Review Article

Effects of Subthalamic Nucleus Deep Brain Stimulation on Facial Emotion Recognition in Parkinson’s Disease: A Critical Literature Review

Table 1

Studies accessing facial emotion recognition after STN DBS in PD.

StudyNumber of participants (m, f)FER test stimuli (number of stimuli and emotions, display time)Age (years)Disease duration (years)Hoehn and \Yahr score (pre-DBS)LED mean (mg/day) pre-DBS//post-DBSAssessment conditionsAssessment time (range)Outcome

Schroeder et al. 2004 [43]10 PD (6m, 4f)4 blocks each of 60 computer-transformed facial stimuli from the Ekman and Friesen series, 6 emotions, each stimulus containing different intensities of two emotions, display time n/an/an/a//600ON STN vs. OFF STN (med off) months (3-24) after DBSAnger recognition accuracy significantly reduced in the ON STN condition

Dujardin et al. 2004 [40]12 PD (5m, 7f)
12 HC
12 facial stimuli from Hess and Blairy series, (male and female), more than 3 sec4 (3-5) off med statePre vs. post op (med on vs. med on, STN ON)Before and 3 months after DBSSign. reduction of total FER accuracy, sadness, and anger, (trend for disgust) regardless of expression intensity

Biseul et al. 2005 [44]Different PD patients before and after DBS (15 (9m, 6f) in each group, matched for disease duration)
15 HC
55 facial stimuli from Ekman and Friesen series, 7 emotions, 3 s years (post-DBS group) years (post-DBS group)n/an/aPre vs. post DBS
ON vs. OFF STN
(on med in all conditions)
Before and months after DBS (1-48 months)Pre- vs. post-DBS: sign. reduction of fear accuracy (either ON or OFF STN) post-DBS
ON vs. OFF STN: no sign. difference for all emotions

Geday et al. 2006 [66]7 PD
22 HC
6 series each of 30 facial stimuli from the Empathy Picture System, 3 emotions (sadness, neutral, happiness), 3 sec yearsn/an/an/aON vs. OFF STN DBS (med off)3-25 months after DBSFaces were scored as less pleasant ON DBS in comparison to OFF (rating on a scale from -3 to +3)

Drapier et al. 2008 [63]17 PD (11m, 6f)55 facial stimuli from Ekman and Friesen series, 7 emotions, 3 sec (on med)Pre- vs. post-op (med on vs. med on, STN ON)3 months before and 3 months after DBSSign. reduction in the recognition accuracy of fear and sadness

Le Jeune et al. 2008 [42]13 PD (9m, 4f)
30 HC
55 facial stimuli from Ekman and Friesen, 7 emotions, 3 sec (on med)Pre- vs. post-op (on med vs. on med, ON STN)3 months before and 3 months afterSign. reduction of total FER and fear score

Peron et al. 2010 [41]24 PD STN DBS (17 m, 7f), 20 treated with apomorphine (APO), 30 HC55 facial stimuli from Ekman and Friesen, 7 emotions, 3 sec (on med)Pre vs. post (med on vs. med on, STN ON)3 months before and 3 months after DBSSign. reduction of total FER accuracy, sadness, fear after DBS

Mondillon et al. 2012 [62]14 PD (9m, 5f)
14 HC
56 facial stimuli in each block from Karolinska directed emotional faces database, 7 emotions, 500 msn/apost-DBS 4 conditions post-op
(med off, STN OFF; med off, STN ON; med on, STN ON; med on, STN OFF)
At least 6 months after ( year)ON vs. OFF STN DBS (off med): sign. worse recognition accuracy in ON condition
ON vs. OFF STN DBS (on med): better FER recognition accuracy in ON condition
Greater FER benefit when two therapies (L-Dopa, DBS) combined

Aiello et al. 2014 [46]12 PD (8m, 4f)
13 HC
30 facial stimuli from Nim Stim Set, 6 emotions, display time n/an/an/aPre- (on- and off- medication) vs. post-DBS (on med, OFF STN and on med, ON STN)Before and after DBS:
OFF STN: 5 days after
ON STN: 2-6 months after
Pre- vs. post-DBS (on med vs. on med, ON STN): no sign. FER accuracy difference
Pre- vs. post-DBS (on med vs. on med, OFF STN): no sign. FER accuracy difference
ON vs. OFF stimulation (on med): no sign. FER accuracy difference

Albuquerque et al. 2014 [47]30 PD (18m, 12f)16 facial stimuli from CATS, 7 emotions, no time limits (on med)Pre vs. post-op (on med vs. on med, STN ON)Before DBS and 1 year afterNo sign. accuracy difference in FER tasks (neither for positive nor for negative emotions)

Mermillod et al. 2014 [65]14 PD (9m, 5f)
14 HC
105 facial stimuli from the Ekman and Friesen series in broad (BSF), high ( cycles/image) and low ( cycles/image) spatial frequency resolutions, 7 emotions, 200 msn/apost-DBS Post-DBS (4 conditions: med off, STN OFF; med on, STN OFF; med off, STN ON; med on, STN ON)At least 6 months after DBS ( years)ON vs. OFF: no sign. effect of stimulation for BSF and LSF faces, lower total FER accuracy for HSF in the ON condition

McIntosh et al. 2015 [49]Two early PD groups: 7 PD (5m, 2f) optimal drug therapy, 9 PD (8m, 1f) optimal drug therapy and STN DBS, 21 matched young and 23 aged HCFacial emotional stimuli from TASIT (EET part, 28 stimuli) and RMET test (36 pictures), complex emotions, display time n/a (optimal drug therapy+DBS group)n/a≤2 (optimal drug therapy + DBS group)ON drug therapy and optimal DBS
OFF med (24 h) and OFF DBS (24 h)
n/aNo accuracy difference between the PD groups (optimal drug therapy or optimal drug therapy and DBS) or treatment conditions (ON, OFF)

Enrici et al. 2017 [48]18 PD (9m, 9f) STN DBS
20 PD receiving DRT
20 HC
60 pictures of Ekman test, 6 basic emotions, display time n/a (STN-DBS group) (STN-DBS group) (on med)STN-DBS group:
DRT-PD group:
On med (DRT-PD group) on med, ON STN (STN-DBS group)1.72 (±1.18) yearsNo statistically sign. FER accuracy differences between the DRT-PD and STN-DBS groups

Wagenbreth et al. 2019 [45]14 PD (10m, 4f)Implicit and explicit emotional processing task, regions around the eyes from the Ekman 60 faces test, 112 stimuli (16 faces, 96 words),
4 emotions (happiness, fear, disgust, neutral), no time limit
n/aPost-DBS On med, ON STN vs. OFF med, OFF STN months after DBS (3-77 months)STN-DBS ON vs. OFF: for the explicit emotional processing task in the ON condition general decrease in response accuracy, sign. decrease in accuracy and longer reaction time for disgust, improved accuracy for fear

Abbreviations: STN: subthalamic nucleus; DBS: deep brain stimulation; FER: facial emotion recognition; PD: Parkinson’s disease; HC: healthy controls; sd: standard deviation; n/a: not available; m: male; f: female; 7 emotions: happiness, sadness, fear, surprise, disgust, anger, and no emotion; ms: milliseconds; LED: levodopa equivalent dose; vs.: versus; sign.: significant; med: medication; ON STN: on stimulation; OFF STN: off stimulation; DRT: dopamine replacement therapy; CATS: comprehensive affect testing system; TASIT: Awareness of Social Inference Test; EET: Emotion Evaluation Test; RMET: reading the mind in the eye task; BSF: broad spatial frequency; HSF: high spatial frequency; LSF: low spatial frequency. Calculated from reported data. Note: the outcome refers to comparisons of PD patients’ different conditions (not comparisons with HC).