Table 1.
Summaries of the studies investigating the effects of non-invasive brain stimulation applied over the dorsolateral prefrontal cortex on mood, emotional processing, and attentional processing of emotional information in healthy individuals.
| References | Study design | N (Males) | Mean age in years | Site of stimulation* | NIBS parameters** | Experimental outcomes (Time of assessment) | Main results |
|---|---|---|---|---|---|---|---|
| (A) EFFECTS OF NIBS ON MOOD | |||||||
| rTMS studies | |||||||
| Schaller et al., 2011 | Parallel Sham controlled 9 rTMS sessions |
44 (44) | Range: 19–33 | L DLPFC (5 cm anterior to M1) |
25 Hz 15 trains of 2 s 8 s ITI 750 pulses Increasing MT across sessions (from 100 to 136.9%) |
1. BDI 2. 6-item mood VAS: happy/unhappy, cheerful/sad, energetic/lack of energy, lively/gloomy, even-tempered/restless, serious/smiling (day 0, day 5, day 9) |
Active vs. sham rTMS: 1. BDI: Reduced sum scores and scores on "libido", "fatigability" and "weight loss" at day 5 and 9 2. Mood VAS: No effect |
| Baeken et al., 2010 | Parallel No sham |
10 (0) | N/A | L DLPFC (MRI BN) |
10 Hz 40 trains of 3.9 s 26.1 s ITI 1560 pulses 100% MT |
1. POMS-32 (t0, t1) | Before vs. after active L DLPFC rTMS: 1. POMS-32: No effect Before vs. after active R DLPFC rTMS: 1. POMS-32: No effect |
| 10 (0) | N/A | R DLPFC (MRI BN) |
|||||
| Hoy et al., 2010 | Crossover Sham controlled rTMS combined with exposure to positive or neutral pictures |
10 (4) | 31.2 | L DLPFC (10/20 EEG) |
5 Hz 30 trains of 10 s 20 s ITI 1500 pulses 120% MT |
1. AGN task with happy and sad words 2. 5-item mood VAS: sadness, happiness, tiredness, anxiety, pain-discomfort 3. Valence and arousal ratings on IAPS pictures (t0, t1) |
Active vs. sham rTMS: 1. AGN task: No effect 2. Mood VAS: No effect 3. Valence and arousal ratings: No effect |
| Baeken et al., 2008 | Crossover Sham controlled |
27 (0) | 25.2 | R DLPFC (MRI BN) |
10 Hz 40 trains of 4.9 s 26.1 s ITI 1560 pulses 110% MT |
1.5-item mood VAS: sadness, tension, vigor, anger, tiredness 2. POMS-32 (t0, t1, t30) |
Active R DLPFC vs. sham rTMS: 1. Mood VAS: No effect 2. POMS-32: No effect |
| Crossover Sham controlled |
20 (0) | 25.6 | L DLPFC (MRI BN) |
10 Hz 40 trains of 4.9 s 26.1 s ITI 1560 pulses 110% MT |
1.5-item mood VAS: sadness, tension, vigor, anger, tiredness 2. POMS-32 (t0, t1, t30) |
Active L DLPFC vs. sham rTMS: 1. Mood VAS: No effect 2. POMS-32: No effect |
|
| Baeken et al., 2006 | Crossover Sham controlled |
28 (0) | 28.7 | L DLPFC (MRI BN) |
10 Hz 40 trains of 3.9 s 26.1 s ITI 1560 pulses 110% MT |
1.5-item mood VAS: sadness, tension, vigor, anger, tiredness 2. POMS-32 (t0, t1, t30) |
Active vs. sham rTMS: 1. Mood VAS: No effect 2. POMS-32: No effect |
| Grisaru et al., 2001 | Crossover Sham controlled |
18 (7) | 40.5 | L DLPFC R DLPFC (5 cm anterior to M1 or M2) |
1 Hz 1 single train 500 pulses 110% MT |
1.4-item mood VAS: irritability, anxiety, depression, happiness (t0, t5, t10, t30, t240) |
Active (either L or R DLPFC ) vs. sham rTMS: 1. Mood VAS: No effect |
| Padberg et al., 2001 | Crossover No sham | 9 (5) | 29.8 | L DLPFC R DLPFC (5 cm anterior to M1 or M2) |
10 Hz 10 trains of 5 s 30 s ITI 500 pulses 110% MT |
1.8-item mood VAS: mood, emotion, general state, anxiety, activity, physical condition, self-perception (t0, t1, t15) 2. Facial expressions recording with ultrasonic signal emitted by mouth and eyes muscles during a funny movie (t0, t1) |
Active rTMS, L vs. R DLPFC: 1. Mood VAS: No effect 2. Facial expressions: Increased frequencies of laughing and shorter RT of laughing movements |
| Schutter et al., 2001 | Crossover Sham controlled |
12 (8) | 28.4 | R DLPFC (10/20 EEG) |
1 Hz 1 single train 1200 pulses 130% MT |
1. STAI 2. STAS (t0, t1, t35, t65) |
Active vs. sham rTMS: 1. STAI: Reduced anxiety 2. STAS: No effect |
| Mosimann et al., 2000 | Crossover Sham controlled |
25 (25) | 22.4 | L PFC (5 cm anterior, 2 cm lateral to M1) | 20 Hz 40 trains of 2 s 30 s ITI 1600 pulses 100% MT |
1.5-item mood VAS: tiredness, happiness, sadness, pain, anxiety (t0, t20) |
Active vs. sham rTMS: 1. Mood VAS: No effect |
| George et al., 1996 | Crossover No sham | 10 (6) | 35 | L DLPFC R DLPFC (5 cm anterior to M1 or M2) |
5 Hz 10 trains of 10 s 1 s ITI 500 pulses 120% MT |
1. NIMH mood scale 2. Forced-choice mood VAS 3. PANAS (t0, t30, t60, t90, t180, t480, t1440) |
Active rTMS, L vs. R DLPFC: 1. NIMH mood scale: Reduced happiness and increased sadness 2. Forced-choice mood-VAS: No effect 3. PANAS: No effect Active rTMS, R vs. L DLPFC: 1. NIMH mood scale: Reduced sadness and increased happiness 2. Forced-choice mood-VAS: No effect 3. PANAS: No effect |
| Pascual-Leone et al., 1996 | Crossover No sham | 10 (4) | Range: 22–27 | L DLPFC R DLPFC (5 cm anterior to M1 or M2) Mid PFC |
10 Hz 10 trains of 10 s 25 s ITI 500 pulses 110% MT |
1.5-item mood VAS: pain discomfort, sadness, happiness, anxiety, tiredness (t0, t1) |
Active rTMS, L vs. R DLPFC: 1. Mood VAS: Decreased happiness and increased sadness Active rTMS, L vs. Mid PFC: 1. Mood VAS: Increased pain/discomfort, anxiety and sadness Active rTMS, R vs. L DLPFC: 1. Mood VAS: Increased happiness |
| tDCS studies | |||||||
| Plewnia et al., 2015 | Parallel Sham controlled |
28 (28) | 27.9 | L DLPFC/R deltoid (10/20 EEG) |
1 mA 20 min 35 cm2 |
1. PANAS 2. PASAT |
1. PANAS: No effect on positive affect. Increase in “upset” item after sham vs. active tDCS 2. PASAT: Shorter inter-stimulus interval after anodal vs. sham tDCS Slower inter-stimulus interval were correlated to increased upset |
| Morgan et al., 2014 | Crossover No sham | 18 (9) | 23.2 | L DLPFC/R DLPFC R DLPFC/L DLPFC (10/20 EEG) |
1 mA 12 min 9 cm2 |
1. PANAS 2. Motivational state questionnaire 3. Memory task with IAPS pictures (t0, t1) |
Active tDCS, L DLPFC/R DLPFCvs. R DLPFC/L DLPFC: 1. PANAS: No effect 2. Motivational state questionnaire: No effect 3. Memory task: No effect |
| Motohashi et al., 2013 | Crossover Sham controlled 4 tDCS sessions |
12 (12) | 22 | L DLPFC/ supraorbital region (10/20 EEG) |
1 mA 20 min 35 cm2 |
1. POMS-30 (day 0, day 4) |
Active vs. sham tDCS: 1. POMS-30: No effect |
| Plazier et al., 2012 | Crossover Sham controlled |
17 (17) | 21.5 | R DLPFC/L DLPFC L DLPFC/R DLPFC O2/O1 O1/O2 (10/20 EEG) |
1.5 mA 20 min 35 cm2 |
1. SUDS 2. POMS-32 3. PANAS 4. BISBAS (t0, t1) |
Active (either four conditions) vs. sham tDCS: 1. SUDS: No effect 2. POMS-32: No effect 3. PANAS: No effect 4. BISBAS: No effect |
| (B) EFFECTS OF NIBS ON EMOTIONAL PROCESSING | |||||||
| rTMS studies | |||||||
| Balconi and Cobelli, 2015 | Crossover Sham controlled |
69 (31) | 28.1 | L DLPFC Pz (10/20 EEG) |
5 Hz 90 trains of 1 s 5 s ITI 450 pulses 100% MT |
1. Memory task with positive and negative words and pictures with high and low arousal (t0.5) 2. Valence and arousal questionnaire with words and pictures (t1) |
Active rTMS, L DLPFC vs. Pz and sham: 1. Memory task: Increased accuracy and reduced RT for positive high arousal words and pictures 2. Valence and arousal questionnaire: No effect |
| Balconi and Ferrari, 2013 | Crossover Sham controlled |
27 (12) | Range: 21–36 | L DLPFC Cz (10/20 EEG) |
5 Hz 180 trains of 1 s 5 s ITI 900 pulses 100% MT |
1. Memory task with positive and negative words among semantically related or unrelated distractors (t0.5) | Active rTMS, L DLPFC vs. Cz and sham: 1. Memory task: Reduced RT for positive targets and positive (related and unrelated) distractors in subjects with high and low anxiety level |
| Balconi and Ferrari, 2012b | Crossover Sham controlled |
30 (13) | Range: 21–31 | L DLPFC Cz (10/20 EEG) |
5 Hz 90 trains of 1 s 5 s ITI 450 pulses 100% MT |
1. Memory task with positive and negative words (t0.5) | Active rTMS, L DLPFC vs. Cz and sham: 1. Memory task: increased accuracy for positive vs. negative words in subjects with high and low anxiety level. Reduced RT for positive vs. negative words in subjects with high anxiety level |
| Balconi and Ferrari, 2012a | Crossover Sham controlled |
27 | Range: 21–37 | L DLPFC Cz (10/20 EEG) |
5 Hz 90 trains of 1 s 5 s ITI 450 pulses 100% MT |
1. Memory task with positive and negative words among semantically related or unrelated distractors (t0.5) | Active rTMS, L DLPFC vs. Cz and sham: 1. Memory task: Reduced RT for positive vs. negative words and related vs. unrelated positive distractors |
| tDCS studies | |||||||
| Conson et al., 2015 | Crossover Sham controlled |
16 (8) | Range: 22–30 | L DLPFC/R DLPFC R DLPFC/L DLPFC (10/20 EEG) |
1 mA 15 min 35 cm2 |
1. Recognition of facial expressions task | Active tDCS, R DLPFC/L DLPFCvs. L DLPFC/R DLPFCand sham: 1. Recognition of facial expressions task: Reduced RT for fearful faces in male but not female subjects |
| Nitsche et al., 2012 | Crossover Sham controlled |
14 (9) | 33.3 | L DLPFC/ supraorbital region Supraorbital region/L DLPFC (10/20 EEG) |
1 mA 20 min 35 cm2 |
1.14-item mood VAS (t0, t15, t30, t45, t60, t120, t180, t240, t300, following morning) |
Active tDCS, L DLPFC/supraorbital region vs. supraorbital region/L DLPFC and sham: 1. Mood VAS: No effect |
| Crossover Sham controlled |
17 (9) | 24.9 | L DLPFC / supraorbital region Supraorbital region/L DLPFC (10/20 EEG) |
1 mA 10 min 35 cm2 |
1. Recognition of facial expressions task (t0, t0.5, t5, t10, t20, t30, t60) | Active L DLPFC /supraorbital region vs. supraorbital region/L DLPFC: 1. Recognition of facial expression task: Reduced RT for positive (t0.5–t10) and negative faces (t0.5) Active supraorbital region/L DLPFC vs. sham tDCS: 1. Recognition of facial expression task: Reduced RT for negative faces (t10–t20) |
|
| Peña-Gómez et al., 2011 | Crossover Sham controlled |
16 (0) | 22.9 | L DLPFC/M2 (10/20 EEG) |
1 mA 20 min 35 cm2 |
1. Valence rating task with IAPS stimuli (t0.5) 2. Mood 5-item VAS: annoyance, contentment, hope, nervousness, sadness 3. PANAS 4. STAI-state (t0, t1) |
Active vs. sham tDCS: 1. Valence rating task: Negative pictures were rated as less negative Change in valence rating negatively correlated to extraversion score 2. Mood VAS: No effect 3. PANAS: No effect 4. STAI-state: No effect |
| Crossover Sham controlled |
9 (0) | 25.8 | M2/L DLPFC (10/20 EEG) |
1 mA 20 min 35 cm2 |
1. Valence rating task with IAPS stimuli (t0.5) | Active vs. sham tDCS: 1. Valence rating task: No effect |
|
| (C) EFFECTS OF NIBS ON ATTENTIONAL PROCESSING OF EMOTIONAL INFORMATION | |||||||
| rTMS studies | |||||||
| Vanderhasselt et al., 2011 | Crossover Sham controlled |
28 (0) | 22.3 | R DLPFC (MNI BN) |
10 Hz 40 trains of 3.9 s 26.1 s ITI 1560 pulses 110% MT |
1. Exogenous cueing task with neutral and angry faces (t0, t1) 2. POMS-32 (t0, t1, t30) |
Active vs. sham rTMS: 1. Exogenous cueing task: Increased AB for angry faces 2. POMS-32: No effect |
| De Raedt et al., 2010 | Crossover (n = 18) and parallel (n = 19) sham controlled |
37 (0) | 22.6 | L DLPFC R DLPFC (MNI BN) |
10 Hz 40 trains of 3.9 s 26.1 s ITI 1560 pulses 110% MT |
1. Exogenous cueing task with neutral and angry faces during an fMRI scanning (t0, t30) 2. Mood 5-item VAS: sadness, tension, vigor, fatigue, anger (t0, t1, t40) |
Active R DLPFC vs. sham rTMS: 1. Exogenous cueing task and fMRI: Larger disengagement score for angry faces associated with decreased activation in R DLPFC , dorsal ACC, and L SPG 2. Mood VAS: No effect Active L DLPFC vs. sham rTMS: 1. Lower engagement score for angry faces associated with increased activation in the L OFC, R DLPFC , dorsal/pregenual ACC, R SPG 2. Mood VAS: No effect |
| Leyman et al., 2009 | Crossover Sham controlled |
18 (0) | 21.1 | R DLPFC |
10 Hz 40 trains of 3.9 s 26.1 s ITI 1560 pulses 110% MT |
1. NAP task with happy, sad and neutral faces (t0, t1) 2. Mood 5-item VAS: sadness, tension, vigor, fatigue, anger (t0, t1, t40) |
Active R DLPFC vs. sham rTMS: 1. NAP task: Decreased scores for negative faces 2. Mood VAS: No effect |
| Crossover Sham controlled |
22 (0) | 24 | L DLPFC (MNI BN) |
10 Hz 40 trains of 3.9 s 26.1 s ITI 1560 pulses 110% MT |
1. NAP task with happy, sad and neutral faces (t0, t1) 2. Mood 5-item VAS: sadness, tension, vigor, fatigue, anger (t0, t1, t40) |
Active L DLPFC vs. sham rTMS: 1. NAP task: No effect 2. Mood VAS: No effect |
|
| Van Honk et al., 2002b | Crossover Sham controlled |
8 (4) | Range: 20–26 | R DLPFC (10/20 EEG) |
1 Hz 1 single train 1200 pulses 130% MT |
1. Emotional Stroop task with masked and unmasked neutral and fearful faces (t30) | Active vs. sham rTMS: 1. Emotional Stroop task: Decreased attention for unmasked fearful faces |
| van Honk et al., 2002a | Crossover with no sham | 10 (0) | Range: 18–30 | L DLPFC R DLPFC (5 cm anterior to M1 or M2) |
0.6 Hz 1 single train 540 pulses 130% MT |
1. Emotional Stroop task with neutral and angry faces (t1) 2. PEP (t0, t1) |
Active rTMS, R vs. L DLPFC: 1. Emotional Stroop task: Increased attention for angry faces 2. PEP: Reduced PEP Correlation between increased attention and reduced PEP |
| d'Alfonso et al., 2000 | Crossover No sham |
10 (0) | Range: 18–30 | L DLPFC R DLPFC (5 cm anterior to M1 or M2) |
0.6 Hz 1 single train 540 pulses 130% MT |
1. Emotional Stroop task with neutral and angry faces (t10) 2. POMS-32 (t0, t1) |
Active rTMS, L vs. R DLPFC: 1. Emotional Stroop task: Decreased attention for angry faces 2. POMS-32: No effect Active rTMS, R vs. L DLPFC 1. Emotional Stroop task: Increased attention for angry faces 2. POMS-32: No effect |
| tDCS studies | |||||||
| Wolkenstein et al., 2014 | Crossover Sham controlled |
28 (8) | 30.9 | R deltoid/L DLPFC (10/20 EEG) |
1 mA 20 min 35 cm2 |
1. DWM (t0.5) 2. AIT with positive, neutral and negative pictures (t1) 3. PANAS (t0, t1) |
Active vs. sham tDCS: 1. DWM: Reduced accuracy for negative vs. neutral and positive pictures 2. AIT: Longer RT for negative vs. neutral and positive pictures 3. PANAS: No effect |
| Clarke et al., 2014 | Parallel Sham controlled “Attend threat” ABM + active tDCS “Avoid threat” ABM + active tDCS |
17 (7) 20 (6) |
19.6 19.6 |
L DLPFC/L superior trapezius (10/20 EEG) |
1 mA mean 17 min 24 cm2 |
1. AB assessment task with neutral and threatening words (t0, t1) | “Attend threat” ABM combined with active tDCS vs. “attend threat” ABM combined with sham tDCS: 1. AB assessment task: Increased AB to threat “Avoid threat” ABM combined with active tDCS vs. “Avoid threat” combined with sham tDCS: 1. AB assessment task: Decreased AB to threat |
| “Attend threat” ABM + sham tDCS | 22 (7) | 20.6 | |||||
| “Avoid threat” ABM + sham tDCS | 18 (8) | 19.9 | |||||
| Feeser et al., 2014 | Parallel sham controlled tDCS applied during emotional regulation (4 conditions: maintain neutral emotions, downregulate, upregulate, or maintain negative emotions) | 42 (20) | 28.5 | R DLFPC/L supraorbital region (10/20 EEG) |
1.5 mA 20 min Anodal: 35 cm2 Cathodal: 100 cm2 |
1. Arousal ratings on IAPS pictures (t0.5) 2. Skin conductance response (t0.5) 3. Gaze fixation (t0.5) 4. Multidimensional State Questionnaire (t0, t1) |
Active vs. Sham tDCS: 1. Arousal ratings: Lower in the downregulation conditions. Higher and in the negative maintain in the upregulation condition 2. Skin conductance: Lower response in the downregulation condition. Higher response in the upregulation condition 3. Gaze fixation: No effect 4. Multidimensional State Questionnaire: No effect |
*
Site of stimulation is provided as follows, for rTMS: coil position, for tDCS: anode/cathode position. The method used to define the target is provided as follows, (10/20 EEG), Electrode placements according to 10/20 EEG system; (MRI BN), Magnetic Resonance Imaging based neuronavigation.
**
NIBS parameters are provided as follows, for rTMS: frequency, trains number and duration, ITI, number of pulses, intensity, for tDCS: intensity, duration, electrode size. AB, Attentional bias; ABM, Attentional bias modification task; ACC, Anterior cingulate cortex; AGN, Affective go-no-go; AIT, Arithmetic inhibition task; BDI, Beck depression inventory; BISBAS, Behavioral inhibition system and behavioral approach system; Cz, Central midline; DLPFC, Dorsolateral prefrontal cortex; DWM, Delayed response working memory task; IAPS, International affective picture system; ITI, Intertrain interval; L, Left; M1, Left primary motor cortex; M2, Right primary motor cortex; MT, Motor threshold; N, number of subjects; NAP, Negative affective priming; NIBS, Non-invasive brain stimulation; NIMH, National institute of mental health; OFC, Orbitofrontal cortex; O1, Left occipital cortex; O2, Right occipital cortex; PANAS, Positive affect and negative affect schedule; PASAT, Paced auditory serial addition task; PEP, Preejection period; POMS, Profile of mood states; Pz, Parietal midline; R, Right; RT, Reaction Time; rTMS, repetitive transcranial magnetic stimulation; SPG, Superior parietal gyrus; STAI, State-trait anxiety index; STAS, State-trait anger scale; SUDS, Subjective unit of distress schedule; t0, Baseline; t0.5, During stimulation, t1, Immediately after stimulation, tX, X minutes after stimulation; tDCS, transcranial Direct Current Stimulation; VAS, Visual analog scale.