Delayed enhancement of multitasking performance: Effects of anodal transcranial direct current stimulation on the prefrontal cortex

BACKGROUND The dorsolateral prefrontal cortex (DLPFC) has been proposed to play an important role in neural processes that underlie multitasking performance. However, this claim is underexplored in terms of direct causal evidence. OBJECTIVE The current study aimed to delineate the causal involvement of the DLPFC during multitasking by modulating neural activity with transcranial direct current stimulation (tDCS) prior to engagement in a demanding multitasking paradigm. METHODS The study is a single-blind, crossover, sham-controlled experiment. Anodal tDCS or sham tDCS was applied over left DLPFC in forty-one healthy young adults (aged 18-35 years) immediately before they engaged in a 3-D video game designed to assess multitasking performance. Participants were separated into three subgroups: real-sham (i.e., real tDCS in the first session, followed by sham tDCS in the second session 1 h later), sham-real (sham tDCS first session, real tDCS second session), and sham-sham (sham tDCS in both sessions). RESULTS The real-sham group showed enhanced multitasking performance and decreased multitasking cost during the second session, compared to first session, suggesting delayed cognitive benefits of tDCS. Interestingly, performance benefits were observed only for multitasking and not on a single-task version of the game. No significant changes were found between the first and second sessions for either the sham-real or the sham-sham groups. CONCLUSIONS These results suggest a causal role of left prefrontal cortex in facilitating the simultaneous performance of more than one task, or multitasking. Moreover, these findings reveal that anodal tDCS may have delayed benefits that reflect an enhanced rate of learning.

[1]  R. Marois,et al.  The attentional blink: A review of data and theory , 2009, Attention, perception & psychophysics.

[2]  M. Nitsche,et al.  Excitability changes induced in the human primary visual cortex by transcranial direct current stimulation: direct electrophysiological evidence. , 2004, Investigative ophthalmology & visual science.

[3]  M. Nitsche,et al.  Physiological Basis of Transcranial Direct Current Stimulation , 2011, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[4]  L. Leyman,et al.  The influence of rTMS over the left dorsolateral prefrontal cortex on Stroop task performance , 2006, Experimental Brain Research.

[5]  Neil A. Macmillan,et al.  Detection theory: A user's guide, 2nd ed. , 2005 .

[6]  M. Bikson,et al.  Role of cortical cell type and morphology in subthreshold and suprathreshold uniform electric field stimulation in vitro , 2009, Brain Stimulation.

[7]  Susan M. Ravizza,et al.  Shifting set about task switching: Behavioral and neural evidence for distinct forms of cognitive flexibility , 2008, Neuropsychologia.

[8]  H. Pashler.  Dual-task interference in simple tasks: data and theory. , 1994, Psychological bulletin.

[9]  N. Birbaumer,et al.  Enhancement of Planning Ability by Transcranial Direct Current Stimulation , 2009, The Journal of Neuroscience.

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

[11]  Camarin E. Rolle,et al.  Video game training enhances cognitive control in older adults , 2013, Nature.

[12]  T. Goldberg,et al.  Uncoupling Cognitive Workload and Prefrontal Cortical Physiology: A PET rCBF Study , 1998, NeuroImage.

[13]  M. D’Esposito,et al.  Functional connectivity during working memory maintenance , 2004, Cognitive, affective & behavioral neuroscience.

[14]  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.

[15]  D. Schutter,et al.  Inhibitory deficits in the dorsolateral prefrontal cortex in psychopathic offenders , 2013, Cortex.

[16]  Walter Paulus,et al.  Modulation of cortical excitability by weak direct current stimulation--technical, safety and functional aspects. , 2003, Supplements to Clinical neurophysiology.

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

[18]  M. D’Esposito,et al.  The neural basis of the central executive system of working memory , 1995, Nature.

[19]  Kimron Shapiro,et al.  Attentional blink , 2009, Scholarpedia.

[20]  Arthur F. Kramer,et al.  Assessing the development of automatic processing: An application of dual-task and event-related brain potential methodologies , 1988, Biological Psychology.

[21]  Shin Ishii,et al.  Hierarchical Rule Switching in Prefrontal Cortex , 2022 .

[22]  Paolo Maria Rossini,et al.  Naming facilitation induced by transcranial direct current stimulation , 2010, Behavioural Brain Research.

[23]  Arthur F Kramer,et al.  Training effects on dual-task performance: are there age-related differences in plasticity of attentional control? , 2005, Psychology and aging.

[24]  Paige E. Scalf,et al.  Training-induced functional activation changes in dual-task processing: an FMRI study. , 2006, Cerebral cortex.

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

[26]  K. A. Hadland,et al.  The Effect of Cingulate Cortex Lesions on Task Switching and Working Memory , 2003, Journal of Cognitive Neuroscience.

[27]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[28]  J. Rothwell,et al.  Level of action of cathodal DC polarisation induced inhibition of the human motor cortex , 2003, Clinical Neurophysiology.

[29]  Richard S. J. Frackowiak,et al.  How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? , 2005, The European journal of neuroscience.

[30]  Jacob Cohen,et al.  A power primer. , 1992, Psychological bulletin.

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

[32]  Christopher L. Asplund,et al.  Isolation of a Central Bottleneck of Information Processing with Time-Resolved fMRI , 2006, Neuron.

[33]  A. Luxen,et al.  Involvement of both prefrontal and inferior parietal cortex in dual-task performance. , 2005, Brain research. Cognitive brain research.

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

[35]  C. Summerfield,et al.  Two Mechanisms for Task Switching in the Prefrontal Cortex , 2009, The Journal of Neuroscience.

[36]  Kathy A. Low,et al.  Share or compete? Load-dependent recruitment of prefrontal cortex during dual-task performance. , 2009, Psychophysiology.

[37]  Jason B. Mattingley,et al.  Improved multitasking following prefrontal tDCS , 2013, Cortex.

[38]  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.

[39]  G. Mangun,et al.  Effects of practice on executive control investigated with fMRI. , 2002, Brain research. Cognitive brain research.

[40]  J D Gabrieli,et al.  A resource model of the neural basis of executive working memory. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  R. E. Passingham,et al.  Interference with Performance of a Response Selection Task that has no Working Memory Component: An rTMS Comparison of the Dorsolateral Prefrontal and Medial Frontal Cortex , 2001, Journal of Cognitive Neuroscience.

[42]  R Andy McKinley,et al.  Acceleration of image analyst training with transcranial direct current stimulation. , 2013, Behavioral neuroscience.

[43]  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.

[44]  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.

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

[46]  Theodore P. Zanto,et al.  Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory , 2011, Nature Neuroscience.

[47]  A. Tachibana,et al.  Activation of dorsolateral prefrontal cortex in a dual neuropsychological screening test: An fMRI approach , 2012, Behavioral and Brain Functions.

[48]  R. Marois,et al.  Capacity limits of information processing in the brain , 2005, Trends in Cognitive Sciences.

[49]  J. Rothwell,et al.  Speech Facilitation by Left Inferior Frontal Cortex Stimulation , 2011, Current Biology.

[50]  M. Nitsche,et al.  Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans , 2001, Neurology.

[51]  Felipe M. Ortuño,et al.  Sustained attention in a counting task: Normal performance and functional neuroanatomy , 2001, NeuroImage.

[52]  A. Javadi,et al.  Transcranial Direct Current Stimulation (tDCS) Enhances Reconsolidation of Long-Term Memory , 2013, Brain Stimulation.

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

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

[55]  D. V. von Cramon,et al.  Localization of Executive Functions in Dual-Task Performance with fMRI , 2002, Journal of Cognitive Neuroscience.

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

[57]  A. Priori,et al.  Non‐synaptic mechanisms underlie the after‐effects of cathodal transcutaneous direct current stimulation of the human brain , 2005, The Journal of physiology.

[58]  John F. Larish,et al.  Training for attentional control in dual task settings: A comparison of young and old adults , 1995 .

[59]  Mark D'Esposito,et al.  A functional MRI study of the influence of practice on component processes of working memory , 2004, NeuroImage.

[60]  Mariko Osaka,et al.  Cooperation of the anterior cingulate cortex and dorsolateral prefrontal cortex for attention shifting , 2004, NeuroImage.