Impaired emotion processing in functional (psychogenic) tremor: A functional magnetic resonance imaging study

Abstract

Background: Despite its high prevalence and associated disability, the neural correlates of emotion processing in patients with functional (psychogenic) tremor (FT), the most common functional movement disorder, remain poorly understood.

Methods: In this cross sectional functional magnetic resonance imaging (fMRI) study at 4T, 27 subjects with FT, 16 with essential tremor (ET), and 25 healthy controls (HCs) underwent a finger-tapping motor task, a basic-emotion task, and an intense-emotion task to probe motor and emotion circuitries. Anatomical and functional MRI data were processed with FSL (FMRIB Software Library) and AFNI (Analysis of Functional Neuroimages), followed by seed-to-seed connectivity analyses using anatomical regions defined from the Harvard-Oxford subcortical atlas; all analyses were corrected for multiple comparisons.

Results: After controlling for depression scores and correcting for multiple comparisons, the FT group showed increased activation in the right cerebellum compared to ET during the motor task; and increased activation in the paracingulate gyrus and left Heschl's gyrus compared with HC with decreased activation in the right precentral gyrus compared with ET during the basic-emotion task. No significant differences were found after adjusting for multiple comparisons during the intense-emotion task but increase in connectivity between the left amygdala and left middle frontal gyrus survived corrections in the FT subjects during this task, compared to HC.

Conclusions: In response to emotional stimuli, functional tremor is associated with alterations in activation and functional connectivity in networks involved in emotion processing and theory of mind. These findings may be relevant to the pathophysiology of functional movement disorders.

Keywords: AFNI, Analysis of Functional Neuroimages; CPT-END, continuous performance task with emotional and neutral distracters; Conversion disorder; EPI, echo-planar imaging; Emotion processing; FSL, FMRIB Software Library; FT, functional tremor; Functional movement disorders; Functional tremor; HAM-A, Hamilton Anxiety Rating Scale; HAM-D, Hamilton Depression Rating Scale; MDEFT, modified equilibrium Fourier transform; MINI, Mini International Neuropsychiatric Interview; Psychogenic tremor; fMRI; fMRI, functional magnetic resonance imaging.

Fig. 1

Regions of interest used in connectivity analysis based on the activation patterns from the intense-emotion task and subcortical atlas. The anatomical regions of interest included the anterior cingulate gyrus, posterior cingulate gyrus and left and right regions of the uncus/amygdala, thalamus, caudate, putamen, and subthalamic nuclei. The regions from the group activation of the task included regions in the left cerebral cortex, right frontal pole, right postcentral gyrus, left precuneus cortex and right superior frontal gyrus along with two regions in the left lateral occipital cortex, two regions in the left cingulate gyrus, three regions in the right lateral occipital cortex, and regions in the left and right middle frontal gyrus.

Fig. 2

Differences in fMRI activation for the finger-tapping task. A region in the right cerebellum with increased activation in the FT group compared to ET during right tapping compared to rest. Images are shown at a threshold of Z > 2.3 and p < 0.05 corrected, after controlling for HAM-D.

Fig. 3

Differences in fMRI activation for the basic-emotion task (sad greater than neutral faces). Above, paracingulate gyrus and left Heschl's gyrus showed greater activation in the FT group than HC. Below, right precentral gyrus showed reduced activation in the FT compared to ET. Images are shown at a threshold of Z > 2.3 and p < 0.05 corrected, controlling for HAM-D.