circuits. CNS Spectr. 2014; 19(5): 357–365.Google Scholar
5. Witt, K, van Dorn, R, Fazel, S. Risk factors for violence in psychosis: systematic review and meta-regression analysis of 110 studies. PLoS One. 2013; 8(2): e55942.Google Scholar
6. Nolan, KA, Czobor, P, Roy, BB, et al. Characteristics of assaultive behavior among psychiatric inpatients. Psychiatr Serv. 2003; 54(7): 1012–1016.CrossRefGoogle ScholarPubMed
7. Dodge, KA, Lochman, JE, Harnish, JD, Bates, JE, Pettit, GS. Reactive and proactive aggression in school children and psychiatrically impaired chronically assaultive youth. J Abnorm Psychol. 1997; 106(1): 37–51.Google Scholar
8. McDermott, BE, Holoyda, BJ. Assessment of aggression in inpatient settings. CNS Spectr. 2014; 19(05): 425–431.Google Scholar
9. Nolan, KA, Volavka, J, Mohr, P, Czobor, P. Psychopathy and violent behavior among patients with schizophrenia or schizoaffective disorder. Psychiatr Serv. 1999; 50(6): 787.Google Scholar
10. Patton, JH, Stanford, MS, Barratt, ES. Factor structure of the Barratt impulsiveness scale. J Clin Psychol. 1995; 51(6): 768–774.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
11. Nolan, KA, D’Angelo, D, Hoptman, MJ. Self-report and laboratory measures of impulsivity in patients with schizophrenia or schizoaffective disorder and healthy controls. Psychiatry Res. 2011; 187(1–2): 301–303.Google Scholar
12. Barratt, ES. Impulsivity: integrating cognitive, behavioral, biological, and environmental data. In: McCowan W, Johnson J, Shure M, eds. The Impulsive Client: Theory, Research, and Treatment. American Psychological Association; 1993: 39–56.CrossRefGoogle Scholar
13. Lipszyc, J, Schachar, R. Inhibitory control and psychopathology: a meta-analysis of studies using the stop signal task. J Int Neuropsychol Soc. 2010; 16(6): 1064–1076.CrossRefGoogle ScholarPubMed
14. Chambers, CD, Garavan, H, Bellgrove, MA. Insights into the neural basis of response inhibition from cognitive and clinical neuroscience. Neurosci Biobehav Rev. 2009; 33(5): 631–646.Google Scholar
15. Enticott, PG, Ogloff, JRP, Bradshaw, JL, Daffern, M. Contrary to popular belief, a lack of behavioural inhibitory control may not be associated with aggression. Crim Behav Ment Health. 2007; 17(3): 179–183.Google Scholar
16. Whiteside, SP, Lynam, DR. The five factor model and impulsivity: using a structural model of personality to understand impulsivity. Personality and Individual Differences. 2001; 30(4): 669–689.CrossRefGoogle Scholar
17. Cyders, MA, Smith, GT. Mood-based rash action and its components: positive and negative urgency. Personality and Individual Differences. 2007; 43(4): 839–850.CrossRefGoogle Scholar
18. Hoptman, MJ, Antonius, D, Mauro, CJ, Parker, EM, Javitt, DC. Cortical thinning, functional connectivity, and mood-related impulsivity in schizophrenia: relationship to aggressive attitudes and behavior. Am J Psychiatry. 2014; 171(9): 943–948.CrossRefGoogle ScholarPubMed
19. Cyders, MA, Smith, GT. Emotion-based dispositions to rash action: positive and negative urgency. Psychol Bull. 2008; 134(6): 807–828.CrossRefGoogle ScholarPubMed
20. Cyders, MA, Dzemidzic, M, Eiler, WJ, Coskunpinar, A, Karyadi, KA, Kareken, DA. Negative urgency mediates the relationship between amygdala and orbitofrontal cortex activation to negative emotional stimuli and general risk-taking. Cereb Cortex. doi:10.1093/cercor/bhu123.Google Scholar
21. Enticott, PG, Ogloff, JR, Bradshaw, JL. Response inhibition and impulsivity in schizophrenia. Psychiatry Res. 2008; 157(1): 251–254.CrossRefGoogle ScholarPubMed
22. Enticott, PG, Ogloff, JR, Bradshaw, JL. Associations between laboratory measures of executive inhibitory control and self-reported impulsivity. Personality and Individual Differences. 2006; 41(2): 285–294.CrossRefGoogle Scholar
23. Pawliczek, CM, Derntl, B, Kellermann, T, Kohn, N, Gur, RC, Habel, U. Inhibitory control and trait aggression: neural and behavioral insights using the emotional stop signal task. Neuroimage. 2013; 79: 264–274.CrossRefGoogle ScholarPubMed
24. Green, MF, Lee, J. Neural bases of emotional experience versus perception in schizophrenia. Biol Psychiatry. 2012; 71(2): 96–97.CrossRefGoogle ScholarPubMed
25. Insel, TR, Cuthbert, BN, Garvey, MA, et al. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am J Psychiatry. 2010; 167(7): 748–751.CrossRefGoogle Scholar
26. Yudofsky, SC, Silver, JM, Jackson, W, Endicott, J, Williams, D. The Overt Aggression Scale for the objective rating of verbal and physical aggression. Am J Psychiatry. 1986; 143(1): 35–39.Google ScholarPubMed
27. Buss, AH, Perry, M. The aggression questionnaire. J Pers Soc Psychol. 1992; 63(3): 452–459.Google Scholar
28. Taylor, SP. Aggressive behavior and physiological arousal as a function of provocation and the tendency to inhibit aggression. J Pers. 1967; 35(2): 297–310.Google Scholar
29. Cherek, DR, Moeller, FG, Dougherty, DM, Rhoades, H. Studies of violent and nonviolent male parolees: II. Laboratory and psychometric measurements of impulsivity. Biol Psychiatry. 1997; 41(5): 523–529.Google Scholar
30. Soyka, M. Neurobiology of aggression and violence in schizophrenia. Schizophr Bull. 2011; 37(5): 913–920.Google Scholar
31. Hoptman, MJ, Antonius, D. Neuroimaging correlates of aggression in schizophrenia: an update. Curr Opin Psychiatry. 2011; 24(2): 100–106.CrossRefGoogle ScholarPubMed
32. Weiss, EM. Neuroimaging and neurocognitive correlates of aggression and violence in schizophrenia. Scientifica. 2012; 2012: 158646.Google Scholar
33. Volavka, J. Neurobiology of Violence, 2nd ed. Washington, DC: American Psychiatric Association; 2001.Google Scholar
34. Hoptman, MJ, Volavka, J, Czobor, P, et al. Aggression and quantitative MRI measures of caudate in patients with chronic schizophrenia or schizoaffective disorder. J Neuropsychiatry Clin Neurosci. 2006; 18(4): 509–515.Google Scholar
35. Hoptman, MJ, Volavka, J, Weiss, EM, et al. Quantitative MRI measures of orbitofrontal cortex in patients with chronic schizophrenia or schizoaffective disorder. Psychiatry Res. 2005; 140(2): 133–145.CrossRefGoogle ScholarPubMed
36. Chakos, MH, Lieberman, JA, Bilder, RM, et al. Increase in caudate nuclei volumes of first-episode schizophrenic patients taking antipsychotic drugs. Am J Psychiatry. 1994; 151(10): 1430–1436.Google Scholar
37. Rüsch, N, Spoletini, I, Wilke, M, et al. Inferior frontal white matter volume and suicidality in schizophrenia. Psychiatry Res. 2008; 164(3): 206–214.CrossRefGoogle ScholarPubMed
38. Narayan, VM, Narr, KL, Kumari, V, et al. Regional cortical thinning in subjects with violent antisocial personality disorder or schizophrenia. Am J Psychiatry. 2007; 164(9): 1418–1427.CrossRefGoogle ScholarPubMed
39. Hoptman, MJ, Volavka, J, Johnson, G, Weiss, E, Bilder, RM, Lim, KO. Frontal white matter microstructure, aggression, and impulsivity in men with schizophrenia: a preliminary study. Biol Psychiatry. 2002; 52(1): 9–14.CrossRefGoogle ScholarPubMed
40. Raine, A, Buchsbaum, MS, Stanley, J, Lottenberg, S, Abel, L, Stoddard, J. Selective reductions in prefrontal glucose metabolism in murderers. Biol Psychiatry. 1994; 36(6): 365–373.Google Scholar
41. Volkow, ND, Tancredi, LR, Grant, C, et al. Brain glucose metabolism in violent psychiatric patients: a preliminary study. Psychiatry Res. 1995; 61(4): 243–253.CrossRefGoogle ScholarPubMed
42. Wong, MTH, Fenwick, PBC, Lumsden, J, et al. Positron emission tomography in male violent offenders with schizophrenia. Psychiatry Res. 1997; 68(2): 111–123.CrossRefGoogle ScholarPubMed
43. Joyal, C, Putkonen, A, Mancini-Marie, A, et al. Violent persons with schizophrenia and comorbid disorders: a functional magnetic resonance imaging study. Schizophr Res. 2007; 91(1): 97–102.Google Scholar
44. Kumari, V, Das, M, Taylor, PJ, et al. Neural and behavioural responses to threat in men with a history of serious violence and schizophrenia or antisocial personality disorder. Schizophr Res. 2009; 110(1): 47–58.CrossRefGoogle ScholarPubMed
45. Dolan, MC, Fullam, RS. Psychopathy and functional magnetic resonance imaging blood oxygenation level-dependent responses to emotional faces in violent patients with schizophrenia. Biol Psychiatry. 2009; 66(6): 570–577.Google Scholar
46. Hoptman, MJ, D’Angelo, D, Catalano, D, et al. Amygdalofrontal functional disconnectivity and aggression in schizophrenia. Schizophr Bull. 2010; 36(5): 1020–1028.Google Scholar
47. Szeszko, PR. Aggression in schizophrenia and its relationship to neural circuitry of urgency. Am J Psychiatry. 2014; 171(9): 897–900.Google Scholar
48. Davidson, RJ, Putnam, KM, Larson, CL. Dysfunction in the neural circuitry of emotion regulation—a possible prelude to violence. Science. 2000; 289(5479): 591–594.CrossRefGoogle ScholarPubMed
49. Kring, AM, Werner, KH. Emotion regulation and psychopathology. In: Philippot P, Feldman RS, eds. The Regulation of Emotion. Mahwah, NJ: Lawrence Erlbaum Associates; 2004: 359–385.Google Scholar
50. Gross, JJ, Jazaieri, H. Emotion, emotion regulation, and psychopathology: an affective science perspective. Clinical Psychological Science. 2014; 2(4): 387–401.Google Scholar
51. Perry, Y, Henry, JD, Nangle, MR, Grisham, JR. Regulation of negative affect in schizophrenia: the effectiveness of acceptance versus reappraisal and suppression. J Clin Exp Neuropsychol. 2012; 34(5): 497–508.Google Scholar
52. Krakowski, MI, Czobor, P, Citrome, L, Bark, N, Cooper, TB. Atypical antipsychotic agents in the treatment of violent patients with schizophrenia and schizoaffective disorder. Arch Gen Psychiatry. 2006; 63(6): 622–629.CrossRefGoogle ScholarPubMed
53. Volavka, J, Czobor, P, Nolan, K, et al. Overt aggression and psychotic symptoms in patients with schizophrenia treated with clozapine, olanzapine, risperidone, or haloperidol. J Clin Psychopharmacol. 2004; 24(2): 225–228.Google Scholar
54. Arango, V, Underwood, MD, Mann, JJ. Serotonin brain circuits involved in major depression and suicide. Prog Brain Res. 2002; 136: 443–453.Google Scholar
55. Citrome, L, Volavka, J. The psychopharmacology of violence: making sensible decisions. CNS Spectr. 2014; 19(5): 411–418.Google Scholar
56. Biswal, BB, Mennes, M, Zuo, XN, et al. Toward discovery science of human brain function. Proc Natl Acad Sci U S A. 2010; 107(10): 4734–4739.Google Scholar
57. Bersani, F, Minichino, A, Enticott, P, et al. Deep transcranial magnetic stimulation as a treatment for psychiatric disorders: a comprehensive review. Eur Psychiatry. 2013; 28(1): 30–39.Google Scholar
58. LaConte, SM, Peltier, SJ, Hu, XP. Real-time fMRI using brain-state classification. Hum Brain Mapp. 2007; 28(10): 1033–1044.CrossRefGoogle ScholarPubMed
59. Raichle, ME, MacLeod, AM, Snyder, AZ, Powers, WJ, Gusnard, DA, Shulman, GL. A default mode of brain function. Proc Natl Acad Sci U S A. 2001; 98(2): 676–682.CrossRefGoogle ScholarPubMed
60. Gusnard, DA, Akbudak, E, Shulman, GL, Raichle, ME. Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc Natl Acad Sci U S A. 2001; 98(7): 4259–4264.Google Scholar
61. Ruiz, S, Lee, S, Soekadar, SR, et al. Acquired self-control of insula cortex modulates emotion recognition and brain network connectivity in schizophrenia. Hum Brain Mapp. 2013; 34(1): 200–212.Google Scholar
62. Hampson, M, Stoica, T, Saksa, J, et al. Real-time fMRI biofeedback targeting the orbitofrontal cortex for contamination anxiety. J Vis Exp. 2012; (59): 3535.Google Scholar
63. Sitaram, R, Caria, A, Veit, R, Gaber, T, Ruiz, S, Birbaumer, N. Volitional control of the anterior insula in criminal psychopaths using real-time fMRI neurofeedback: a pilot study. Front Behav Neurosci. 2014; 8: 344.Google Scholar
64. Keers, R, Ullrich, S, DeStavola, BL, Coid, JW. Association of violence with emergence of persecutory delusions in untreated schizophrenia. Am J Psychiatry. 2014; 171(3): 332–339.CrossRefGoogle ScholarPubMed
65. Coid, JW, Ullrich, S, Kallis, C, et al. The relationship between delusions and violence: findings from the East London first episode psychosis study. JAMA Psychiatry. 2013; 70(5): 465–471.Google Scholar
66. Johnson, SL, Carver, CS, Joormann, J. Impulsive responses to emotion as a transdiagnostic vulnerability to internalizing and externalizing symptoms. J Affect Disord. 2013; 150(3): 872–878.Google Scholar
67. Dambacher, F, Sack, AT, Lobbestael, J, Arntz, A, Brugman, S, Schuhmann, T. Out of control evidence for anterior insula involvement in motor impulsivity and reactive aggression. Soc Cogn Affect Neurosci. doi:10.1093/scan/nsu077.Google Scholar
68. Dambacher, F, Sack, AT, Lobbestael, J, Arntz, A, Brugmann, S, Schuhmann, T. The role of right prefrontal and medial cortex in response inhibition: Interfering with action restraint and action cancellation using transcranial magnetic brain stimulation. J Cogn Neurosci. 2014; 26(8): 1775–1784.Google Scholar
69. Warburton, K. The new mission of forensic mental health services: managing violence as a medical syndrome in an environment that balances treatment and safety. CNS Spectr. 2014; 19(5): 368–373.CrossRefGoogle Scholar
70. Stahl, SM, Morrissette, DA, Cummings, M, et al. California State Hospital Violence Assessment and Treatment (Cal-VAT). CNS Spectr. 2014; 19(5): 449–465.CrossRefGoogle ScholarPubMed