Facial emotion processing in patients with seizure disorders

Jerzy P Szaflarski; Jane B Allendorfer; Rodolphe Nenert; W Curt LaFrance Jr; Helen I Barkan; Jennifer DeWolfe; Sandipan Pati; Ashley E Thomas; Lawrence Ver Hoef

doi:10.1016/j.yebeh.2017.12.004

Facial emotion processing in patients with seizure disorders

Epilepsy Behav. 2018 Feb:79:193-204. doi: 10.1016/j.yebeh.2017.12.004. Epub 2018 Jan 6.

Authors

Jerzy P Szaflarski¹, Jane B Allendorfer², Rodolphe Nenert³, W Curt LaFrance Jr⁴, Helen I Barkan⁵, Jennifer DeWolfe⁵, Sandipan Pati⁵, Ashley E Thomas⁵, Lawrence Ver Hoef⁵

Affiliations

¹ Department of Neurology, University of Alabama at Birmingham, Birmingham, AL, USA; UAB Epilepsy Center, University of Alabama at Birmingham, Birmingham, AL, USA. Electronic address: jszaflarski@uabmc.edu.
² Department of Neurology, University of Alabama at Birmingham, Birmingham, AL, USA; UAB Epilepsy Center, University of Alabama at Birmingham, Birmingham, AL, USA. Electronic address: jallendorfer@uabmc.edu.
³ Department of Neurology, University of Alabama at Birmingham, Birmingham, AL, USA.
⁴ Departments of Neurology and Psychiatry, Rhode Island Hospital, Brown University, Providence, RI, USA.
⁵ Department of Neurology, University of Alabama at Birmingham, Birmingham, AL, USA; UAB Epilepsy Center, University of Alabama at Birmingham, Birmingham, AL, USA.

PMID: 29309953
DOI: 10.1016/j.yebeh.2017.12.004

Abstract

Studies of emotion processing are needed to better understand the pathophysiology of psychogenic nonepileptic seizures (PNES). We examined the differences in facial emotion processing between 12 patients with PNES, 12 patients with temporal lobe epilepsy (TLE), and 24 matched healthy controls (HCs) using fMRI with emotional faces task (EFT) (happy/sad/fearful/neutral) and resting state connectivity. Compared with TLE, patients with PNES exhibited increased fMRI response to happy, neutral, and fearful faces in visual, temporal, and/or parietal regions and decreased fMRI response to sad faces in the putamen bilaterally. Regions showing significant differences between PNES and TLE were used as functional seed regions of interest (ROIs), in addition to amygdala structural seed ROIs for resting state functional connectivity analyses. Whole brain analyses showed that compared with TLE and HCs, patients with PNES exhibited increased functional connectivity of the functional seed ROIs to several brain regions, particularly to cerebellar, visual, motor, and frontotemporal regions. Connectograms showed increased functional connections between left parahippocampal gyrus/uncus ROIs and right temporal ROIs in PNES compared with both the TLE and HC groups. Resting state functional connectivity of the left and right amygdala to various brain regions including emotion regulation and motor control circuits was increased in PNES when compared with those with TLE. This study provides preliminary evidence that patients with PNES exhibit altered facial emotion processing compared with patients with TLE and HCs and increased amygdala functional connectivity compared with TLE. These findings identify potential key differences in facial emotion processing reflective of neurophysiologic markers of neural circuitry alterations that can be used to generate further hypotheses for developing studies that examine the contributions of emotion processing to the development and maintenance of PNES.

Keywords: Conversion disorder; Emotion processing; Face processing task; Functional connectivity; PNES; Psychogenic nonepileptic seizures; Temporal lobe epilepsy; fMRI.

MeSH terms

Adult
Amygdala / physiopathology
Brain / physiopathology
Cerebellum / physiopathology
Emotions / physiology*
Epilepsy, Temporal Lobe* / physiopathology
Facial Expression*
Fear
Female
Humans
Magnetic Resonance Imaging
Male
Parahippocampal Gyrus / physiopathology
Seizures / physiopathology*
Young Adult