An Exploratory TMS Study on Prefrontal Lateralization in Valence Categorization of Facial Expressions
Abstract
Abstract. Converging neuroimaging and patient data suggest that the dorsolateral prefrontal cortex (DLPFC) is involved in emotional processing. However, it is still not clear whether the DLPFC in the left and right hemisphere is differentially involved in emotion recognition depending on the emotion considered. Here we used transcranial magnetic stimulation (TMS) to shed light on the possible causal role of the left and right DLPFC in encoding valence of positive and negative emotional facial expressions. Participants were required to indicate whether a series of faces displayed a positive or negative expression, while TMS was delivered over the right DLPFC, the left DLPFC, and a control site (vertex). Interfering with activity in both the left and right DLPFC delayed valence categorization (compared to control stimulation) to a similar extent irrespective of emotion type. Overall, we failed to demonstrate any valence-related lateralization in the DLPFC by using TMS. Possible methodological limitations are discussed.
References
2012). rTMS stimulation on left DLPFC affects emotional cue retrieval as a function of anxiety level and gender. Depression and Anxiety, 29, 976–982. doi: 10.1002/da.21968
(2013). Random effects structure for confirmatory hypothesis testing: Keep it maximal. Journal of Memory and Language, 68, 255–278. doi: 10.1016/j.jml.2012.11.001
(2005). Left prefrontal repetitive transcranial magnetic stimulation impairs performance in affective go/no-go task. Neuroreport, 16, 615–619.
(2014). The causal role of the lateral occipital complex in visual mirror symmetry detection and grouping: An fMRI-guided TMS study. Cortex, 51, 46–55. doi: 10.1016/j.cortex.2013.11.004
(2007). Left frontal eye field remembers “where” but not “what”. Neuropsychologia, 45, 2340–2345. doi: 10.1016/j.neuropsychologia.2007.02.009
(2014a). Happiness takes you right: The effect of emotional stimuli on line bisection. Cognition & Emotion, 28, 325–344. doi: 10.1080/02699931.2013.824871
(2014b). The role of prefrontal and parietal cortices in esthetic appreciation of representational and abstract art: A TMS study. NeuroImage, 99, 443–450. doi: 10.1016/j.neuroimage.2014.05.037
(2011). The role of the human extrastriate visual cortex in mirror symmetry discrimination: A TMS-adaptation study. Brain and Cognition, 77, 120–127. doi: 10.1016/j.bandc.2011.04.007
(2011). The role of the prefrontal cortex in controlling gender-stereotypical associations: A TMS investigation. NeuroImage, 56, 1839–1846. doi: 10.1016/j.neuroimage.2011.02.037
(2009). Control of prepotent responses by the superior medial frontal cortex. NeuroImage, 44, 537–545. doi: 10.1016/j.neuroimage.2008.09.005
(2013). Temporal and spatial neural dynamics in the perception of basic emotions from complex scenes. Social Cognitive and Affective Neuroscience, 9, 1690–1703. doi: 10.1093/scan/nst164
(2000). Laterality effects in selective attention to threat after repetitive transcranial magnetic stimulation at the prefrontal cortex in female subjects. Neuroscience Letters, 280, 195–198. doi: 10.1016/S0304-3940(00)00781-3
(1992). Anterior cerebral asymmetry and the nature of emotion. Brain and Cognition, 20, 125–151. doi: 10.1016/0278-2626(92)90065-T
(1995).
(Cerebral asymmetry, emotion, and affective style . In R. J. DavidsonK. HugdahlEds., Brain asymmetry (pp. 361–388). Cambridge, MA: MIT Press.1990). Approach-withdrawal and cerebral asymmetry: Emotional expression and brain physiology I. Journal of Personality and Social Psychology, 58, 330–341. doi: 10.1037/0022-3514.58.2.330
(1999). The functional neuroanatomy of emotion and affective style. Trends in Cognitive Science, 3, 11–21. doi: 10.1016/S1364-6613(98)01265-0
(2011). Emotion in the brain: Of low roads, high roads and roads less travelled. Nature Reviews Neuroscience, 12, 425. doi: 10.1038/nrn2920-c1
(2010). Neurocognitive effects of HF-rTMS over the dorsolateral prefrontal cortex on the attentional processing of emotional information in healthy women: An event-related fMRI study. Biological Psychology, 85, 487–495. doi: 10.1016/j.biopsycho.2010.09.015
(2005). Brain lateralization of emotional processing: historical roots and a future incorporating “dominance”. Behavioral and Cognitive Neuroscience Reviews, 4, 3–20. doi: 10.1177/1534582305276837
(2004). Dissociable effects of arousal and valence on prefrontal activity indexing emotional evaluation and subsequent memory: An event-related fMRI study. NeuroImage, 23, 64–74. doi: 10.1016/j.neuroimage.2004.05.015
(2013). Lateralization of affective processing in the insula. NeuroImage, 78, 159–175. doi: 10.1016/j.neuroimage.2013.04.014
(2007). Event-related brain potential correlates of emotional face processing. Neuropsychologia, 45, 15–31. doi: 10.1016/j.neuropsychologia.2006.04.022
(2007). Specificity of regional brain activity in anxiety types during emotion processing. Psychophysiology, 44, 352–363. doi: 10.1111/j.1469-8986.2007.00518.x
(1998). Identification of emotion in a dichotic listening task: Event-related brain potential and behavioral findings. Brain and Cognition, 37, 286–307. doi: 10.1006/brcg.1998.0984
(2007). Activation of prefrontal cortex by transcranial direct current stimulation reduces appetite for risk during ambiguous decision making. The Journal of Neuroscience, 27, 6212–6218. doi: 10.1523/JNEUROSCI.0314-07.2007
(2016). The dorsomedial prefrontal cortex plays a causal role in integrating social impressions from faces and verbal descriptions. Cerebral Cortex, 26, 156–165. doi: 10.1093/cercor/bhu186
(2009). Functional atlas of emotional faces processing: A voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry & Neuroscience, 34, 418–432.
(2001). Explicit and incidental facial expression processing: An fMRI study. NeuroImage, 14, 465–473. doi: 10.1006/nimg.2001.0811
(2006). Segregated neural representation of distinct emotion dimensions in the prefrontal cortex – An fMRI study. NeuroImage, 30, 325–340. doi: 10.1016/j.neuroimage.2005.09.006
(2012). Neural mechanisms underlying the integration of emotion and working memory. NeuroImage, 61, 1188–1194. doi: 10.1016/j.neuroimage.2012.04.004
(2010). The role of asymmetric frontal cortical activity in emotion-related phenomena: A review and update. Biological Psychology, 84, 451–462. doi: 10.1016/j.biopsycho.2009.08.010
(2001). Transcranial magnetic stimulation of medial-frontal cortex impairs the processing of angry facial expressions. Nature Neuroscience, 4, 17–18. doi: 10.1038/82854
(2003). An fMRI study of simple ethical decision-making. Neuroreport, 14, 1215–1219.
(2005). Emotion-modulated performance and activity in left dorsolateral prefrontal cortex. Emotion, 5, 200–207. doi: 10.1037/1528-3542.5.2.200
(2005). Decisions under uncertainty: Probabilistic context influences activation of prefrontal and parietal cortices. The Journal of Neuroscience, 25, 3304–3311. doi: 10.1523/JNEUROSCI.5070-04.2005
(2014). What are the odds? A practical guide to computing and reporting Bayes factors. The Journal of Problem Solving, 7, 2. doi: 10.7771/1932-6246.1167
(2010). Presentation and validation of the Radboud Faces Database. Cognition and Emotion, 24, 1377–1388. doi: 10.1080/02699930903485076
(2015). The brain basis of positive and negative affect: Evidence from a meta-analysis of the human neuroimaging literature. Cerebral Cortex, 26, 1910–1922. doi: 10.1093/cercor/bhv001
(2012). The brain basis of emotion: A meta-analytic review. Behavioral and Brain Sciences, 35, 121–143. doi: 10.1017/S0140525X11000446
(2004). Detection theory: A user’s guide. New York, NY: Psychology press.
(2009). Neural correlates of regulation of positive and negative emotions: An fMRI study. Neuroscience Letters, 457, 101–106. doi: 10.1016/j.neulet.2009.03.094
(2011). Transcranial magnetic stimulation of medial prefrontal cortex modulates face expressions processing in a priming task. Neuropsychologia, 49, 992–998. doi: 10.1016/j.neuropsychologia.2011.01.038
(2013). Issues in localization of brain function: The case of lateralized frontal cortex in cognition, emotion and psychopathology. Frontiers in Integrative Neuroscience, 7, 2. doi: 10.3389/fnint.2013.00002
(2015). Package ‘BayesFactor’. Retrieved from https://cran.r-project.org/web/packages/BayesFactor/BayesFactor.pdf
(1996). Lesion location and poststroke depression. The Journal of Neuropsychiatry and Clinical Neurosciences, 8, 399–403. doi: 10.1176/jnp.8.4.399
(2013). Response inhibition is modulated by functional cerebral asymmetries for facial expression perception. Frontiers in Psychology, 4, 879. doi: 10.3389/fpsyg.2013.00879
(2015). Non-invasive human brain stimulation in cognitive neuroscience: A primer. Neuron, 87, 932–945. doi: 10.1016/j.neuron.2015.07.032
(2005). Neural substrates for voluntary suppression of negative affect: A functional magnetic resonance imaging study. Biological Psychiatry, 57, 210–219. doi: 10.1016/j.biopsych.2004.10.030
(2014). Facial expression recognition takes longer in the posterior superior temporal sulcus than in the occipital face area. The Journal of Neuroscience, 34, 9173–9177. doi: 10.1523/JNEUROSCI.5038-13.2014
(2014). Combined TMS and fMRI reveal dissociable cortical pathways for dynamic and static face perception. Current Biology, 24, 2066–2070. doi: 10.1016/j.cub.2014.07.060
(2008). Transcranial magnetic stimulation disrupts the perception and embodiment of facial expressions. The Journal of Neuroscience, 28, 8929–8933. doi: 10.1523/JNEUROSCI.1450-08.2008
(2007). TMS evidence for the involvement of the right occipital face area in early face processing. Current Biology, 17, 1568–1573. doi: 10.1016/j.cub.2007.07.063
(1995). Bayesian model selection in social research. Sociological Methodology, 25, 111–163. doi: 10.2307/271063
(2013). Processing of featural and configural aspects of faces is lateralized in dorsolateral prefrontal cortex: A TMS study. NeuroImage, 74, 45–51. doi: 10.1016/j.neuroimage.2013.02.015
(2003). Studies in cognition: The problems solved and created by transcranial magnetic stimulation. Journal of Cognitive Neuroscience, 15, 948–960. doi: 10.1162/089892903770007344
(2011). Screening questionnaire before TMS: An update. Clinical Neurophysiology, 122, 1686. doi: 10.1016/j.clinph.2010.12.037
(2010). Optimal transcranial magnetic stimulation coil placement for targeting the dorsolateral prefrontal cortex using novel magnetic resonance image-guided neuronavigation. Human Brain Mapping, 31, 1643–1652. doi: 10.1002/hbm.20964
(2011). Emotional perception: Meta-analyses of face and natural scene processing. NeuroImage, 54, 2524–2533. doi: 10.1016/j.neuroimage.2010.10.011
(2016). The role of the dorsolateral prefrontal cortex in early threat processing: A TMS study. Social Cognitive and Affective Neuroscience, 11, 1992–1998. doi: 10.1093/scan/nsw105
(2012). Valence-specific laterality effects in vocal emotion: Interactions with stimulus type, blocking and sex. Brain and Cognition, 79, 129–137. doi: 10.1016/j.bandc.2012.03.001
(2001). Effects of slow rTMS at the right dorsolateral prefrontal cortex on EEG asymmetry and mood. Neuroreport, 12, 445–447.
(1989). Mood changes after right-hemisphere lesions. The British Journal of Psychiatry, 155, 79–85. doi: 10.1192/bjp.155.1.79
(2002). 1 hz rTMS over the right prefrontal cortex reduces vigilant attention to unmasked but not to masked fearful faces. Biological Psychiatry, 52, 312–317. doi: 10.1016/S0006-3223(02)01346-X
(2006). The influence of rTMS over the left dorsolateral prefrontal cortex on Stroop task performance. Experimental Brain Research, 169, 279–282. doi: 10.1007/s00221-005-0344-z
(2010). Nonlinear relationship between emotional valence and brain activity: Evidence of separate negative and positive valence dimensions. Human Brain Mapping, 31, 1030–1040. doi: 10.1002/hbm.20915
(2012). Neural processing of emotional valence of facial expressions. Open Journal of Neuroscience, 2, 3.
(2007). A practical solution to the pervasive problems of p values. Psychonomic Bulletin and Review, 14, 779–804. doi: 10.3758/BF03194105
(2003). Valence, gender, and lateralization of functional brain anatomy in emotion: A meta-analysis of findings from neuroimaging. NeuroImage, 19, 513–531. doi: 10.1016/S1053-8119(03)00078-8
(2010). Bring it on: Angry facial expressions potentiate approach-motivated motor behavior. Journal of Personality and Social Psychology, 98, 201. doi: 10.1037/a0017992
(2014). Inhibitory repetitive transcranial magnetic stimulation (rTMS) of the dorsolateral prefrontal cortex modulates early affective processing. NeuroImage, 101, 193–203. doi: 10.1016/j.neuroimage.2014.07.003
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