Hypoactive medial prefrontal cortex functioning in adults reporting childhood emotional maltreatment

Anne-Laura van Harmelen; Marie-José van Tol; Tim Dalgleish; Nic J A van der Wee; Dick J Veltman; André Aleman; Philip Spinhoven; Brenda W J H Penninx; Bernet M Elzinga

doi:10.1093/scan/nsu008

Hypoactive medial prefrontal cortex functioning in adults reporting childhood emotional maltreatment

Soc Cogn Affect Neurosci. 2014 Dec;9(12):2026-33. doi: 10.1093/scan/nsu008. Epub 2014 Feb 3.

Authors

Anne-Laura van Harmelen¹, Marie-José van Tol², Tim Dalgleish³, Nic J A van der Wee², Dick J Veltman³, André Aleman³, Philip Spinhoven², Brenda W J H Penninx², Bernet M Elzinga²

Affiliations

¹ Leiden Institute for Brain and Cognition (LIBC), Postzone C2-S, P.O. Box 9600, 2300 RC Leiden, the Netherlands, Clinical, Health and Neuropsychology Unit, Leiden University, Pieter de la Court Gebouw, Wassenaarseweg 52, 2333 AK Leiden, the Netherlands, Department of Developmental Psychiatry, University of Cambridge School of Clinical Medicine, Box 189 Cambridge Biomedical Campus, Cambridge, UK, CB2 2QQ, Department of Psychiatry, Leiden University Medical Center, Albinusdreef 2, 2333 ZA Leiden, the Netherlands, Neuro-imaging Center, University Medical Center Groningen, and Department of Psychology, University of Groningen, Antonius Deusinglaan 29713 AW Groningen, the Netherlands, Medical Research Council, Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge, UK CB2 7EF, and Department of Psychiatry, VU University Medical Center, A.J. Ernststraat 1187, 1081 HL Amsterdam, the Netherlands Leiden Institute for Brain and Cognition (LIBC), Postzone C2-S, P.O. Box 9600, 2300 RC Leiden, the Netherlands, Clinical, Health and Neuropsychology Unit, Leiden University, Pieter de la Court Gebouw, Wassenaarseweg 52, 2333 AK Leiden, the Netherlands, Department of Developmental Psychiatry, University of Cambridge School of Clinical Medicine, Box 189 Cambridge Biomedical Campus, Cambridge, UK, CB2 2QQ, Department of Psychiatry, Leiden University Medical Center, Albinusdreef 2, 2333 ZA Leiden, the Netherlands, Neuro-imaging Center, University Medical Center Groningen, and Department of Psychology, University of Groningen, Antonius Deusinglaan 29713 AW Groningen, the Netherlands, Medical Research Council, Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge, UK CB2 7EF, and Department of Psychiatry, VU University Medical Center, A.J. Ernststraat 1187, 1081 HL Amsterdam, the Netherlands Leiden Institute for Brain and Cognition (LIBC), Postzone C2-S, P.O. Box 9600, 2300 RC Leiden, the Netherlands, Clinical, Health and Neuropsychology Unit, Leiden University, Pieter de la
² Leiden Institute for Brain and Cognition (LIBC), Postzone C2-S, P.O. Box 9600, 2300 RC Leiden, the Netherlands, Clinical, Health and Neuropsychology Unit, Leiden University, Pieter de la Court Gebouw, Wassenaarseweg 52, 2333 AK Leiden, the Netherlands, Department of Developmental Psychiatry, University of Cambridge School of Clinical Medicine, Box 189 Cambridge Biomedical Campus, Cambridge, UK, CB2 2QQ, Department of Psychiatry, Leiden University Medical Center, Albinusdreef 2, 2333 ZA Leiden, the Netherlands, Neuro-imaging Center, University Medical Center Groningen, and Department of Psychology, University of Groningen, Antonius Deusinglaan 29713 AW Groningen, the Netherlands, Medical Research Council, Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge, UK CB2 7EF, and Department of Psychiatry, VU University Medical Center, A.J. Ernststraat 1187, 1081 HL Amsterdam, the Netherlands Leiden Institute for Brain and Cognition (LIBC), Postzone C2-S, P.O. Box 9600, 2300 RC Leiden, the Netherlands, Clinical, Health and Neuropsychology Unit, Leiden University, Pieter de la Court Gebouw, Wassenaarseweg 52, 2333 AK Leiden, the Netherlands, Department of Developmental Psychiatry, University of Cambridge School of Clinical Medicine, Box 189 Cambridge Biomedical Campus, Cambridge, UK, CB2 2QQ, Department of Psychiatry, Leiden University Medical Center, Albinusdreef 2, 2333 ZA Leiden, the Netherlands, Neuro-imaging Center, University Medical Center Groningen, and Department of Psychology, University of Groningen, Antonius Deusinglaan 29713 AW Groningen, the Netherlands, Medical Research Council, Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge, UK CB2 7EF, and Department of Psychiatry, VU University Medical Center, A.J. Ernststraat 1187, 1081 HL Amsterdam, the Netherlands.
³ Leiden Institute for Brain and Cognition (LIBC), Postzone C2-S, P.O. Box 9600, 2300 RC Leiden, the Netherlands, Clinical, Health and Neuropsychology Unit, Leiden University, Pieter de la Court Gebouw, Wassenaarseweg 52, 2333 AK Leiden, the Netherlands, Department of Developmental Psychiatry, University of Cambridge School of Clinical Medicine, Box 189 Cambridge Biomedical Campus, Cambridge, UK, CB2 2QQ, Department of Psychiatry, Leiden University Medical Center, Albinusdreef 2, 2333 ZA Leiden, the Netherlands, Neuro-imaging Center, University Medical Center Groningen, and Department of Psychology, University of Groningen, Antonius Deusinglaan 29713 AW Groningen, the Netherlands, Medical Research Council, Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge, UK CB2 7EF, and Department of Psychiatry, VU University Medical Center, A.J. Ernststraat 1187, 1081 HL Amsterdam, the Netherlands.

Abstract

Childhood emotional maltreatment (CEM) has adverse effects on medial prefrontal cortex (mPFC) morphology, a structure that is crucial for cognitive functioning and (emotional) memory and which modulates the limbic system. In addition, CEM has been linked to amygdala hyperactivity during emotional face processing. However, no study has yet investigated the functional neural correlates of neutral and emotional memory in adults reporting CEM. Using functional magnetic resonance imaging, we investigated CEM-related differential activations in mPFC during the encoding and recognition of positive, negative and neutral words. The sample (N = 194) consisted of patients with depression and/or anxiety disorders and healthy controls (HC) reporting CEM (n = 96) and patients and HC reporting no abuse (n = 98). We found a consistent pattern of mPFC hypoactivation during encoding and recognition of positive, negative and neutral words in individuals reporting CEM. These results were not explained by psychopathology or severity of depression or anxiety symptoms, or by gender, level of neuroticism, parental psychopathology, negative life events, antidepressant use or decreased mPFC volume in the CEM group. These findings indicate mPFC hypoactivity in individuals reporting CEM during emotional and neutral memory encoding and recognition. Our findings suggest that CEM may increase individuals' risk to the development of psychopathology on differential levels of processing in the brain; blunted mPFC activation during higher order processing and enhanced amygdala activation during automatic/lower order emotion processing. These findings are vital in understanding the long-term consequences of CEM.

Keywords: Anxiety; childhood abuse; depression; emotional maltreatment; magnetic resonance imaging (MRI); medial prefrontal cortex (PFC).

Publication types

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

MeSH terms

Adult
Analysis of Variance
Child
Child Abuse / psychology*
Female
Humans
Image Processing, Computer-Assisted
Magnetic Resonance Imaging
Male
Middle Aged
Mood Disorders / etiology
Mood Disorders / pathology*
Neuropsychological Tests
Prefrontal Cortex / physiopathology*
Psychiatric Status Rating Scales
Psychometrics
Recognition, Psychology / physiology*

Grants and funding

MC_U105579215/MRC_/Medical Research Council/United Kingdom