Dorsolateral Prefrontal Cortex Stimulation Modulates Electrocortical Measures of Visual Attention: Evidence from Direct Bilateral Epidural Cortical Stimulation in Treatment-resistant Mood Disorder Ine Regional Specificity of Pfc Stimulation on the Parietally- Maximal Late Positive Potential (lpp), a

Electrocortical activity is increasingly being used to study emotion regulation and the impact of cognitive control on neural response to visual stimuli. In the current study, we used direct epidural cortical stimulation (EpCS) to examine regional specificity of PFC stimulation on the parietally-maximal late positive potential (LPP), an event-related potential (ERP) biomarker of visual attention to salient stimuli. Five patients with treatment-resistant mood disorders were stereotactically implanted with stimulating paddles over frontopolar (FP) and dorsolateral (DL) prefrontal cortex bilaterally. On their first day of activation, patients underwent sham-controlled EpCS coupled with 64-channel electroencephalograph (EEG) recordings and passive viewing of aversive and neutral images. In addition to sham, patients had either FP or DL prefrontal cortex stimulated at 2 or 4 V while they viewed neutral and aversive pictures. As expected during the sham condition, LPP was larger for aversive compared to neutral stimuli (F(1,4)=232.07, P<.001). Stimulation of DL compared to FP prefrontal cortex resulted in a reduction of the LPP (F(1,4)=8.15, P=.048). These data provide additional and unique support to the role of the DL prefrontal cortex in regulating measures of neural activity that have been linked to emotional arousal and attention. Future studies with EpCS can help directly map out various prefrontal functions in treatment-resistant mood disorder.

[1]  Dean Sabatinelli,et al.  Affective picture perception: gender differences in visual cortex? , 2004, Neuroreport.

[2]  M. Bradley,et al.  Large-scale neural correlates of affective picture processing. , 2002, Psychophysiology.

[3]  P. Lang,et al.  International Affective Picture System (IAPS): Instruction Manual and Affective Ratings (Tech. Rep. No. A-4) , 1999 .

[4]  Arthur W. Toga,et al.  Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template , 2008, NeuroImage.

[5]  A. Priori,et al.  Chronic epidural motor cortical stimulation for movement disorders , 2007, The Lancet Neurology.

[6]  Markus Junghöfer,et al.  Selective Visual Attention to Emotion , 2007, The Journal of Neuroscience.

[7]  M. Petrides.  Lateral prefrontal cortex: architectonic and functional organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[8]  Atsushi Sato,et al.  Association of neural and physiological responses during voluntary emotion suppression , 2006, NeuroImage.

[9]  Andreas Keil,et al.  Additive effects of emotional content and spatial selective attention on electrocortical facilitation. , 2005, Cerebral cortex.

[10]  G. Hajcak,et al.  Event-Related Potentials, Emotion, and Emotion Regulation: An Integrative Review , 2010, Developmental neuropsychology.

[11]  Abraham Z. Snyder,et al.  A default mode of brain function: A brief history of an evolving idea , 2007, NeuroImage.

[12]  Ross A. Thompson,et al.  Emotion regulation: Conceptual foundations , 2007 .

[13]  Heather L. Urry,et al.  Failure to Regulate: Counterproductive Recruitment of Top-Down Prefrontal-Subcortical Circuitry in Major Depression , 2007, The Journal of Neuroscience.

[14]  M. Bradley,et al.  Brain potentials in perception: picture complexity and emotional arousal. , 2007, Psychophysiology.

[15]  Dan Foti,et al.  Motivated and controlled attention to emotion: Time-course of the late positive potential , 2009, Clinical Neurophysiology.

[16]  Peter J. Lang,et al.  Attention and Orienting : Sensory and Motivational Processes , 1997 .

[17]  廣瀬雄一,et al.  Neuroscience , 2019, Workplace Attachments.

[18]  J. Cacioppo,et al.  Bioelectrical echoes from evaluative categorizations: I. A late positive brain potential that varies as a function of trait negativity and extremity. , 1994, Journal of personality and social psychology.

[19]  Kamryn T. Eddy,et al.  Amygdala-frontal connectivity during emotion regulation. , 2007, Social cognitive and affective neuroscience.

[20]  Peter Lang,et al.  Brain processes in emotional perception: Motivated attention , 2004 .

[21]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[22]  Daniel S. Margulies,et al.  Functional connectivity of the human amygdala using resting state fMRI , 2009, NeuroImage.

[23]  James J. Gross,et al.  Handbook of emotion regulation , 2007 .

[24]  Harald T. Schupp,et al.  Emotional Facilitation of Sensory Processing in the Visual Cortex , 2003, Psychological science.

[25]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[26]  R. Veit,et al.  Regulation of emotional responses elicited by threat‐related stimuli , 2007, Human brain mapping.

[27]  A. Owen,et al.  Anterior prefrontal cortex: insights into function from anatomy and neuroimaging , 2004, Nature Reviews Neuroscience.

[28]  R. Lane,et al.  Neuroanatomical correlates of happiness, sadness, and disgust. , 1997, The American journal of psychiatry.

[29]  Dan Foti,et al.  Deconstructing Reappraisal: Descriptions Preceding Arousing Pictures Modulate the Subsequent Neural Response , 2008, Journal of Cognitive Neuroscience.

[30]  M. Bradley,et al.  Brain potentials in affective picture processing: covariation with autonomic arousal and affective report , 2000, Biological Psychology.

[31]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[32]  Greg Hajcak,et al.  Attending to affect: appraisal strategies modulate the electrocortical response to arousing pictures. , 2006, Emotion.

[33]  M. Junghöfer,et al.  The selective processing of briefly presented affective pictures: an ERP analysis. , 2004, Psychophysiology.

[34]  S. Nolen-Hoeksema,et al.  The role of rumination in depressive disorders and mixed anxiety/depressive symptoms. , 2000, Journal of abnormal psychology.

[35]  Timothy J Ziemlewicz,et al.  Neural correlates of telling lies: a functional magnetic resonance imaging study at 4 Tesla. , 2005, Academic radiology.

[36]  G. Hajcak,et al.  Differentiating neural responses to emotional pictures: evidence from temporal-spatial PCA. , 2009, Psychophysiology.

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

[38]  M. Beauregard,et al.  Neural Correlates of Conscious Self-Regulation of Emotion , 2001, The Journal of Neuroscience.

[39]  M. Bradley,et al.  Affective picture processing: the late positive potential is modulated by motivational relevance. , 2000, Psychophysiology.

[40]  Tor D Wager,et al.  Neuroimaging studies of shifting attention: a meta-analysis , 2004, NeuroImage.

[41]  D. Pandya,et al.  Efferent Association Pathways from the Rostral Prefrontal Cortex in the Macaque Monkey , 2007, The Journal of Neuroscience.

[42]  J. Gabrieli,et al.  The frontopolar cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex , 2000, Psychobiology.

[43]  B. Mensour,et al.  Neural circuitry underlying voluntary suppression of sadness , 2003, Biological Psychiatry.

[44]  M. Codispoti,et al.  When does size not matter? Effects of stimulus size on affective modulation. , 2006, Psychophysiology.

[45]  Carla L. Harenski,et al.  Neural correlates of regulating negative emotions related to moral violations , 2006, NeuroImage.

[46]  S. Nieuwenhuis,et al.  Reappraisal modulates the electrocortical response to unpleasant pictures , 2006, Cognitive, affective & behavioral neuroscience.

[47]  Jejo D. Koola,et al.  Emotion facilitates action: a transcranial magnetic stimulation study of motor cortex excitability during picture viewing. , 2007, Psychophysiology.

[48]  R. Post,et al.  Prefrontal cortex dysfunction in clinical depression , 1994 .

[49]  M. Bradley,et al.  Emotion, Motivation, and Anxiety: Brain Mechanisms and Psychophysiology the Motivational Organization of Emotion Patterns of Human Emotion Emotion and Perception the Psychophysiology of Picture Processing Neural Imaging: Motivation in the Visual Cortex Motivational Circuits in the Brain , 2022 .

[50]  Dan Foti,et al.  Neural response to emotional pictures is unaffected by concurrent task difficulty: an event-related potential study. , 2007, Behavioral neuroscience.

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

[52]  Raymond J. Dolan,et al.  Anxiety Reduction through Detachment: Subjective, Physiological, and Neural Effects , 2005, Journal of Cognitive Neuroscience.

[53]  J. Gabrieli,et al.  Rethinking Feelings: An fMRI Study of the Cognitive Regulation of Emotion , 2002, Journal of Cognitive Neuroscience.

[54]  Greg Hajcak,et al.  See no evil: directing visual attention within unpleasant images modulates the electrocortical response. , 2009, Psychophysiology.

[55]  S. Reeves,et al.  Bilateral Epidural Prefrontal Cortical Stimulation for Treatment-Resistant Depression , 2010, Biological Psychiatry.

[56]  Patricia S. Goldman.  TOPOGRAPHY OF COGNITION: Parallel Distributed Networks in Primate Association Cortex , 1988 .

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

[58]  O. John,et al.  Individual differences in two emotion regulation processes: implications for affect, relationships, and well-being. , 2003, Journal of personality and social psychology.

[59]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[60]  Dan Foti,et al.  Tell me about it: neural activity elicited by emotional pictures and preceding descriptions. , 2009, Emotion.