Enhancing anger perception in older adults by stimulating inferior frontal cortex with high frequency transcranial random noise stimulation

&NA; Extensive behavioural evidence has shown that older people have declined ability in facial emotion perception. Recent work has begun to examine the neural mechanism that contribute to this, and potential tools to support emotion perception during aging. The aim of this study was to investigate whether high frequency tRNS applied to the inferior frontal cortex would enhance facial expression perception in older adults. Healthy aged adults (60+ years) were randomly assigned to receive active high‐frequency or sham tRNS targeted at bilateral inferior frontal cortices. Each group completed tests of facial identity perception, facial happiness perception and facial anger perception. These tasks were completed before and after stimulation. The results showed that, compared to the sham group, the active tRNS group showed greater gains in performance after stimulation in anger perception (relative to performance before stimulation). The same tRNS stimulation did not significantly change performance on the two other face perception tasks assessing facial identity and facial happiness perception. Examination of how inter‐individual variability related to changes in anger perception following tRNS indicated that the degree of performance change in anger perception following active tRNS to inferior frontal cortex was predicted by baseline ability and gender of older adult participants. The findings suggest that high frequency tRNS may be a potential tool to aid anger perception in typical aging, but flag that performance variability and gender may interact with stimulation leading to different outcomes. HighlightsHigh‐frequency tRNS targeted at the inferior frontal cortex improved older adults' anger perception.The degree of improvement was influenced by baseline ability and gender.The same stimulation did not improve happiness perception or identity perception.The findings suggest tRNS as a potential tool to aid old adults' anger perception.

[1]  M. Mather.  The Affective Neuroscience of Aging. , 2016, Annual review of psychology.

[2]  C. Miniussi,et al.  Random Noise Stimulation Improves Neuroplasticity in Perceptual Learning , 2011, The Journal of Neuroscience.

[3]  松岡 恵子,et al.  日本語版National Adult Reading Test(JART)の作成 , 2002 .

[4]  Emiliano Santarnecchi,et al.  Non-invasive brain stimulation of the aging brain: State of the art and future perspectives , 2016, Ageing Research Reviews.

[5]  A. Antal,et al.  Increasing Human Brain Excitability by Transcranial High- Frequency Random Noise Stimulation , 2009, NeuroImage.

[6]  C. Juan,et al.  Individual Differences and State-Dependent Responses in Transcranial Direct Current Stimulation , 2016, Front. Hum. Neurosci..

[7]  Roberto Cabeza,et al.  Aging Gracefully: Compensatory Brain Activity in High-Performing Older Adults , 2002, NeuroImage.

[8]  D. Isaacowitz,et al.  Age effects and gaze patterns in recognising emotional expressions: An in-depth look at gaze measures and covariates , 2010 .

[9]  Justin A. Harris,et al.  Neuroscience and Biobehavioral Reviews Modelling Non-invasive Brain Stimulation in Cognitive Neuroscience , 2022 .

[10]  A. Cronin-Golomb,et al.  Visual scanning patterns and executive function in relation to facial emotion recognition in aging , 2013, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[11]  O. Tzeng,et al.  Unleashing Potential: Transcranial Direct Current Stimulation over the Right Posterior Parietal Cortex Improves Change Detection in Low-Performing Individuals , 2012, The Journal of Neuroscience.

[12]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[13]  P. Reuter-Lorenz,et al.  Neurocognitive Aging and the Compensation Hypothesis , 2008 .

[14]  M. Nitsche,et al.  Anodal-tDCS over the human right occipital cortex enhances the perception and memory of both faces and objects , 2016, Neuropsychologia.

[15]  J. Grafman,et al.  Effects of High-Definition and Conventional tDCS on Response Inhibition , 2016, Brain Stimulation.

[16]  L. M. Ward,et al.  Stochastic resonance and sensory information processing: a tutorial and review of application , 2004, Clinical Neurophysiology.

[17]  R. Cohen Kadosh,et al.  Long-Term Enhancement of Brain Function and Cognition Using Cognitive Training and Brain Stimulation , 2013, Current Biology.

[18]  Morris Moscovitch,et al.  Face Processing Changes in Normal Aging Revealed by fMRI Adaptation , 2011, Journal of Cognitive Neuroscience.

[19]  T. Ruffman,et al.  EMOTION RECOGNITION DEFICITS IN THE ELDERLY , 2004, The International journal of neuroscience.

[20]  Ailbhe N. Finnerty,et al.  Age-related differences in processing face configuration: the importance of the eye region. , 2013, The journals of gerontology. Series B, Psychological sciences and social sciences.

[21]  R. Cabeza.  Hemispheric asymmetry reduction in older adults: the HAROLD model. , 2002, Psychology and aging.

[22]  Sukhvinder S. Obhi,et al.  Task-dependent and distinct roles of the temporoparietal junction and inferior frontal cortex in the control of imitation , 2014, Social cognitive and affective neuroscience.

[23]  K. Nakayama,et al.  Please Scroll down for Article Cognitive Neuropsychology Family Resemblance: Ten Family Members with Prosopagnosia and Within-class Object Agnosia , 2022 .

[24]  R. Cabeza.  Hemispheric asymmetry reduction in older adults: the HAROLD model. , 2002, Psychology and aging.

[25]  B. Bahrami,et al.  Brain Structure Links Loneliness to Social Perception , 2012, Current Biology.

[26]  Geoffrey Bird,et al.  Enhancing Social Ability by Stimulating Right Temporoparietal Junction Tdcs of Right Tpj , 2022 .

[27]  Q. Wang,et al.  Gender Differences in Current Received during Transcranial Electrical Stimulation , 2014, Front. Psychiatry.

[28]  Theodore P. Zanto,et al.  Effects of noninvasive brain stimulation on cognitive function in healthy aging and Alzheimer's disease: a systematic review and meta-analysis , 2015, Neurobiology of Aging.

[29]  Skyler T. Hawk,et al.  Presentation and validation of the Radboud Faces Database , 2010 .

[30]  Jeffery J. Summers,et al.  Does transcranial direct current stimulation enhance cognitive and motor functions in the ageing brain? A systematic review and meta- analysis , 2016, Ageing Research Reviews.

[31]  Emiliano Santarnecchi,et al.  State-Dependent Effects of Transcranial Oscillatory Currents on the Motor System: What You Think Matters , 2013, The Journal of Neuroscience.

[32]  Chi-Hung Juan,et al.  Transcranial direct current stimulation over right posterior parietal cortex changes prestimulus alpha oscillation in visual short-term memory task , 2014, NeuroImage.

[33]  Natalie C. Ebner,et al.  Oxytocin and socioemotional aging: Current knowledge and future trends , 2013, Front. Hum. Neurosci..

[34]  J. Henry,et al.  A meta-analytic review of emotion recognition and aging: Implications for neuropsychological models of aging , 2008, Neuroscience & Biobehavioral Reviews.

[35]  Roi Cohen Kadosh,et al.  Not all brains are created equal: the relevance of individual differences in responsiveness to transcranial electrical stimulation , 2014, Front. Syst. Neurosci..

[36]  Corinna E. Löckenhoff,et al.  Age differences in recognition of emotion in lexical stimuli and facial expressions. , 2007, Psychology and aging.

[37]  Patrick Ragert,et al.  The medial frontal cortex mediates self-other discrimination in the joint Simon task: A tDCS study , 2016 .

[38]  N. George,et al.  Older adults' configural processing of faces: role of second-order information. , 2011, Psychology and aging.

[39]  K. Nakamura,et al.  Activation of the right inferior frontal cortex during assessment of facial emotion. , 1999, Journal of neurophysiology.

[40]  Natalie C. Ebner,et al.  Emotion and aging: evidence from brain and behavior , 2014, Front. Psychol..

[41]  S. Hutton,et al.  Age differences in emotion recognition skills and the visual scanning of emotion faces. , 2007, The journals of gerontology. Series B, Psychological sciences and social sciences.

[42]  Norihiro Sadato,et al.  Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: an event-related fMRI study , 2004, NeuroImage.

[43]  Lars Nyberg,et al.  Age-related differences in brain regions supporting successful encoding of emotional faces , 2010, Cortex.

[44]  K. K. Tan,et al.  The spatial location of EEG electrodes: locating the best-fitting sphere relative to cortical anatomy. , 1993, Electroencephalography and clinical neurophysiology.

[45]  Michael J. Banissy,et al.  Enhancing Anger Perception With Transcranial Alternating Current Stimulation Induced Gamma Oscillations , 2015, Brain Stimulation.

[46]  P. McGuire,et al.  Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. , 2009, Journal of psychiatry & neuroscience : JPN.

[47]  A. Antal,et al.  Comparing cutaneous perception induced by electrical stimulation using rectangular and round shaped electrodes , 2011, Clinical Neurophysiology.

[48]  Ken Nakayama,et al.  No global processing deficit in the Navon task in 14 developmental prosopagnosics. , 2007, Social cognitive and affective neuroscience.

[49]  Geoffrey Bird,et al.  Functional lateralization of temporoparietal junction – imitation inhibition, visual perspective‐taking and theory of mind , 2015, The European journal of neuroscience.

[50]  Roberta Sellaro,et al.  The stimulated social brain: effects of transcranial direct current stimulation on social cognition , 2016, Annals of the New York Academy of Sciences.

[51]  Xin Zheng,et al.  Effects of transcranial direct current stimulation (tDCS) on human regional cerebral blood flow , 2011, NeuroImage.

[52]  Qingyang Li,et al.  Emotional perception: Meta-analyses of face and natural scene processing , 2011, NeuroImage.

[53]  Ann Dowker,et al.  Cognitive Enhancement or Cognitive Cost: Trait-Specific Outcomes of Brain Stimulation in the Case of Mathematics Anxiety , 2014, The Journal of Neuroscience.

[54]  Bonnie Wong,et al.  Patterns of visual scanning as predictors of emotion identification in normal aging. , 2005, Neuropsychology.

[55]  Carles Falcón,et al.  Repetitive transcranial magnetic stimulation effects on brain function and cognition among elders with memory dysfunction. A randomized sham-controlled study. , 2006, Cerebral cortex.

[56]  E. Frank,et al.  Recognition of Nonverbal Communication of Affect Following Traumatic Brain Injury , 2000 .

[57]  M. Banissy,et al.  Social perception in synaesthesia for colour , 2016, Cognitive neuropsychology.

[58]  Walter Paulus,et al.  Gender-specific modulation of short-term neuroplasticity in the visual cortex induced by transcranial direct current stimulation , 2008, Visual Neuroscience.

[59]  V. Walsh,et al.  Modulating Neuronal Activity Produces Specific and Long-Lasting Changes in Numerical Competence , 2010, Current Biology.

[60]  B. Duchaine,et al.  High-Frequency Transcranial Random Noise Stimulation Enhances Perception of Facial Identity , 2015, Cerebral cortex.

[61]  F. Fregni,et al.  Bilateral temporal cortex transcranial direct current stimulation worsens male performance in a multisensory integration task , 2012, Neuroscience Letters.

[62]  Normal social evaluations of faces in acquired prosopagnosia , 2014, Cortex.

[63]  N. Sadato,et al.  Brain regions involved in verbal or non‐verbal aspects of facial emotion recognition , 2000, Neuroreport.