Battery powered thought: Enhancement of attention, learning, and memory in healthy adults using transcranial direct current stimulation

This article reviews studies demonstrating enhancement with transcranial direct current stimulation (tDCS) of attention, learning, and memory processes in healthy adults. Given that these are fundamental cognitive functions, they may also mediate stimulation effects on other higher-order processes such as decision-making and problem solving. Although tDCS research is still young, there have been a variety of methods used and cognitive processes tested. While these different methods have resulted in seemingly contradictory results among studies, many consistent and noteworthy effects of tDCS on attention, learning, and memory have been reported. The literature suggests that although tDCS as typically applied may not be as useful for localization of function in the brain as some other methods of brain stimulation, tDCS may be particularly well-suited for practical applications involving the enhancement of attention, learning, and memory, in both healthy subjects and in clinical populations.

[1]  S Marceglia,et al.  Improved isometric force endurance after transcranial direct current stimulation over the human motor cortical areas , 2007, The European journal of neuroscience.

[2]  M. Nitsche,et al.  Pharmacological Modulation of Cortical Excitability Shifts Induced by Transcranial Direct Current Stimulation in Humans , 2003, The Journal of physiology.

[3]  O. Lippold,et al.  A Preliminary Account of the Clinical Effects of Polarizing the Brain in Certain Psychiatric Disorders , 1964, British Journal of Psychiatry.

[4]  R Dolhem,et al.  [The history of electrostimulation in rehabilitation medicine]. , 2008, Annales de readaptation et de medecine physique : revue scientifique de la Societe francaise de reeducation fonctionnelle de readaptation et de medecine physique.

[5]  Korsakov Ia,et al.  Psychophysical characteristics of perception and of brain electrical activity during occipital micropolarization. , 1982 .

[6]  James L Olds,et al.  Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. , 1954, Journal of comparative and physiological psychology.

[7]  Walter Paulus,et al.  Introducing graph theory to track for neuroplastic alterations in the resting human brain: A transcranial direct current stimulation study , 2011, NeuroImage.

[8]  Mark S. George,et al.  Reducing procedural pain and discomfort associated with transcranial direct current stimulation , 2011, Brain Stimulation.

[9]  O. Lippold,et al.  Mental Changes Resulting from the Passage of Small Direct Currents Through the Human Brain , 1964, British Journal of Psychiatry.

[10]  A. Antal,et al.  Electrode-distance dependent after-effects of transcranial direct and random noise stimulation with extracephalic reference electrodes , 2010, Clinical Neurophysiology.

[11]  Scott T. Grafton,et al.  Human functional anatomy of visually guided finger movements. , 1992, Brain : a journal of neurology.

[12]  T. Robbins,et al.  The neuropsychology of ventral prefrontal cortex: Decision-making and reversal learning , 2004, Brain and Cognition.

[13]  Walter Paulus,et al.  Therapeutic effects of non-invasive brain stimulation with direct currents (tDCS) in neuropsychiatric diseases , 2014, NeuroImage.

[14]  Gottfried Schlaug,et al.  Contralateral and ipsilateral motor effects after transcranial direct current stimulation , 2006, Neuroreport.

[15]  D. Reato,et al.  Gyri – precise head model of transcranial DC stimulation : Improved spatial focality using a ring electrode versus conventional rectangular pad , 2010 .

[16]  Catherine E. Myers,et al.  Relative Risk of Probabilistic Category Learning Deficits in Patients with Schizophrenia and Their Siblings , 2010, Biological Psychiatry.

[17]  R. Engle Working Memory Capacity as Executive Attention , 2002 .

[18]  P. Enticott,et al.  Improving working memory: the effect of combining cognitive activity and anodal transcranial direct current stimulation to the left dorsolateral prefrontal cortex , 2011, Brain Stimulation.

[19]  S. Kéri,et al.  Probabilistic classification learning in Tourette syndrome , 2002, Neuropsychologia.

[20]  Chang-Hwan Im,et al.  A Novel Array-Type Transcranial Direct Current Stimulation (tDCS) System for Accurate Focusing on Targeted Brain Areas , 2010, IEEE Transactions on Magnetics.

[21]  V. Clark,et al.  Impact of tDCS on performance and learning of target detection: Interaction with stimulus characteristics and experimental design , 2012, Neuropsychologia.

[22]  G. Fink,et al.  Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches , 2011, Brain : a journal of neurology.

[23]  P. Lachenbruch Statistical Power Analysis for the Behavioral Sciences (2nd ed.) , 1989 .

[24]  Alberto Leal,et al.  Comparing different electrode configurations using the 10-10 international system in tDCS: A finite element model analysis , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[25]  K. Hoffmann,et al.  Direct Current Stimulation over V5 Enhances Visuomotor Coordination by Improving Motion Perception in Humans , 2004, Journal of Cognitive Neuroscience.

[26]  N. Bolognini,et al.  Enhancing multisensory spatial orienting by brain polarization of the parietal cortex , 2010, The European journal of neuroscience.

[27]  J. Jefferys,et al.  Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro , 2004, The Journal of physiology.

[28]  A. Shapiro,et al.  A HISTORIC AND HEURISTIC DEFINITION OF THE PLACEBO. , 1964, Psychiatry.

[29]  Ingrid R. Olson,et al.  A selective working memory impairment after transcranial direct current stimulation to the right parietal lobe , 2010, Neuroscience Letters.

[30]  K. Willmes,et al.  On the Functional Neuroanatomy of Intrinsic and Phasic Alertness , 2001, NeuroImage.

[31]  Ethan R. Buch,et al.  Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation , 2009, Proceedings of the National Academy of Sciences.

[32]  R. Parasuraman The attentive brain , 1998 .

[33]  M. Nitsche,et al.  Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. , 2002, Brain : a journal of neurology.

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

[35]  Joel S. Warm,et al.  Vigilance Requires Hard Mental Work and Is Stressful , 2008, Hum. Factors.

[36]  P. Matthews,et al.  Polarity-Sensitive Modulation of Cortical Neurotransmitters by Transcranial Stimulation , 2009, The Journal of Neuroscience.

[37]  Sara Marceglia,et al.  Cerebellar Transcranial Direct Current Stimulation Impairs the Practice-dependent Proficiency Increase in Working Memory , 2008, Journal of Cognitive Neuroscience.

[38]  G. Fink,et al.  Bidirectional alterations of interhemispheric parietal balance by non-invasive cortical stimulation. , 2009, Brain : a journal of neurology.

[39]  Colleen Loo,et al.  Transcranial direct current stimulation influences probabilistic association learning in schizophrenia , 2011, Schizophrenia Research.

[40]  D. Reato,et al.  Gyri-precise head model of transcranial direct current stimulation: Improved spatial focality using a ring electrode versus conventional rectangular pad , 2009, Brain Stimulation.

[41]  F. Fregni,et al.  Enhancement of selective attention by tDCS: Interaction with interference in a Sternberg task , 2012, Neuroscience Letters.

[42]  Violeta Dimova,et al.  Electrified minds: Transcranial direct current stimulation (tDCS) and Galvanic Vestibular Stimulation (GVS) as methods of non-invasive brain stimulation in neuropsychology—A review of current data and future implications , 2010, Neuropsychologia.

[43]  J. Aronowitz,et al.  Ethereal fire: antecedents of radiology and radiotherapy. , 2007, AJR. American journal of roentgenology.

[44]  Joel S. Warm,et al.  Enhancing vigilance in operators with prefrontal cortex transcranial direct current stimulation (tDCS) , 2014, NeuroImage.

[45]  M. Posner,et al.  The attention system of the human brain. , 1990, Annual review of neuroscience.

[46]  M. Nitsche,et al.  External modulation of visual perception in humans , 2001, Neuroreport.

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

[48]  Walter Paulus,et al.  Modulation of moving phosphene thresholds by transcranial direct current stimulation of V1 in human , 2003, Neuropsychologia.

[49]  C. Bundesen A theory of visual attention. , 1990, Psychological review.

[50]  Alvaro Pascual-Leone,et al.  Effects of transcranial direct current stimulation on working memory in patients with Parkinson's disease , 2006, Journal of the Neurological Sciences.

[51]  Leslie G. Ungerleider,et al.  Imaging Brain Plasticity during Motor Skill Learning , 2002, Neurobiology of Learning and Memory.

[52]  A. Priori Brain polarization in humans: a reappraisal of an old tool for prolonged non-invasive modulation of brain excitability , 2003, Clinical Neurophysiology.

[53]  Myoung-Hwan Ko,et al.  Enhancing the Working Memory of Stroke Patients Using tDCS , 2009, American journal of physical medicine & rehabilitation.

[54]  M. Clare,et al.  ANALYSIS OF THE FORM AND DISTRIBUTION OF EVOKED CORTICAL POTENTIALS UNDER THE INFLUENCE OF POLARIZING CURRENTS. , 1964, Journal of neurophysiology.

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

[56]  Ethan R. Buch,et al.  Noninvasive brain stimulation: from physiology to network dynamics and back , 2013, Nature Neuroscience.

[57]  Paul Sacco,et al.  Modulation of internal model formation during force field‐induced motor learning by anodal transcranial direct current stimulation of primary motor cortex , 2009, The Journal of physiology.

[58]  Guglielmo Foffani,et al.  Prefrontal hemodynamic changes produced by anodal direct current stimulation , 2010, NeuroImage.

[59]  Markus Zahn,et al.  Transcranial direct current stimulation: A computer-based human model study , 2007, NeuroImage.

[60]  M. Nitsche,et al.  Modulating functional connectivity patterns and topological functional organization of the human brain with transcranial direct current stimulation , 2011, Human brain mapping.

[61]  C A Terzuolo,et al.  MEASUREMENT OF IMPOSED VOLTAGE GRADIENT ADEQUATE TO MODULATE NEURONAL FIRING. , 1956, Proceedings of the National Academy of Sciences of the United States of America.

[62]  P. Kellaway,et al.  The part played by electric fish in the early history of bioelectricity and electrotherapy. , 1946, Bulletin of the history of medicine.

[63]  V. Clark,et al.  Transcranial direct current stimulation (tDCS) produces localized and specific alterations in neurochemistry: A 1H magnetic resonance spectroscopy study , 2011, Neuroscience Letters.

[64]  L. Bindman,et al.  The action of brief polarizing currents on the cerebral cortex of the rat (1) during current flow and (2) in the production of long‐lasting after‐effects , 1964, The Journal of physiology.

[65]  Vince D. Calhoun,et al.  TDCS guided using fMRI significantly accelerates learning to identify concealed objects , 2012, NeuroImage.

[66]  Ralph Weidner,et al.  Enhanced visual selection after 2 mA cathodal tDCS of right intraparietal sulcus in healthy subjects , 2012 .

[67]  L. Cohen,et al.  Transcranial direct current stimulation: State of the art 2008 , 2008, Brain Stimulation.

[68]  D. Kumaran,et al.  Frames, Biases, and Rational Decision-Making in the Human Brain , 2006, Science.

[69]  O. Creutzfeldt,et al.  Influence of transcortical d-c currents on cortical neuronal activity. , 1962, Experimental neurology.

[70]  Y. Kim,et al.  Time-dependent effect of transcranial direct current stimulation on the enhancement of working memory , 2008, Neuroreport.

[71]  N J Davey,et al.  Somatotopy of Perceptual Threshold to Cutaneous Electrical Stimulation in Man , 2001, Experimental physiology.

[72]  John S. Duncan,et al.  Challenging the classical distinction between long-term and short-term memory: reconsidering the role of the hippocampus , 2011 .

[73]  Raja Parasuraman,et al.  Complacency and Bias in Human Use of Automation: An Attentional Integration , 2010, Hum. Factors.

[74]  S. Shimojo,et al.  Illusions: What you see is what you hear , 2000, Nature.

[75]  Sergio P. Rigonatti,et al.  Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory , 2005, Experimental Brain Research.

[76]  S. Reeves,et al.  A pilot study of the tolerability and effects of high-definition transcranial direct current stimulation (HD-tDCS) on pain perception. , 2011, The journal of pain : official journal of the American Pain Society.

[77]  S. Knecht,et al.  Non-invasive brain stimulation improves object-location learning in the elderly , 2012, Neurobiology of Aging.

[78]  Heidi M. Schambra,et al.  Direct Current Stimulation Promotes BDNF-Dependent Synaptic Plasticity: Potential Implications for Motor Learning , 2010, Neuron.

[79]  M. Nitsche,et al.  Shaping the effects of transcranial direct current stimulation of the human motor cortex. , 2007, Journal of neurophysiology.

[80]  V. Clark,et al.  Enhancement of object detection with transcranial direct current stimulation is associated with increased attention , 2012, BMC Neuroscience.

[81]  J. D.,et al.  THE EFFECTS OF POLARIZING CURRENTS ON THE CONSOLIDATION OF LEARNING , 2002 .

[82]  C. Tesche,et al.  Transcranial direct current stimulation modulates shifts in global/local attention , 2009, Neuroreport.

[83]  Aaron R. Seitz,et al.  A unified model for perceptual learning , 2005, Trends in Cognitive Sciences.

[84]  G MEYER-SCHWICKERATH,et al.  [Selective electric excitability of various portions of the retina]. , 1951, Albrecht von Graefe's Archiv fur Ophthalmologie.

[85]  M. Nitsche,et al.  Facilitation of Implicit Motor Learning by Weak Transcranial Direct Current Stimulation of the Primary Motor Cortex in the Human , 2003, Journal of Cognitive Neuroscience.

[86]  Sarah E. Pekny,et al.  Stimulation of the Human Motor Cortex Alters Generalization Patterns of Motor Learning , 2011, The Journal of Neuroscience.

[87]  M. Hallett,et al.  Modulation of cortical motor output maps during development of implicit and explicit knowledge. , 1994, Science.

[88]  R. Veit,et al.  The truth about lying: inhibition of the anterior prefrontal cortex improves deceptive behavior. , 2010, Cerebral cortex.

[89]  F. Castellanos,et al.  Characterizing cognition in ADHD: beyond executive dysfunction , 2006, Trends in Cognitive Sciences.

[90]  Pablo Celnik,et al.  Brain polarization enhances the formation and retention of motor memories. , 2009, Journal of neurophysiology.

[91]  M. Hallett,et al.  What does the ratio of injected current to electrode area tell us about current density in the brain during tDCS? , 2009, Clinical Neurophysiology.

[92]  Walter Paulus,et al.  Modulation of motor consolidation by external DC stimulation. , 2003, Supplements to Clinical neurophysiology.

[93]  P. Hancock,et al.  Cerebral lateralization of vigilance: A function of task difficulty , 2010, Neuropsychologia.

[94]  G. Meyer-Schwickerath,et al.  Über selektive elektrische Erregbarkeit verschiedener Netzhautanteile , 1951, Albrecht von Graefes Archiv für Ophthalmologie.

[95]  Jin Fan,et al.  The activation of attentional networks , 2005, NeuroImage.

[96]  Walter Paulus,et al.  Facilitation of probabilistic classification learning by transcranial direct current stimulation of the prefrontal cortex in the human , 2004, Neuropsychologia.

[97]  D. Purpura,et al.  INTRACELLULAR ACTIVITIES AND EVOKED POTENTIAL CHANGES DURING POLARIZATION OF MOTOR CORTEX. , 1965, Journal of neurophysiology.

[98]  Min Jae Baek,et al.  Non-invasive cortical stimulation improves post-stroke attention decline. , 2009, Restorative neurology and neuroscience.

[99]  Jan Born,et al.  Bifrontal transcranial direct current stimulation slows reaction time in a working memory task , 2005, BMC Neuroscience.

[100]  Géza Gergely Ambrus,et al.  Cutaneous perception thresholds of electrical stimulation methods: Comparison of tDCS and tRNS , 2010, Clinical Neurophysiology.

[101]  L. Squire The neuropsychology of human memory. , 1982, Annual review of neuroscience.

[102]  Raja Parasuraman,et al.  Neuroergonomics , 2011 .

[103]  James C. Christensen,et al.  Neuroergonomics: The brain in action and at work , 2012, NeuroImage.

[104]  M. Hallett,et al.  Dynamic cortical involvement in implicit and explicit motor sequence learning. A PET study. , 1998, Brain : a journal of neurology.

[105]  Raja Parasuraman,et al.  Transcranial Direct Current Stimulation Augments Perceptual Sensitivity and 24-Hour Retention in a Complex Threat Detection Task , 2012, PloS one.

[106]  P. Koehler,et al.  A history of non-drug treatment in headache, particularly migraine. , 2010, Brain : a journal of neurology.

[107]  F. Fregni,et al.  Temporal cortex direct current stimulation enhances performance on a visual recognition memory task in Alzheimer disease , 2008, Journal of Neurology, Neurosurgery, and Psychiatry.

[108]  I A Korsakov,et al.  Psychophysical characteristics of perception and of brain electrical activity during occipital micropolarization. , 1982, Human physiology.

[109]  Thomas F Münte,et al.  Errorless and errorful learning modulated by transcranial direct current stimulation , 2011, BMC Neuroscience.

[110]  J. Thorne,et al.  Transcranial direct current stimulation of the prefrontal cortex modulates working memory performance: combined behavioural and electrophysiological evidence , 2011, BMC Neuroscience.

[111]  Walter Paulus,et al.  Manipulation of phosphene thresholds by transcranial direct current stimulation in man , 2003, Experimental Brain Research.

[112]  B. Bussel,et al.  Effects of anodal tDCS on lumbar propriospinal system in healthy subjects , 2012, Clinical Neurophysiology.

[113]  M. Nitsche,et al.  Modulating cortico‐striatal and thalamo‐cortical functional connectivity with transcranial direct current stimulation , 2012, Human brain mapping.

[114]  Walter Paulus,et al.  Facilitation of visuo‐motor learning by transcranial direct current stimulation of the motor and extrastriate visual areas in humans , 2004, The European journal of neuroscience.

[115]  Gyula Kovács,et al.  Direct current stimulation over MT+/V5 modulates motion aftereffect in humans , 2004, Neuroreport.

[116]  Jordan Grafman,et al.  Bilateral frontal transcranial direct current stimulation: Failure to replicate classic findings in healthy subjects , 2009, Clinical Neurophysiology.

[117]  B. Rockstroh,et al.  The influence of low-level transcortical DC-currents on response speed in humans. , 1981, The International journal of neuroscience.

[118]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[119]  P. Matthews,et al.  Polarity and timing-dependent effects of transcranial direct current stimulation in explicit motor learning , 2011, Neuropsychologia.

[120]  J. Born,et al.  Transcranial Direct Current Stimulation during Sleep Improves Declarative Memory , 2004, The Journal of Neuroscience.

[121]  R. Dolhem,et al.  [The history of electrostimulation in rehabilitation medicine]. , 2008, Annales de readaptation et de medecine physique : revue scientifique de la Societe francaise de reeducation fonctionnelle de readaptation et de medecine physique.

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

[123]  Raymond J. Wlodkowski Accelerated learning in colleges and universities , 2003 .

[124]  Abhishek Datta,et al.  One-dimensional representation of a neuron in a uniform electric field , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[125]  Jacob Cohen Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.