Functional Connectivity Bias in the Prefrontal Cortex of Psychopaths

Oren Contreras-Rodríguez; Jesus Pujol; Iolanda Batalla; Ben J Harrison; Carles Soriano-Mas; Joan Deus; Marina López-Solà; Dídac Macià; Vanessa Pera; Rosa Hernández-Ribas; Josep Pifarré; José M Menchón; Narcís Cardoner

doi:10.1016/j.biopsych.2014.03.007

Functional Connectivity Bias in the Prefrontal Cortex of Psychopaths

Biol Psychiatry. 2015 Nov 1;78(9):647-55. doi: 10.1016/j.biopsych.2014.03.007. Epub 2014 Mar 14.

Authors

Affiliations

¹ Bellvitge Biomedical Research Institute-IDIBELL (OC-R, CS-M, RH-R, JMM, NC), Psychiatry Department, Bellvitge University Hospital, CIBERSAM at Barcelona; Department of Clinical Psychology and Institute of Neuroscience F. Olóriz (OC-R), University of Granada; MRI Research Unit (OC-R, JPu, BJH, JD, ML-S, DM), CRC Mar, Hospital del Mar at Barcelona, Spain.
² Department of Clinical Psychology and Institute of Neuroscience F. Olóriz (OC-R), University of Granada; MRI Research Unit (OC-R, JPu, BJH, JD, ML-S, DM), CRC Mar, Hospital del Mar at Barcelona, Spain; Centro Investigación Biomédica en Red de Salud Mental (JPu), CIBERSAM G21, Barcelona, Spain. Electronic address: jpujol@crccorp.es.
³ GSS (IB, VP, JPi), Hospital Santa Maria and Biomedical Research Institute at Lleida.
⁴ Department of Clinical Psychology and Institute of Neuroscience F. Olóriz (OC-R), University of Granada; MRI Research Unit (OC-R, JPu, BJH, JD, ML-S, DM), CRC Mar, Hospital del Mar at Barcelona, Spain; Melbourne Neuropsychiatry Centre (BJH), Department of Psychiatry, The University of Melbourne and Melbourne Health, Melbourne, Australia.
⁵ Bellvitge Biomedical Research Institute-IDIBELL (OC-R, CS-M, RH-R, JMM, NC), Psychiatry Department, Bellvitge University Hospital, CIBERSAM at Barcelona.
⁶ Department of Clinical Psychology and Institute of Neuroscience F. Olóriz (OC-R), University of Granada; MRI Research Unit (OC-R, JPu, BJH, JD, ML-S, DM), CRC Mar, Hospital del Mar at Barcelona, Spain; Department of Clinical and Health Psychology (JD), Autonomous University of Barcelona, Spain.
⁷ Department of Clinical Psychology and Institute of Neuroscience F. Olóriz (OC-R), University of Granada; MRI Research Unit (OC-R, JPu, BJH, JD, ML-S, DM), CRC Mar, Hospital del Mar at Barcelona, Spain; Department of Psychology and Neuroscience (ML-S), University of Colorado, Boulder, Colorado.
⁸ Department of Clinical Psychology and Institute of Neuroscience F. Olóriz (OC-R), University of Granada; MRI Research Unit (OC-R, JPu, BJH, JD, ML-S, DM), CRC Mar, Hospital del Mar at Barcelona, Spain.
⁹ GSS (IB, VP, JPi), Hospital Santa Maria and Biomedical Research Institute at Lleida; Child-Juvenile Mental Health Center of Sant Joan de Déu at Lleida (VP), Lleida, Spain.

PMID: 24742618
DOI: 10.1016/j.biopsych.2014.03.007

Abstract

Background: Psychopathy is characterized by a distinctive interpersonal style that combines callous-unemotional traits with inflexible and antisocial behavior. Traditional emotion-based perspectives link emotional impairment mostly to alterations in amygdala-ventromedial frontal circuits. However, these models alone cannot explain why individuals with psychopathy can regularly benefit from emotional information when placed on their focus of attention and why they are more resistant to interference from nonaffective contextual cues. The present study aimed to identify abnormal or distinctive functional links between and within emotional and cognitive brain systems in the psychopathic brain to characterize further the neural bases of psychopathy.

Methods: High-resolution anatomic magnetic resonance imaging with a functional sequence acquired in the resting state was used to assess 22 subjects with psychopathy and 22 control subjects. Anatomic and functional connectivity alterations were investigated first using a whole-brain analysis. Brain regions showing overlapping anatomic and functional changes were examined further using seed-based functional connectivity mapping.

Results: Subjects with psychopathy showed gray matter reduction involving prefrontal cortex, paralimbic, and limbic structures. Anatomic changes overlapped with areas showing increased degree of functional connectivity at the medial-dorsal frontal cortex. Subsequent functional seed-based connectivity mapping revealed a pattern of reduced functional connectivity of prefrontal areas with limbic-paralimbic structures and enhanced connectivity within the dorsal frontal lobe in subjects with psychopathy.

Conclusions: Our results suggest that a weakened link between emotional and cognitive domains in the psychopathic brain may combine with enhanced functional connections within frontal executive areas. The identified functional alterations are discussed in the context of potential contributors to the inflexible behavior displayed by individuals with psychopathy.

Keywords: Amygdala; Dorsal executive network; Flexible self-regulation; Functional magnetic resonance imaging; Psychopathy; Resting-state functional connectivity.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adult
Antisocial Personality Disorder / pathology*
Antisocial Personality Disorder / physiopathology*
Brain Mapping
Gray Matter / pathology
Gray Matter / physiopathology
Humans
Image Processing, Computer-Assisted
Magnetic Resonance Imaging
Male
Middle Aged
Neural Pathways / pathology
Neural Pathways / physiopathology
Organ Size
Prefrontal Cortex / pathology*
Prefrontal Cortex / physiopathology*
Psychiatric Status Rating Scales
Rest