Transcranial direct current stimulation of dorsolateral prefrontal cortex during encoding improves recall but not recognition memory

Leshikar, Eric D.; Leach, Ryan C.; McCurdy, Matthew P.; Trumbo, Michael Christopher Stefan; Sklenar, Allison M.; Frankenstein, Andrea N.; Matzen, Laura E.

doi:10.1016/j.neuropsychologia.2017.10.022

Transcranial direct current stimulation of dorsolateral prefrontal cortex during encoding improves recall but not recognition memory

Journal Article · Thu Oct 19 00:00:00 EDT 2017 · Neuropsychologia

DOI:https://doi.org/10.1016/j.neuropsychologia.2017.10.022· OSTI ID:1421859

Leshikar, Eric D. ^[1]; Leach, Ryan C. ^[1]; McCurdy, Matthew P. ^[1]; Trumbo, Michael Christopher Stefan ^[2]; Sklenar, Allison M. ^[1]; Frankenstein, Andrea N. ^[1]; Matzen, Laura E. ^[2]

Univ. of Illinois at Chicago, Chicago, IL (United States)
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)

Prior work demonstrates that application of transcranial direct current stimulation (tDCS) improves memory. In this study, we investigated tDCS effects on face-name associative memory using both recall and recognition tests. Participants encoded face-name pairs under either active (1.5 mA) or sham (.1 mA) stimulation applied to the scalp adjacent to the left dorsolateral prefrontal cortex (dlPFC), an area known to support associative memory. Participants’ memory was then tested after study (day one) and then again after a 24-h delay (day two), to assess both immediate and delayed stimulation effects on memory. Results indicated that active relative to sham stimulation led to substantially improved recall (more than 50%) at both day one and day two. Recognition memory performance did not differ between stimulation groups at either time point. These results suggest that stimulation at encoding improves memory performance by enhancing memory for details that enable a rich recollective experience, but that these improvements are evident only under some testing conditions, especially those that rely on recollection. Altogether, stimulation of the dlPFC could have led to recall improvement through enhanced encoding from stimulation or from carryover effects of stimulation that influenced retrieval processes, or both.

View Accepted Manuscript (DOE)

Research Organization:: Sandia National Laboratories (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: NIH; USDOE

Grant/Contract Number:: AC04-94AL85000

OSTI ID:: 1421859

Alternate ID(s):: OSTI ID: 1549355

Report Number(s):: SAND--2017-13369J; 659419

Journal Information:: Neuropsychologia, Journal Name: Neuropsychologia Journal Issue: C Vol. 106; ISSN 0028-3932

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (66)

Neuroenhancement of the aging brain: Restoring skill acquisition in old subjects Zimerman, Máximo; Nitsch, Marie; Giraux, Pascal Annals of Neurology, Vol. 73, Issue 1 https://doi.org/10.1002/ana.23761	journal	December 2012
Effects of transcranial direct current stimulation in combination with motor practice on dexterous grasping and manipulation in healthy older adults Parikh, Pranav J.; Cole, Kelly J. Physiological Reports, Vol. 2, Issue 3 https://doi.org/10.1002/phy2.255	journal	March 2014
The Nature of Recollection and Familiarity: A Review of 30 Years of Research Yonelinas, Andrew P. Journal of Memory and Language, Vol. 46, Issue 3 https://doi.org/10.1006/jmla.2002.2864	journal	April 2002
Enhanced long-term memory encoding after parietal neurostimulation Jones, Kevin T.; Gözenman, Filiz; Berryhill, Marian E. Experimental Brain Research, Vol. 232, Issue 12 https://doi.org/10.1007/s00221-014-4090-y	journal	September 2014
Optimizing Transcranial Direct Current Stimulation Protocols to Promote Long-Term Learning Au, Jacky; Karsten, Carley; Buschkuehl, Martin Journal of Cognitive Enhancement, Vol. 1, Issue 1 https://doi.org/10.1007/s41465-017-0007-6	journal	January 2017
Putting names to faces: Sperling, Reisa; Chua, Elizabeth; Cocchiarella, Andrew NeuroImage, Vol. 20, Issue 2 https://doi.org/10.1016/S1053-8119(03)00391-4	journal	October 2003
Level of action of cathodal DC polarisation induced inhibition of the human motor cortex Nitsche, Michael A.; Nitsche, Maren S.; Klein, Cornelia C. Clinical Neurophysiology, Vol. 114, Issue 4 https://doi.org/10.1016/S1388-2457(02)00412-1	journal	April 2003
Transcranial direct current stimulation over the parietal cortex alters bias in item and source memory tasks Pergolizzi, Denise; Chua, Elizabeth F. Brain and Cognition, Vol. 108 https://doi.org/10.1016/j.bandc.2016.06.009	journal	October 2016
Visual memory improved by non-invasive brain stimulation Chi, Richard P.; Fregni, Felipe; Snyder, Allan W. Brain Research, Vol. 1353 https://doi.org/10.1016/j.brainres.2010.07.062	journal	September 2010
Oppositional transcranial direct current stimulation (tDCS) of parietal substrates of attention during encoding modulates episodic memory Jacobson, Liron; Goren, Nir; Lavidor, Michal Brain Research, Vol. 1439 https://doi.org/10.1016/j.brainres.2011.12.036	journal	February 2012
Baseline effects of transcranial direct current stimulation on glutamatergic neurotransmission and large-scale network connectivity Hunter, Michael A.; Coffman, Brian A.; Gasparovic, Charles Brain Research, Vol. 1594 https://doi.org/10.1016/j.brainres.2014.09.066	journal	January 2015
Effects of non-invasive brain stimulation on associative memory Matzen, Laura E.; Trumbo, Michael C.; Leach, Ryan C. Brain Research, Vol. 1624 https://doi.org/10.1016/j.brainres.2015.07.036	journal	October 2015
Transcranial direct current stimulation (tDCS) of the left dorsolateral prefrontal cortex modulates declarative memory Javadi, Amir Homayoun; Walsh, Vincent Brain Stimulation, Vol. 5, Issue 3 https://doi.org/10.1016/j.brs.2011.06.007	journal	July 2012
Short duration transcranial direct current stimulation (tDCS) modulates verbal memory Javadi, Amir Homayoun; Cheng, Paul; Walsh, Vincent Brain Stimulation, Vol. 5, Issue 4 https://doi.org/10.1016/j.brs.2011.08.003	journal	October 2012
Transcranial Direct Current Stimulation Modulates Activation and Effective Connectivity During Spatial Navigation Hampstead, Benjamin M.; Brown, Gregory S.; Hartley, Justin F. Brain Stimulation, Vol. 7, Issue 2 https://doi.org/10.1016/j.brs.2013.12.006	journal	March 2014
Perception of comfort during transcranial DC stimulation: Effect of NaCl solution concentration applied to sponge electrodes Dundas, J. E.; Thickbroom, G. W.; Mastaglia, F. L. Clinical Neurophysiology, Vol. 118, Issue 5 https://doi.org/10.1016/j.clinph.2007.01.010	journal	May 2007
What does the ratio of injected current to electrode area tell us about current density in the brain during tDCS? Miranda, Pedro Cavaleiro; Faria, Paula; Hallett, Mark Clinical Neurophysiology, Vol. 120, Issue 6 https://doi.org/10.1016/j.clinph.2009.03.023	journal	June 2009
Effect of prefrontal and parietal tDCS on learning and recognition of verbal and non-verbal material Manuel, Aurélie L.; Schnider, Armin Clinical Neurophysiology, Vol. 127, Issue 7 https://doi.org/10.1016/j.clinph.2016.04.015	journal	July 2016
Electrically stimulating prefrontal cortex at retrieval improves recollection accuracy Gray, Stephen J.; Brookshire, Geoffrey; Casasanto, Daniel Cortex, Vol. 73 https://doi.org/10.1016/j.cortex.2015.09.003	journal	December 2015
Similarity to the self affects memory for impressions of others Leshikar, Eric D.; Gutchess, Angela H. Journal of Applied Research in Memory and Cognition, Vol. 4, Issue 1 https://doi.org/10.1016/j.jarmac.2014.10.002	journal	March 2015
The generation effect revisited: Fewer generation constraints enhances item and context memory McCurdy, Matthew P.; Leach, Ryan C.; Leshikar, Eric D. Journal of Memory and Language, Vol. 92 https://doi.org/10.1016/j.jml.2016.06.007	journal	February 2017
Transcranial direct current stimulation (tDCS) produces localized and specific alterations in neurochemistry: A 1H magnetic resonance spectroscopy study Clark, Vincent P.; Coffman, Brian A.; Trumbo, Michael C. Neuroscience Letters, Vol. 500, Issue 1 https://doi.org/10.1016/j.neulet.2011.05.244	journal	August 2011
Non-invasive brain stimulation improves object-location learning in the elderly Flöel, Agnes; Suttorp, Wiebke; Kohl, Oliver Neurobiology of Aging, Vol. 33, Issue 8 https://doi.org/10.1016/j.neurobiolaging.2011.05.007	journal	August 2012
Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping Okamoto, Masako; Dan, Haruka; Sakamoto, Kuniko NeuroImage, Vol. 21, Issue 1 https://doi.org/10.1016/j.neuroimage.2003.08.026	journal	January 2004
Battery powered thought: Enhancement of attention, learning, and memory in healthy adults using transcranial direct current stimulation Coffman, Brian A.; Clark, Vincent P.; Parasuraman, Raja NeuroImage, Vol. 85 https://doi.org/10.1016/j.neuroimage.2013.07.083	journal	January 2014
Revealing the brain's adaptability and the transcranial direct current stimulation facilitating effect in inhibitory control by multiscale entropy Liang, Wei-Kuang; Lo, Men-Tzung; Yang, Albert C. NeuroImage, Vol. 90 https://doi.org/10.1016/j.neuroimage.2013.12.048	journal	April 2014
Focalised stimulation using high definition transcranial direct current stimulation (HD-tDCS) to investigate declarative verbal learning and memory functioning Nikolin, Stevan; Loo, Colleen K.; Bai, Siwei NeuroImage, Vol. 117 https://doi.org/10.1016/j.neuroimage.2015.05.019	journal	August 2015
Source memory performance is modulated by transcranial direct current stimulation over the left posterior parietal cortex Chen, Nai-Feng; Lo, Chien-Ming; Liu, Tzu-Ling NeuroImage, Vol. 139 https://doi.org/10.1016/j.neuroimage.2016.06.032	journal	October 2016
Transcranial direct current stimulation (tDCS) of the parietal cortex leads to increased false recognition Pergolizzi, Denise; Chua, Elizabeth F. Neuropsychologia, Vol. 66 https://doi.org/10.1016/j.neuropsychologia.2014.11.012	journal	January 2015
Guess who? Investigating the proper name processing network by means of tDCS Pisoni, Alberto; Vernice, Mirta; Iasevoli, Luigi Neuropsychologia, Vol. 66 https://doi.org/10.1016/j.neuropsychologia.2014.11.025	journal	January 2015
Transcranial direct current stimulation in the treatment of major depression: a meta-analysis Kalu, U. G.; Sexton, C. E.; Loo, C. K. Psychological Medicine, Vol. 42, Issue 9 https://doi.org/10.1017/S0033291711003059	journal	January 2012
Pragmatics of measuring recognition memory: Applications to dementia and amnesia. Snodgrass, Joan G.; Corwin, June Journal of Experimental Psychology: General, Vol. 117, Issue 1 https://doi.org/10.1037/0096-3445.117.1.34	journal	January 1988
Strengthening of horizontal cortical connections following skill learning Rioult-Pedotti, Mengia -S.; Friedman, Daniel; Hess, Grzegorz Nature Neuroscience, Vol. 1, Issue 3 https://doi.org/10.1038/678	journal	July 1998
Mechanisms of Action Underlying the Effect of Repetitive Transcranial Magnetic Stimulation on Mood: Behavioral and Brain Imaging Studies Barrett, Jennifer; Della-Maggiore, Valeria; Chouinard, Philippe A. Neuropsychopharmacology, Vol. 29, Issue 6 https://doi.org/10.1038/sj.npp.1300411	journal	March 2004
Consolidation of Human Motor Cortical Neuroplasticity by D-Cycloserine Nitsche, Michael A.; Jaussi, Wiebke; Liebetanz, David Neuropsychopharmacology, Vol. 29, Issue 8 https://doi.org/10.1038/sj.npp.1300517	journal	June 2004
Self-referencing enhances recollection in both young and older adults Leshikar, Eric D.; Dulas, Michael R.; Duarte, Audrey Aging, Neuropsychology, and Cognition, Vol. 22, Issue 4 https://doi.org/10.1080/13825585.2014.957150	journal	September 2014
Recollection Training and Transfer Effects in Older Adults: Successful Use of a Repetition-Lag Procedure Jennings, Janine M.; Webster, Lauren M.; Kleykamp, Bethea A. Aging, Neuropsychology, and Cognition, Vol. 12, Issue 3 https://doi.org/10.1080/138255890968312	journal	September 2005
Medial prefrontal cortex supports source memory accuracy for self-referenced items Leshikar, Eric D.; Duarte, Audrey Social Neuroscience, Vol. 7, Issue 2 https://doi.org/10.1080/17470919.2011.585242	journal	March 2012
Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability Liebetanz, D. Brain, Vol. 125, Issue 10 https://doi.org/10.1093/brain/awf238	journal	October 2002
Long-term effects of transcranial direct current stimulation combined with computer-assisted cognitive training in healthy older adults Park, See-Hyun; Seo, Jeong-Hwan; Kim, Yun-Hee NeuroReport, Vol. 25, Issue 2 https://doi.org/10.1097/WNR.0000000000000080	journal	January 2014
Time-dependent effect of transcranial direct current stimulation on the enhancement of working memory Ohn, Suk Hoon; Park, Chang-Il; Yoo, Woo-Kyoung NeuroReport, Vol. 19, Issue 1 https://doi.org/10.1097/WNR.0b013e3282f2adfd	journal	January 2008
Test-Enhanced Learning: Taking Memory Tests Improves Long-Term Retention Roediger, Henry L.; Karpicke, Jeffrey D. Psychological Science, Vol. 17, Issue 3 https://doi.org/10.1111/j.1467-9280.2006.01693.x	journal	March 2006
Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation Nitsche, M. A.; Paulus, W. The Journal of Physiology, Vol. 527, Issue 3 https://doi.org/10.1111/j.1469-7793.2000.t01-1-00633.x	journal	September 2000
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 Bindman, Lynn J.; Lippold, O. C. J.; Redfearn, J. W. T. The Journal of Physiology, Vol. 172, Issue 3 https://doi.org/10.1113/jphysiol.1964.sp007425	journal	August 1964
Pharmacological Modulation of Cortical Excitability Shifts Induced by Transcranial Direct Current Stimulation in Humans Nitsche, M. A.; Fricke, K.; Henschke, U. The Journal of Physiology, Vol. 553, Issue 1 https://doi.org/10.1113/jphysiol.2003.049916	journal	November 2003
Rapid Modulation of GABA Concentration in Human Sensorimotor Cortex During Motor Learning Floyer-Lea, Anna; Wylezinska, Marzena; Kincses, Tamas Journal of Neurophysiology, Vol. 95, Issue 3 https://doi.org/10.1152/jn.00346.2005	journal	March 2006
Noninvasive Brain Stimulation Improves Language Learning Flöel, Agnes; Rösser, Nina; Michka, Olesya Journal of Cognitive Neuroscience, Vol. 20, Issue 8 https://doi.org/10.1162/jocn.2008.20098	journal	August 2008
Putting the Pieces Together: The Role of Dorsolateral Prefrontal Cortex in Relational Memory Encoding Blumenfeld, Robert S.; Parks, Colleen M.; Yonelinas, Andrew P. Journal of Cognitive Neuroscience, Vol. 23, Issue 1 https://doi.org/10.1162/jocn.2010.21459	journal	January 2011
Binding Items and Contexts: The Cognitive Neuroscience of Episodic Memory Ranganath, Charan Current Directions in Psychological Science, Vol. 19, Issue 3 https://doi.org/10.1177/0963721410368805	journal	June 2010
Physiological Basis of Transcranial Direct Current Stimulation Stagg, Charlotte J.; Nitsche, Michael A. The Neuroscientist, Vol. 17, Issue 1 https://doi.org/10.1177/1073858410386614	journal	February 2011
Errorless and errorful learning modulated by transcranial direct current stimulation Hammer, Anke; Mohammadi, Bahram; Schmicker, Marlen BMC Neuroscience, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2202-12-72	journal	January 2011
Direct current induced short-term modulation of the left dorsolateral prefrontal cortex while learning auditory presented nouns Elmer, Stefan; Burkard, Marcel; Renz, Basil Behavioral and Brain Functions, Vol. 5, Issue 1 https://doi.org/10.1186/1744-9081-5-29	journal	January 2009
Temporal Lobe Cortical Electrical Stimulation during the Encoding and Retrieval Phase Reduces False Memories Boggio, Paulo S.; Fregni, Felipe; Valasek, Claudia PLoS ONE, Vol. 4, Issue 3 https://doi.org/10.1371/journal.pone.0004959	journal	March 2009
Effects of Transcranial Direct Current Stimulation on Episodic Memory Related to Emotional Visual Stimuli Penolazzi, Barbara; Di Domenico, Alberto; Marzoli, Daniele PLoS ONE, Vol. 5, Issue 5 https://doi.org/10.1371/journal.pone.0010623	journal	May 2010
Task-Selective Memory Effects for Successfully Implemented Encoding Strategies Leshikar, Eric D.; Duarte, Audrey; Hertzog, Christopher PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0038160	journal	May 2012
Separating Recognition Processes of Declarative Memory via Anodal tDCS: Boosting Old Item Recognition by Temporal and New Item Detection by Parietal Stimulation Pisoni, Alberto; Turi, Zsolt; Raithel, Almuth PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0123085	journal	March 2015
Effects of Unilateral Transcranial Direct Current Stimulation of Left Prefrontal Cortex on Processing and Memory of Emotional Visual Stimuli Balzarotti, Stefania; Colombo, Barbara PLOS ONE, Vol. 11, Issue 7 https://doi.org/10.1371/journal.pone.0159555	journal	July 2016
Unleashing Potential: Transcranial Direct Current Stimulation over the Right Posterior Parietal Cortex Improves Change Detection in Low-Performing Individuals Tseng, P.; Hsu, T. -Y.; Chang, C. -F. Journal of Neuroscience, Vol. 32, Issue 31 https://doi.org/10.1523/JNEUROSCI.0362-12.2012	journal	August 2012
The Dorsolateral Prefrontal Cortex Contributes to Successful Relational Memory Encoding Murray, L. J.; Ranganath, C. Journal of Neuroscience, Vol. 27, Issue 20 https://doi.org/10.1523/JNEUROSCI.0406-07.2007	journal	May 2007
Transcranial Direct Current Stimulation during Sleep Improves Declarative Memory Marshall, L. Journal of Neuroscience, Vol. 24, Issue 44 https://doi.org/10.1523/JNEUROSCI.2725-04.2004	journal	November 2004
Polarity-Sensitive Modulation of Cortical Neurotransmitters by Transcranial Stimulation Stagg, C. J.; Best, J. G.; Stephenson, M. C. Journal of Neuroscience, Vol. 29, Issue 16 https://doi.org/10.1523/JNEUROSCI.4432-08.2009	journal	April 2009
Shaping Memory Accuracy by Left Prefrontal Transcranial Direct Current Stimulation Zwissler, B.; Sperber, C.; Aigeldinger, S. Journal of Neuroscience, Vol. 34, Issue 11 https://doi.org/10.1523/JNEUROSCI.5407-13.2014	journal	March 2014
Anodal Transcranial Direct Current Stimulation Temporarily Reverses Age-Associated Cognitive Decline and Functional Brain Activity Changes Meinzer, M.; Lindenberg, R.; Antonenko, D. Journal of Neuroscience, Vol. 33, Issue 30 https://doi.org/10.1523/JNEUROSCI.5743-12.2013	journal	July 2013
Recognition memory for faces: When familiarity supports associative recognition judgments Yonelinas, A. P.; Kroll, N. E. A.; Dobbins, I. G. Psychonomic Bulletin & Review, Vol. 6, Issue 4 https://doi.org/10.3758/BF03212975	journal	December 1999
FACES—A database of facial expressions in young, middle-aged, and older women and men: Development and validation Ebner, Natalie C.; Riediger, Michaela; Lindenberger, Ulman Behavior Research Methods, Vol. 42, Issue 1 https://doi.org/10.3758/BRM.42.1.351	journal	February 2010
Medial prefrontal cortex supports source memory for self-referenced materials in young and older adults Leshikar, Eric D.; Duarte, Audrey Cognitive, Affective, & Behavioral Neuroscience, Vol. 14, Issue 1 https://doi.org/10.3758/s13415-013-0198-y	journal	August 2013

Cited By (4)

Systematic Review and Network Meta-Analysis of Anodal tDCS Effects on Verbal Episodic Memory: Modeling Heterogeneity of Stimulation Locations Bartl, Gergely Janos; Blackshaw, Emily; Crossman, Margot Zeitschrift für Psychologie, Vol. 228, Issue 1 https://doi.org/10.1027/2151-2604/a000396	journal	March 2020
Neurophysiological characteristics of acts of remembering in the process of positive ageing / Características neurofisiológicas de los actos de recuerdo en el proceso de envejecimiento positivo Tenorio, Marcela; Aparicio, Andrés Estudios de Psicología, Vol. 39, Issue 2-3 https://doi.org/10.1080/02109395.2018.1518680	journal	August 2018
Differential Age Effects of Transcranial Direct Current Stimulation on Associative Memory Leach, Ryan C.; McCurdy, Matthew P.; Trumbo, Michael C. The Journals of Gerontology: Series B, Vol. 74, Issue 7 https://doi.org/10.1093/geronb/gby003	journal	February 2018
Boosting Memory by tDCS to Frontal or Parietal Brain Regions? A Study of the Enactment Effect Shows No Effects for Immediate and Delayed Recognition Meier, Beat; Sauter, Philipp Frontiers in Psychology, Vol. 9 https://doi.org/10.3389/fpsyg.2018.00867	journal	June 2018

Similar Records

Differential Age Effects of Transcranial Direct Current Stimulation on Associative Memory

Journal Article · Wed Jan 31 23:00:00 EST 2018 · The Journals of Gerontology. Series B, Psychological Sciences and Social Sciences · OSTI ID:1562341

Enhanced working memory performance via transcranial direct current stimulation: The possibility of near and far transfer

Journal Article · Sat Oct 15 00:00:00 EDT 2016 · Neuropsychologia · OSTI ID:1335002

Effects of non-invasive brain stimulation on associative memory

Journal Article · Thu Jul 30 00:00:00 EDT 2015 · Brain Research · OSTI ID:1339280

Related Subjects

60 APPLIED LIFE SCIENCES
Associative memory
Brain stimulation
Delayed effects of tDCS
Episodic memory
Immediate effects of tDCS
Recall
Recognition
dlPFC
tDCS

Transcranial direct current stimulation of dorsolateral prefrontal cortex during encoding improves recall but not recognition memory

Citation Formats

References (66)

Cited By (4)

Similar Records

Related Subjects