Effects of Transcranial Alternating Current Stimulation on Cognitive Functions in Healthy Young and Older Adults

Recently, transcranial alternating current stimulation (tACS) has emerged as a tool to enhance human cognitive processes. Here, we provide a brief summary of the rationale behind tACS-induced effects on task-relevant brain oscillations and associated cognitive functions and review previous studies in young subjects that have applied tACS in cognitive paradigms. Additionally, we present pilot data where we administered theta-tACS (6 Hz) over the temporoparietal cortex and a supraorbital reference for 20 min during implicit language learning in healthy young (mean/SD age: 22/2) and older (mean/SD age: 66/4) adults, in a sham-controlled crossover design. Linear mixed models revealed significantly increased retrieval accuracy following tACS-accompanied associative learning, after controlling for session order and learning success. These data provide the first implementation of tACS during cognitive performance in older adults and support recent studies suggesting that tACS in the theta frequency range may serve as a tool to enhance cognition, possibly through direct modulation of task-relevant brain oscillations. So far, studies have been heterogeneous in their designs, leaving a number of issues to be addressed in future research, including the setup of electrodes and optimal stimulation frequencies to be employed, as well as the interaction with age and underlying brain pathologies in specific patient populations.

[1]  Christoph S. Herrmann,et al.  BOLD signal effects of transcranial alternating current stimulation (tACS) in the alpha range: A concurrent tACS–fMRI study , 2016, NeuroImage.

[2]  Walter Paulus,et al.  Transcranial electrical stimulation of the occipital cortex during visual perception modifies the magnitude of BOLD activity: A combined tES–fMRI approach , 2016, NeuroImage.

[3]  A. Engel,et al.  EEG oscillations: From correlation to causality. , 2016, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[4]  Timothy H. Muller,et al.  Individual differences and specificity of prefrontal gamma frequency-tACS on fluid intelligence capabilities , 2016, Cortex.

[5]  N. Wenderoth,et al.  A technical guide to tDCS, and related non-invasive brain stimulation tools , 2016, Clinical Neurophysiology.

[6]  Paul B. Fitzgerald,et al.  The effect of γ-tACS on working memory performance in healthy controls , 2015, Brain and Cognition.

[7]  Peter Dechent,et al.  Transcranial alternating current stimulation affects the BOLD signal in a frequency and task‐dependent manner , 2015, Human brain mapping.

[8]  X. Zuo,et al.  Neuroscience and Biobehavioral Reviews Putting Age-related Task Activation into Large-scale Brain Networks: a Meta-analysis of 114 Fmri Studies on Healthy Aging , 2022 .

[9]  Michael X. Cohen,et al.  Frequency Band-Specific Electrical Brain Stimulation Modulates Cognitive Control Processes , 2015, PloS one.

[10]  A. Antal,et al.  Bi-frontal transcranial alternating current stimulation in the ripple range reduced overnight forgetting , 2015, Front. Cell. Neurosci..

[11]  A. Flöel,et al.  Potentials and limits to enhance cognitive functions in healthy and pathological aging by tDCS , 2015, Front. Cell. Neurosci..

[12]  R. Lindenberg,et al.  Transcranial direct current stimulation in mild cognitive impairment: Behavioral effects and neural mechanisms , 2015, Alzheimer's & Dementia.

[13]  M. Grueschow,et al.  The precision of value-based choices depends causally on fronto-parietal phase coupling , 2015, Nature Communications.

[14]  G. Thut,et al.  The implications of state-dependent tDCS effects in aging: Behavioural response is determined by baseline performance , 2015, Neuropsychologia.

[15]  Lars Riecke,et al.  4-Hz Transcranial Alternating Current Stimulation Phase Modulates Hearing , 2015, Brain Stimulation.

[16]  D. Antonenko,et al.  Improved memory consolidation by slow oscillatory brain stimulation during an afternoon nap in older adults , 2015, Alzheimer's & Dementia.

[17]  David Bartrés-Faz,et al.  Reorganization of brain networks in aging: a review of functional connectivity studies , 2015, Front. Psychol..

[18]  Christoph S. Herrmann,et al.  Increase in short-term memory capacity induced by down-regulating individual theta frequency via transcranial alternating current stimulation , 2015, Front. Hum. Neurosci..

[19]  M. Nitsche,et al.  Transcranial direct current stimulation (tDCS) – Application in neuropsychology , 2015, Neuropsychologia.

[20]  Kristin K Sellers,et al.  Targeting the neurophysiology of cognitive systems with transcranial alternating current stimulation , 2015, Expert review of neurotherapeutics.

[21]  A. Pahor,et al.  The effects of theta transcranial alternating current stimulation (tACS) on fluid intelligence. , 2014, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[22]  A. Engel,et al.  Entrainment of Brain Oscillations by Transcranial Alternating Current Stimulation , 2014, Current Biology.

[23]  Norbert Jaušovec,et al.  The influence of theta transcranial alternating current stimulation (tACS) on working memory storage and processing functions. , 2014, Acta psychologica.

[24]  Norbert Jaušovec,et al.  Increasing working memory capacity with theta transcranial alternating current stimulation (tACS) , 2014, Biological Psychology.

[25]  Michal Lavidor,et al.  Prefrontal oscillatory stimulation modulates access to cognitive control references in retrospective metacognitive commentary , 2014, Clinical Neurophysiology.

[26]  R. Lindenberg,et al.  Transcranial direct current stimulation over multiple days improves learning and maintenance of a novel vocabulary , 2014, Cortex.

[27]  Agnes Flöel,et al.  tDCS-enhanced motor and cognitive function in neurological diseases , 2014, NeuroImage.

[28]  F. Fregni,et al.  Head-to-Head Comparison of Transcranial Random Noise Stimulation, Transcranial AC Stimulation, and Transcranial DC Stimulation for Tinnitus , 2013, Front. Psychiatry.

[29]  Shu-Chen Li Neuromodulation and developmental contextual influences on neural and cognitive plasticity across the lifespan , 2013, Neuroscience & Biobehavioral Reviews.

[30]  L. Parra,et al.  Effects of weak transcranial alternating current stimulation on brain activity—a review of known mechanisms from animal studies , 2013, Front. Hum. Neurosci..

[31]  Lisa Marshall,et al.  Contribution of transcranial oscillatory stimulation to research on neural networks: an emphasis on hippocampo-neocortical rhythms , 2013, Front. Hum. Neurosci..

[32]  Justin A. Harris,et al.  Modelling non-invasive brain stimulation in cognitive neuroscience , 2013, Neuroscience & Biobehavioral Reviews.

[33]  Laura E. Matzen,et al.  Frequency-Dependent Enhancement of Fluid Intelligence Induced by Transcranial Oscillatory Potentials , 2013, Current Biology.

[34]  L. Colgin Mechanisms and functions of theta rhythms. , 2013, Annual review of neuroscience.

[35]  A. Antal,et al.  Transcranial alternating current stimulation (tACS) , 2013, Front. Hum. Neurosci..

[36]  C. Herrmann,et al.  Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes , 2013, Front. Hum. Neurosci..

[37]  C. Herrmann,et al.  Orchestrating neuronal networks: sustained after-effects of transcranial alternating current stimulation depend upon brain states , 2013, Front. Hum. Neurosci..

[38]  J. Born,et al.  Napping to renew learning capacity: enhanced encoding after stimulation of sleep slow oscillations , 2013, The European journal of neuroscience.

[39]  P. Brown,et al.  Tremor Suppression by Rhythmic Transcranial Current Stimulation , 2013, Current Biology.

[40]  P. Rossini,et al.  Basic Principles and Methodological Aspects of Transcranial Magnetic Stimulation , 2012 .

[41]  M. Nitsche,et al.  The Importance of Timing in Segregated Theta Phase-Coupling for Cognitive Performance , 2012, Current Biology.

[42]  M. Nitsche,et al.  Effects of Transcranial Electrical Stimulation on Cognition , 2012, Clinical EEG and neuroscience.

[43]  C. Grady The cognitive neuroscience of ageing , 2012, Nature Reviews Neuroscience.

[44]  M. Lavidor,et al.  Transcranial Alternating Current Stimulation Increases Risk-Taking Behavior in the Balloon Analog Risk Task , 2011, Front. Neurosci..

[45]  Rachel Holland,et al.  Can tDCS enhance treatment of aphasia after stroke? , 2011, Aphasiology.

[46]  M. Koslowsky,et al.  tDCS polarity effects in motor and cognitive domains: a meta-analytical review , 2011, Experimental Brain Research.

[47]  C. Herrmann,et al.  Transcranial Alternating Current Stimulation Enhances Individual Alpha Activity in Human EEG , 2010, PloS one.

[48]  D. McCormick,et al.  Endogenous Electric Fields May Guide Neocortical Network Activity , 2010, Neuron.

[49]  Walter Paulus,et al.  Boosting brain excitability by transcranial high frequency stimulation in the ripple range , 2010, The Journal of physiology.

[50]  Lars Bäckman,et al.  Implicit Learning in Aging: Extant Patterns and New Directions , 2009, Neuropsychology Review.

[51]  Stefan Knecht,et al.  Noninvasive Brain Stimulation Improves Language Learning , 2008, Journal of Cognitive Neuroscience.

[52]  A. Antal,et al.  Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients , 2007, Brain Research Bulletin.

[53]  L. Cohen,et al.  Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation , 2006, Clinical Neurophysiology.

[54]  Thomas Wolbers,et al.  Hippocampus activity differentiates good from poor learners of a novel lexicon , 2005, NeuroImage.

[55]  Caterina Breitenstein,et al.  Development and validation of a language learning model for behavioral and functional-imaging studies , 2002, Journal of Neuroscience Methods.

[56]  Ana Ivelisse Avilés,et al.  Linear Mixed Models for Longitudinal Data , 2001, Technometrics.

[57]  G. Molenberghs,et al.  Linear Mixed Models for Longitudinal Data , 2001 .

[58]  M. Nitsche,et al.  Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation , 2000, The Journal of physiology.

[59]  W. Klimesch EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[60]  D. Watson,et al.  Development and validation of brief measures of positive and negative affect: the PANAS scales. , 1988, Journal of personality and social psychology.

[61]  F. Fröhlich,et al.  Experiments and models of cortical oscillations as a target for noninvasive brain stimulation. , 2015, Progress in brain research.

[62]  A. Engel,et al.  Antiphasic 40 Hz Oscillatory Current Stimulation Affects Bistable Motion Perception , 2013, Brain Topography.

[63]  Aneta Szymaszek,et al.  Non-invasive alternating current stimulation induces recovery from stroke. , 2010, Restorative neurology and neuroscience.