Inhibitory repetitive transcranial magnetic stimulation (rTMS) of the dorsolateral prefrontal cortex modulates early affective processing

The dorsolateral prefrontal cortex (dlPFC) has often been suggested as a key modulator of emotional stimulus appraisal and regulation. Therefore, in clinical trials, it is one of the most frequently targeted regions for non-invasive brain stimulation such as repetitive transcranial magnetic stimulation (rTMS). In spite of various encouraging reports that demonstrate beneficial effects of rTMS in anxiety disorders, psychophysiological studies exploring the underlying neural mechanisms are sparse. Here we investigated how inhibitory rTMS influences early affective processing when applied over the right dlPFC. Before and after rTMS or sham stimulation, subjects viewed faces with fearful or neutral expressions while whole-head magnetoencephalography (MEG) was recorded. Due to the disrupted functioning of the right dlPFC, visual processing in bilateral parietal, temporal, and occipital areas was amplified starting at around 90 ms after stimulus onset. Moreover, increased fear-specific activation was found in the right TPJ area in a time-interval between 110 and 170 ms. These neurophysiological effects were reflected in slowed reaction times for fearful, but not for neutral faces in a facial expression identification task while there was no such effect on a gender discrimination control task. Our study confirms the specific and important role of the dlPFC in regulation of early emotional attention and encourages future clinical research to use minimal invasive methods such as transcranial magnetic (TMS) or direct current stimulation (tDCS).

[1]  R. Davidson,et al.  The functional neuroanatomy of emotion and affective style , 1999, Trends in Cognitive Sciences.

[2]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[3]  M. Hallett,et al.  Depression of motor cortex excitability by low‐frequency transcranial magnetic stimulation , 1997, Neurology.

[4]  John T. Cacioppo,et al.  If Attitudes Affect How Stimuli Are Processed, Should They Not Affect the Event-Related Brain Potential? , 1993 .

[5]  L. Leyman,et al.  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 , 2010, Biological Psychology.

[6]  N. Costes,et al.  Emotional Responses to Pleasant and Unpleasant Olfactory, Visual, and Auditory Stimuli: a Positron Emission Tomography Study , 2000, The Journal of Neuroscience.

[7]  I. L. Freeston,et al.  CLINICAL EVALUATION OF CONDUCTION TIME MEASUREMENTS IN CENTRAL MOTOR PATHWAYS USING MAGNETIC STIMULATION OF HUMAN BRAIN , 1986, The Lancet.

[8]  M. Bradley,et al.  Activation of the visual cortex in motivated attention. , 2003, Behavioral neuroscience.

[9]  Thomas Elbert,et al.  Emotion Processing in the Visual Brain: A MEG Analysis , 2008, Brain Topography.

[10]  Margot J. Taylor,et al.  Early processing of the six basic facial emotional expressions. , 2003, Brain research. Cognitive brain research.

[11]  Frank Padberg,et al.  Transcranial magnetic stimulation for panic. , 2002, The American journal of psychiatry.

[12]  Karl J. Friston,et al.  Academic Software Applications for Electromagnetic Brain Mapping Using MEG and EEG , 2011, Comput. Intell. Neurosci..

[13]  D. Lehmann,et al.  Rapid emotional face processing in the human right and left brain hemispheres: an ERP study. , 1999, Neuroreport.

[14]  E M Wassermann,et al.  Repetitive transcranial magnetic stimulation for posttraumatic stress disorder. , 1998, Archives of general psychiatry.

[15]  Markus Junghöfer,et al.  ElectroMagnetoEncephalography Software: Overview and Integration with Other EEG/MEG Toolboxes , 2011, Comput. Intell. Neurosci..

[16]  Ann-Kathrin Bröckelmann,et al.  Rapid and highly resolving associative affective learning: Convergent electro- and magnetoencephalographic evidence from vision and audition , 2013, Biological Psychology.

[17]  Margot J. Taylor,et al.  Attention inhibition of early cortical activation to fearful faces , 2010, Brain Research.

[18]  A. Fallgatter,et al.  Anxiolytic effects of transcranial magnetic stimulation—an alternative treatment option in anxiety disorders? , 2009, Journal of Neural Transmission.

[19]  J. C. Rothwell,et al.  Transcranial magnetic stimulation of medial–frontal cortex impairs the processing of angry facial expressions , 2001, Nature Neuroscience.

[20]  Christo Pantev,et al.  Rapid and Highly Resolving: Affective Evaluation of Olfactorily Conditioned Faces , 2012, Journal of Cognitive Neuroscience.

[21]  H. Sackeim,et al.  Neuropsychiatric applications of transcranial magnetic stimulation: a meta analysis. , 2002, The international journal of neuropsychopharmacology.

[22]  D. Lundqvist,et al.  Karolinska Directed Emotional Faces , 2015 .

[23]  Frank Padberg,et al.  Transcranial magnetic stimulation in therapy studies: examination of the reliability of “standard” coil positioning by neuronavigation , 2001, Biological Psychiatry.

[24]  J. Couturier,et al.  Efficacy of rapid-rate repetitive transcranial magnetic stimulation in the treatment of depression: a systematic review and meta-analysis. , 2005, Journal of psychiatry & neuroscience : JPN.

[25]  C. Mervis,et al.  Neural correlates of genetically abnormal social cognition in Williams syndrome , 2005, Nature Neuroscience.

[26]  N. Grisaru,et al.  Effect of transcranial magnetic stimulation in posttraumatic stress disorder: a preliminary study , 1998, Biological Psychiatry.

[27]  E. Halgren,et al.  Top-down facilitation of visual recognition. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[28]  H Scheich,et al.  Auditory perception of laughing and crying activates human amygdala regardless of attentional state. , 2001, Brain research. Cognitive brain research.

[29]  S. Hillyard,et al.  Cortical sources of the early components of the visual evoked potential , 2002, Human brain mapping.

[30]  M García-Toro,et al.  [Panic disorder and transcranial magnetic stimulation]. , 2002, Actas espanolas de psiquiatria.

[31]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[32]  Peter J. Lang,et al.  Parallel amygdala and inferotemporal activation reflect emotional intensity and fear relevance , 2005, NeuroImage.

[33]  R. Zajonc Feeling and thinking : Preferences need no inferences , 1980 .

[34]  Amanda Holmes,et al.  Effects of anxiety on the processing of fearful and happy faces: An event-related potential study , 2008, Biological Psychology.

[35]  Leonor J. Romero Lauro,et al.  Top-down interference and cortical responsiveness in face processing: A TMS-EEG study , 2013, NeuroImage.

[36]  Olaf Hauk,et al.  Keep it simple: a case for using classical minimum norm estimation in the analysis of EEG and MEG data , 2004, NeuroImage.

[37]  Jack van Honk,et al.  1 hz rTMS over the right prefrontal cortex reduces vigilant attention to unmasked but not to masked fearful faces , 2002, Biological Psychiatry.

[38]  D. Grandjean,et al.  Enhanced extrastriate visual response to bandpass spatial frequency filtered fearful faces: Time course and topographic evoked‐potentials mapping , 2005, Human brain mapping.

[39]  R. Ilmoniemi,et al.  Interpreting magnetic fields of the brain: minimum norm estimates , 2006, Medical and Biological Engineering and Computing.

[40]  Christopher K. Kovach,et al.  Rapid Interactions between the Ventral Visual Stream and Emotion-Related Structures Rely on a Two-Pathway Architecture , 2008, The Journal of Neuroscience.

[41]  L. Leyman,et al.  Influence of high-frequency repetitive transcranial magnetic stimulation over the dorsolateral prefrontal cortex on the inhibition of emotional information in healthy volunteers , 2008, Psychological Medicine.

[42]  Katharina Domschke,et al.  Imaging genetics of anxiety disorders , 2010, NeuroImage.

[43]  Valerie Treyer,et al.  Time-course of “off-line” prefrontal rTMS effects — a PET study , 2008, NeuroImage.

[44]  Alvaro Pascual-Leone,et al.  Repetitive transcranial magnetic stimulation for the treatment of depression. , 2005, Journal of psychiatry & neuroscience : JPN.

[45]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.

[46]  Harumasa Takano,et al.  rCBF changes elicited by rTMS over DLPFC in humans. , 2004, Supplements to Clinical neurophysiology.

[47]  W. Miltner,et al.  Behavioral and Brain Functions , 2008 .

[48]  E H de Haan,et al.  Effects of slow rTMS at the right dorsolateral prefrontal cortex on EEG asymmetry and mood , 2001, Neuroreport.

[49]  W. Miltner,et al.  Psychophysiological correlates of face processing in social phobia , 2006, Brain Research.

[50]  Alan Cowey,et al.  Transcranial magnetic stimulation and cognitive neuroscience , 2000, Nature Reviews Neuroscience.

[51]  H. Hoek,et al.  Should we expand the toolbox of psychiatric treatment methods to include Repetitive Transcranial Magnetic Stimulation (rTMS)? A meta-analysis of the efficacy of rTMS in psychiatric disorders. , 2010, The Journal of clinical psychiatry.

[52]  T. Allison,et al.  Electrophysiological Studies of Face Perception in Humans , 1996, Journal of Cognitive Neuroscience.

[53]  H. Sackeim,et al.  Sham TMS: intracerebral measurement of the induced electrical field and the induction of motor-evoked potentials , 2001, Biological Psychiatry.

[54]  M. Bradley,et al.  Motivated attention: Affect, activation, and action. , 1997 .

[55]  David J. Freedman,et al.  A Comparison of Primate Prefrontal and Inferior Temporal Cortices during Visual Categorization , 2003, The Journal of Neuroscience.

[56]  G. A. Miller,et al.  Lateralization in Emotion and Emotional Disorders , 1998 .

[57]  M. Bradley,et al.  Fleeting images: a new look at early emotion discrimination. , 2001, Psychophysiology.

[58]  Paul Pauli,et al.  Early cortical processing of natural and artificial emotional faces differs between lower and higher socially anxious persons , 2009, Journal of Neural Transmission.

[59]  M. Junghöfer,et al.  Effects of personal familiarity on early neuromagnetic correlates of face perception , 2006, The European journal of neuroscience.

[60]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[61]  Michael Andres,et al.  Dissociable roles of the human somatosensory and superior temporal cortices for processing social face signals , 2004, The European journal of neuroscience.

[62]  E. D. Haan,et al.  Laterality effects in selective attention to threat after repetitive transcranial magnetic stimulation at the prefrontal cortex in female subjects , 2000, Neuroscience Letters.

[63]  J. Duncan,et al.  Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli , 2004, Nature Neuroscience.

[64]  B. Rockstroh,et al.  Statistical control of artifacts in dense array EEG/MEG studies. , 2000, Psychophysiology.

[65]  Dominique Lamy,et al.  Attentional bias in anxiety: A behavioral and ERP study , 2005, Brain and Cognition.

[66]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[67]  Peter Herscovitch,et al.  Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with h2 15o positron emission tomography: II. effects of prefrontal cortex rTMS , 2003, Biological Psychiatry.

[68]  Chris Baeken,et al.  A single session of rTMS over the left dorsolateral prefrontal cortex influences attentional control in depressed patients , 2009, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[69]  Paul Pauli,et al.  Don't look at me in anger! Enhanced processing of angry faces in anticipation of public speaking. , 2010, Psychophysiology.

[70]  J. Gross,et al.  The cognitive control of emotion , 2005, Trends in Cognitive Sciences.

[71]  Hans-Jochen Heinze,et al.  Magnetoencephalography (MEG) determined temporal modulation of visual and auditory sensory processing in the context of classical conditioning to faces , 2006, NeuroImage.

[72]  Sarah H Lisanby,et al.  Repetitive Transcranial Magnetic Stimulation (rTMS) in the treatment of panic disorder (PD) with comorbid major depression. , 2007, Journal of affective disorders.

[73]  Chris Baeken,et al.  The effects of high frequency rTMS on negative attentional bias are influenced by baseline state anxiety , 2011, Neuropsychologia.

[74]  J. Lorberbaum,et al.  Unilateral left prefrontal transcranial magnetic stimulation (TMS) produces intensity-dependent bilateral effects as measured by interleaved BOLD fMRI , 2001, Biological Psychiatry.

[75]  Maimu A. Rehbein,et al.  The neural basis of cognitive change: Reappraisal of emotional faces modulates neural source activity in a frontoparietal attention network , 2013, NeuroImage.

[76]  Jaime Kulisevsky,et al.  Repetitive transcranial magnetic stimulation for the treatment of depression. Systematic review and meta-analysis. , 2003, The British journal of psychiatry : the journal of mental science.

[77]  Jennifer S. Beer,et al.  Prefrontal involvement in the regulation of emotion: convergence of rat and human studies , 2006, Current Opinion in Neurobiology.

[78]  M. Junghöfer,et al.  The facilitated processing of threatening faces: an ERP analysis. , 2004, Emotion.

[79]  Markus Junghöfer,et al.  Neural systems of visual attention responding to emotional gestures , 2009, NeuroImage.

[80]  D. Kupfer,et al.  Abnormal Amygdala-Prefrontal Effective Connectivity to Happy Faces Differentiates Bipolar from Major Depression , 2009, Biological Psychiatry.

[81]  Peter Herscovitch,et al.  Left prefrontal-repetitive transcranial magnetic stimulation (rTMS) and regional cerebral glucose metabolism in normal volunteers , 2002, Psychiatry Research: Neuroimaging.

[82]  S. Rauch,et al.  A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. , 2005, Archives of general psychiatry.

[83]  M. Crommelinck,et al.  The perception of fearful and happy facial expression is modulated by anxiety: an event-related potential study , 2005, Neuroscience Letters.

[84]  Á. Pascual-Leone,et al.  Has repetitive transcranial magnetic stimulation (rTMS) treatment for depression improved? A systematic review and meta‐analysis comparing the recent vs. the earlier rTMS studies , 2007, Acta psychiatrica Scandinavica.

[85]  Alan C. Evans,et al.  Structural asymmetries in the human brain: a voxel-based statistical analysis of 142 MRI scans. , 2001, Cerebral cortex.

[86]  Wioleta Walentowska,et al.  Trait anxiety and involuntary processing of facial emotions. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[87]  Florin Dolcos,et al.  Dissociable effects of arousal and valence on prefrontal activity indexing emotional evaluation and subsequent memory: an event-related fMRI study , 2004, NeuroImage.

[88]  Martin Bares,et al.  The effect of repetitive transcranial magnetic stimulation (rTMS) add on serotonin reuptake inhibitors in patients with panic disorder: a randomized, double blind sham controlled study. , 2007, Neuro endocrinology letters.

[89]  M. Daube-Witherspoon,et al.  Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with H2 15O positron emission tomography: i. effects of primary motor cortex rTMS , 2003, Biological Psychiatry.

[90]  J. Kissler,et al.  Buzzwords , 2007, Psychological science.