Transcranial direct current stimulation of dorsolateral prefrontal cortex during encoding improves recall but not recognition memory
Abstract
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.
- Authors:
-
- Univ. of Illinois at Chicago, Chicago, IL (United States)
- Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
- Publication Date:
- Research Org.:
- Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
- Sponsoring Org.:
- National Institutes of Health (NIH); USDOE National Nuclear Security Administration (NNSA)
- OSTI Identifier:
- 1421859
- Alternate Identifier(s):
- OSTI ID: 1549355
- Report Number(s):
- SAND-2017-13369J
Journal ID: ISSN 0028-3932; 659419
- Grant/Contract Number:
- AC04-94AL85000; NA0003525
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Neuropsychologia
- Additional Journal Information:
- Journal Volume: 106; Journal Issue: C; Journal ID: ISSN 0028-3932
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; Brain stimulation; tDCS; dlPFC; Immediate effects of tDCS; Delayed effects of tDCS; Associative memory; Recall; Recognition; Episodic memory
Citation Formats
Leshikar, Eric D., Leach, Ryan C., McCurdy, Matthew P., Trumbo, Michael Christopher Stefan, Sklenar, Allison M., Frankenstein, Andrea N., and Matzen, Laura E. Transcranial direct current stimulation of dorsolateral prefrontal cortex during encoding improves recall but not recognition memory. United States: N. p., 2017.
Web. doi:10.1016/j.neuropsychologia.2017.10.022.
Leshikar, Eric D., Leach, Ryan C., McCurdy, Matthew P., Trumbo, Michael Christopher Stefan, Sklenar, Allison M., Frankenstein, Andrea N., & Matzen, Laura E. Transcranial direct current stimulation of dorsolateral prefrontal cortex during encoding improves recall but not recognition memory. United States. https://doi.org/10.1016/j.neuropsychologia.2017.10.022
Leshikar, Eric D., Leach, Ryan C., McCurdy, Matthew P., Trumbo, Michael Christopher Stefan, Sklenar, Allison M., Frankenstein, Andrea N., and Matzen, Laura E. Thu .
"Transcranial direct current stimulation of dorsolateral prefrontal cortex during encoding improves recall but not recognition memory". United States. https://doi.org/10.1016/j.neuropsychologia.2017.10.022. https://www.osti.gov/servlets/purl/1421859.
@article{osti_1421859,
title = {Transcranial direct current stimulation of dorsolateral prefrontal cortex during encoding improves recall but not recognition memory},
author = {Leshikar, Eric D. and Leach, Ryan C. and McCurdy, Matthew P. and Trumbo, Michael Christopher Stefan and Sklenar, Allison M. and Frankenstein, Andrea N. and Matzen, Laura E.},
abstractNote = {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.},
doi = {10.1016/j.neuropsychologia.2017.10.022},
journal = {Neuropsychologia},
number = C,
volume = 106,
place = {United States},
year = {2017},
month = {10}
}
Web of Science
Works referenced in this record:
Optimizing Transcranial Direct Current Stimulation Protocols to Promote Long-Term Learning
journal, January 2017
- Au, Jacky; Karsten, Carley; Buschkuehl, Martin
- Journal of Cognitive Enhancement, Vol. 1, Issue 1
Effects of Unilateral Transcranial Direct Current Stimulation of Left Prefrontal Cortex on Processing and Memory of Emotional Visual Stimuli
journal, July 2016
- Balzarotti, Stefania; Colombo, Barbara
- PLOS ONE, Vol. 11, Issue 7
Mechanisms of Action Underlying the Effect of Repetitive Transcranial Magnetic Stimulation on Mood: Behavioral and Brain Imaging Studies
journal, March 2004
- Barrett, Jennifer; Della-Maggiore, Valeria; Chouinard, Philippe A.
- Neuropsychopharmacology, Vol. 29, Issue 6
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
journal, August 1964
- Bindman, Lynn J.; Lippold, O. C. J.; Redfearn, J. W. T.
- The Journal of Physiology, Vol. 172, Issue 3
Putting the Pieces Together: The Role of Dorsolateral Prefrontal Cortex in Relational Memory Encoding
journal, January 2011
- Blumenfeld, Robert S.; Parks, Colleen M.; Yonelinas, Andrew P.
- Journal of Cognitive Neuroscience, Vol. 23, Issue 1
Temporal Lobe Cortical Electrical Stimulation during the Encoding and Retrieval Phase Reduces False Memories
journal, March 2009
- Boggio, Paulo S.; Fregni, Felipe; Valasek, Claudia
- PLoS ONE, Vol. 4, Issue 3
Source memory performance is modulated by transcranial direct current stimulation over the left posterior parietal cortex
journal, October 2016
- Chen, Nai-Feng; Lo, Chien-Ming; Liu, Tzu-Ling
- NeuroImage, Vol. 139
Visual memory improved by non-invasive brain stimulation
journal, September 2010
- Chi, Richard P.; Fregni, Felipe; Snyder, Allan W.
- Brain Research, Vol. 1353
Transcranial direct current stimulation (tDCS) produces localized and specific alterations in neurochemistry: A 1H magnetic resonance spectroscopy study
journal, August 2011
- Clark, Vincent P.; Coffman, Brian A.; Trumbo, Michael C.
- Neuroscience Letters, Vol. 500, Issue 1
Battery powered thought: Enhancement of attention, learning, and memory in healthy adults using transcranial direct current stimulation
journal, January 2014
- Coffman, Brian A.; Clark, Vincent P.; Parasuraman, Raja
- NeuroImage, Vol. 85
Perception of comfort during transcranial DC stimulation: Effect of NaCl solution concentration applied to sponge electrodes
journal, May 2007
- Dundas, J. E.; Thickbroom, G. W.; Mastaglia, F. L.
- Clinical Neurophysiology, Vol. 118, Issue 5
FACES—A database of facial expressions in young, middle-aged, and older women and men: Development and validation
journal, February 2010
- Ebner, Natalie C.; Riediger, Michaela; Lindenberger, Ulman
- Behavior Research Methods, Vol. 42, Issue 1
Direct current induced short-term modulation of the left dorsolateral prefrontal cortex while learning auditory presented nouns
journal, January 2009
- Elmer, Stefan; Burkard, Marcel; Renz, Basil
- Behavioral and Brain Functions, Vol. 5, Issue 1
Noninvasive Brain Stimulation Improves Language Learning
journal, August 2008
- Flöel, Agnes; Rösser, Nina; Michka, Olesya
- Journal of Cognitive Neuroscience, Vol. 20, Issue 8
Non-invasive brain stimulation improves object-location learning in the elderly
journal, August 2012
- Flöel, Agnes; Suttorp, Wiebke; Kohl, Oliver
- Neurobiology of Aging, Vol. 33, Issue 8
Rapid Modulation of GABA Concentration in Human Sensorimotor Cortex During Motor Learning
journal, March 2006
- Floyer-Lea, Anna; Wylezinska, Marzena; Kincses, Tamas
- Journal of Neurophysiology, Vol. 95, Issue 3
Electrically stimulating prefrontal cortex at retrieval improves recollection accuracy
journal, December 2015
- Gray, Stephen J.; Brookshire, Geoffrey; Casasanto, Daniel
- Cortex, Vol. 73
Errorless and errorful learning modulated by transcranial direct current stimulation
journal, January 2011
- Hammer, Anke; Mohammadi, Bahram; Schmicker, Marlen
- BMC Neuroscience, Vol. 12, Issue 1
Transcranial Direct Current Stimulation Modulates Activation and Effective Connectivity During Spatial Navigation
journal, March 2014
- Hampstead, Benjamin M.; Brown, Gregory S.; Hartley, Justin F.
- Brain Stimulation, Vol. 7, Issue 2
Baseline effects of transcranial direct current stimulation on glutamatergic neurotransmission and large-scale network connectivity
journal, January 2015
- Hunter, Michael A.; Coffman, Brian A.; Gasparovic, Charles
- Brain Research, Vol. 1594
Oppositional transcranial direct current stimulation (tDCS) of parietal substrates of attention during encoding modulates episodic memory
journal, February 2012
- Jacobson, Liron; Goren, Nir; Lavidor, Michal
- Brain Research, Vol. 1439
Short duration transcranial direct current stimulation (tDCS) modulates verbal memory
journal, October 2012
- Javadi, Amir Homayoun; Cheng, Paul; Walsh, Vincent
- Brain Stimulation, Vol. 5, Issue 4
Transcranial direct current stimulation (tDCS) of the left dorsolateral prefrontal cortex modulates declarative memory
journal, July 2012
- Javadi, Amir Homayoun; Walsh, Vincent
- Brain Stimulation, Vol. 5, Issue 3
Recollection Training and Transfer Effects in Older Adults: Successful Use of a Repetition-Lag Procedure
journal, September 2005
- Jennings, Janine M.; Webster, Lauren M.; Kleykamp, Bethea A.
- Aging, Neuropsychology, and Cognition, Vol. 12, Issue 3
Enhanced long-term memory encoding after parietal neurostimulation
journal, September 2014
- Jones, Kevin T.; Gözenman, Filiz; Berryhill, Marian E.
- Experimental Brain Research, Vol. 232, Issue 12
Transcranial direct current stimulation in the treatment of major depression: a meta-analysis
journal, January 2012
- Kalu, U. G.; Sexton, C. E.; Loo, C. K.
- Psychological Medicine, Vol. 42, Issue 9
Medial prefrontal cortex supports source memory accuracy for self-referenced items
journal, March 2012
- Leshikar, Eric D.; Duarte, Audrey
- Social Neuroscience, Vol. 7, Issue 2
Medial prefrontal cortex supports source memory for self-referenced materials in young and older adults
journal, August 2013
- Leshikar, Eric D.; Duarte, Audrey
- Cognitive, Affective, & Behavioral Neuroscience, Vol. 14, Issue 1
Task-Selective Memory Effects for Successfully Implemented Encoding Strategies
journal, May 2012
- Leshikar, Eric D.; Duarte, Audrey; Hertzog, Christopher
- PLoS ONE, Vol. 7, Issue 5
Self-referencing enhances recollection in both young and older adults
journal, September 2014
- Leshikar, Eric D.; Dulas, Michael R.; Duarte, Audrey
- Aging, Neuropsychology, and Cognition, Vol. 22, Issue 4
Similarity to the self affects memory for impressions of others
journal, March 2015
- Leshikar, Eric D.; Gutchess, Angela H.
- Journal of Applied Research in Memory and Cognition, Vol. 4, Issue 1
Revealing the brain's adaptability and the transcranial direct current stimulation facilitating effect in inhibitory control by multiscale entropy
journal, April 2014
- Liang, Wei-Kuang; Lo, Men-Tzung; Yang, Albert C.
- NeuroImage, Vol. 90
Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability
journal, October 2002
- Liebetanz, D.
- Brain, Vol. 125, Issue 10
Effect of prefrontal and parietal tDCS on learning and recognition of verbal and non-verbal material
journal, July 2016
- Manuel, Aurélie L.; Schnider, Armin
- Clinical Neurophysiology, Vol. 127, Issue 7
Transcranial Direct Current Stimulation during Sleep Improves Declarative Memory
journal, November 2004
- Marshall, L.
- Journal of Neuroscience, Vol. 24, Issue 44
Effects of non-invasive brain stimulation on associative memory
journal, October 2015
- Matzen, Laura E.; Trumbo, Michael C.; Leach, Ryan C.
- Brain Research, Vol. 1624
The generation effect revisited: Fewer generation constraints enhances item and context memory
journal, February 2017
- McCurdy, Matthew P.; Leach, Ryan C.; Leshikar, Eric D.
- Journal of Memory and Language, Vol. 92
Anodal Transcranial Direct Current Stimulation Temporarily Reverses Age-Associated Cognitive Decline and Functional Brain Activity Changes
journal, July 2013
- Meinzer, M.; Lindenberg, R.; Antonenko, D.
- Journal of Neuroscience, Vol. 33, Issue 30
What does the ratio of injected current to electrode area tell us about current density in the brain during tDCS?
journal, June 2009
- Miranda, Pedro Cavaleiro; Faria, Paula; Hallett, Mark
- Clinical Neurophysiology, Vol. 120, Issue 6
The Dorsolateral Prefrontal Cortex Contributes to Successful Relational Memory Encoding
journal, May 2007
- Murray, L. J.; Ranganath, C.
- Journal of Neuroscience, Vol. 27, Issue 20
Focalised stimulation using high definition transcranial direct current stimulation (HD-tDCS) to investigate declarative verbal learning and memory functioning
journal, August 2015
- Nikolin, Stevan; Loo, Colleen K.; Bai, Siwei
- NeuroImage, Vol. 117
Pharmacological Modulation of Cortical Excitability Shifts Induced by Transcranial Direct Current Stimulation in Humans
journal, November 2003
- Nitsche, M. A.; Fricke, K.; Henschke, U.
- The Journal of Physiology, Vol. 553, Issue 1
Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation
journal, September 2000
- Nitsche, M. A.; Paulus, W.
- The Journal of Physiology, Vol. 527, Issue 3
Consolidation of Human Motor Cortical Neuroplasticity by D-Cycloserine
journal, June 2004
- Nitsche, Michael A.; Jaussi, Wiebke; Liebetanz, David
- Neuropsychopharmacology, Vol. 29, Issue 8
Level of action of cathodal DC polarisation induced inhibition of the human motor cortex
journal, April 2003
- Nitsche, Michael A.; Nitsche, Maren S.; Klein, Cornelia C.
- Clinical Neurophysiology, Vol. 114, Issue 4
Time-dependent effect of transcranial direct current stimulation on the enhancement of working memory
journal, January 2008
- Ohn, Suk Hoon; Park, Chang-Il; Yoo, Woo-Kyoung
- NeuroReport, Vol. 19, Issue 1
Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping
journal, January 2004
- Okamoto, Masako; Dan, Haruka; Sakamoto, Kuniko
- NeuroImage, Vol. 21, Issue 1
Effects of transcranial direct current stimulation in combination with motor practice on dexterous grasping and manipulation in healthy older adults
journal, March 2014
- Parikh, Pranav J.; Cole, Kelly J.
- Physiological Reports, Vol. 2, Issue 3
Effects of Transcranial Direct Current Stimulation on Episodic Memory Related to Emotional Visual Stimuli
journal, May 2010
- Penolazzi, Barbara; Di Domenico, Alberto; Marzoli, Daniele
- PLoS ONE, Vol. 5, Issue 5
Transcranial direct current stimulation (tDCS) of the parietal cortex leads to increased false recognition
journal, January 2015
- Pergolizzi, Denise; Chua, Elizabeth F.
- Neuropsychologia, Vol. 66
Transcranial direct current stimulation over the parietal cortex alters bias in item and source memory tasks
journal, October 2016
- Pergolizzi, Denise; Chua, Elizabeth F.
- Brain and Cognition, Vol. 108
Separating Recognition Processes of Declarative Memory via Anodal tDCS: Boosting Old Item Recognition by Temporal and New Item Detection by Parietal Stimulation
journal, March 2015
- Pisoni, Alberto; Turi, Zsolt; Raithel, Almuth
- PLOS ONE, Vol. 10, Issue 3
Guess who? Investigating the proper name processing network by means of tDCS
journal, January 2015
- Pisoni, Alberto; Vernice, Mirta; Iasevoli, Luigi
- Neuropsychologia, Vol. 66
Binding Items and Contexts: The Cognitive Neuroscience of Episodic Memory
journal, June 2010
- Ranganath, Charan
- Current Directions in Psychological Science, Vol. 19, Issue 3
Strengthening of horizontal cortical connections following skill learning
journal, July 1998
- Rioult-Pedotti, Mengia -S.; Friedman, Daniel; Hess, Grzegorz
- Nature Neuroscience, Vol. 1, Issue 3
Test-Enhanced Learning: Taking Memory Tests Improves Long-Term Retention
journal, March 2006
- Roediger, Henry L.; Karpicke, Jeffrey D.
- Psychological Science, Vol. 17, Issue 3
Pragmatics of measuring recognition memory: Applications to dementia and amnesia.
journal, January 1988
- Snodgrass, Joan G.; Corwin, June
- Journal of Experimental Psychology: General, Vol. 117, Issue 1
Putting names to faces:
journal, October 2003
- Sperling, Reisa; Chua, Elizabeth; Cocchiarella, Andrew
- NeuroImage, Vol. 20, Issue 2
Polarity-Sensitive Modulation of Cortical Neurotransmitters by Transcranial Stimulation
journal, April 2009
- Stagg, C. J.; Best, J. G.; Stephenson, M. C.
- Journal of Neuroscience, Vol. 29, Issue 16
Physiological Basis of Transcranial Direct Current Stimulation
journal, February 2011
- Stagg, Charlotte J.; Nitsche, Michael A.
- The Neuroscientist, Vol. 17, Issue 1
Unleashing Potential: Transcranial Direct Current Stimulation over the Right Posterior Parietal Cortex Improves Change Detection in Low-Performing Individuals
journal, August 2012
- Tseng, P.; Hsu, T. -Y.; Chang, C. -F.
- Journal of Neuroscience, Vol. 32, Issue 31
Recognition memory for faces: When familiarity supports associative recognition judgments
journal, December 1999
- Yonelinas, A. P.; Kroll, N. E. A.; Dobbins, I. G.
- Psychonomic Bulletin & Review, Vol. 6, Issue 4
The Nature of Recollection and Familiarity: A Review of 30 Years of Research
journal, April 2002
- Yonelinas, Andrew P.
- Journal of Memory and Language, Vol. 46, Issue 3
Neuroenhancement of the aging brain: Restoring skill acquisition in old subjects
journal, December 2012
- Zimerman, Máximo; Nitsch, Marie; Giraux, Pascal
- Annals of Neurology, Vol. 73, Issue 1
Shaping Memory Accuracy by Left Prefrontal Transcranial Direct Current Stimulation
journal, March 2014
- Zwissler, B.; Sperber, C.; Aigeldinger, S.
- Journal of Neuroscience, Vol. 34, Issue 11
Works referencing / citing this record:
Systematic Review and Network Meta-Analysis of Anodal tDCS Effects on Verbal Episodic Memory: Modeling Heterogeneity of Stimulation Locations
journal, March 2020
- Bartl, Gergely Janos; Blackshaw, Emily; Crossman, Margot
- Zeitschrift für Psychologie, Vol. 228, Issue 1
Differential Age Effects of Transcranial Direct Current Stimulation on Associative Memory
journal, February 2018
- Leach, Ryan C.; McCurdy, Matthew P.; Trumbo, Michael C.
- The Journals of Gerontology: Series B, Vol. 74, Issue 7
Boosting Memory by tDCS to Frontal or Parietal Brain Regions? A Study of the Enactment Effect Shows No Effects for Immediate and Delayed Recognition
journal, June 2018
- Meier, Beat; Sauter, Philipp
- Frontiers in Psychology, Vol. 9
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
journal, August 2018
- Tenorio, Marcela; Aparicio, Andrés
- Estudios de Psicología, Vol. 39, Issue 2-3