Theta band high definition transcranial alternating current stimulation, but not transcranial direct current stimulation, improves associative memory performance

Stefan Lang, Liu Shi Gan, Tazrina Alrazi, Oury Monchi, Stefan Lang, Liu Shi Gan, Tazrina Alrazi, Oury Monchi

Abstract

Associative memory (AM) deficits are common in neurodegenerative disease and novel therapies aimed at improving these faculties are needed. Theta band oscillations within AM networks have been shown to be important for successful memory encoding and modulating these rhythms represents a promising strategy for cognitive enhancement. Transcranial alternating current stimulation (TACS) has been hypothesized to entrain and increase power of endogenous brain rhythms. For this reason, we hypothesized that focal delivery of theta band electrical current, using high-definition TACS, would result in improved AM performance compared to sham stimulation or transcranial direct current stimulation (TDCS). In this pilot study, 60 healthy subjects were randomized to receive high definition TACS, high definition TDCS, or sham stimulation delivered to the right fusiform cortex during encoding of visual associations. Consistent with our hypothesis, improved AM performance was observed in the TACS group, while TDCS had no effect. However, TACS also resulted in improved correct rejection of never seen items, reduced false memory, and reduced forgetting, suggesting the effect may not be specific for AM processes. Overall, this work informs strategies for improving associative memory and suggests alternating current is more effective than direct current stimulation in some contexts.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Trial Overview.
Figure 2
Figure 2
(A) Face and Scene Task (FAST): 27 encoding pairs are displayed sequentially, followed by a distraction task and then the recognition phase. In the recognition phase, 81 pairs are shown in random order with 1/3 consisting of ‘Together’ (Old) Pairs, 1/3 ‘Not-together’ (Lure) Pairs, and 1/3 ‘Never Seen’ (New) Pairs. (B) Memory Outcomes: Five memory outcomes were derived depending on the subjects response.
Figure 3
Figure 3
Study Protocol. Subjects undergo a brief training phase, followed by the complete FAST task to measure baseline performance. Subjects subsequently completed an alternate version of the FAST Task, with stimulation (TACS/TDCS/Sham) applied during the encoding phase. They returned 24 hours later to complete the recognition phase of the recognition test.
Figure 4
Figure 4
High definition Transcranial Electrical Stimulation (HD-TES). (A) Soterix MxN HD-TES system and the HD-Targets software were used to define the optimal electrode montage to focally stimulate the right fusiform cortex. (B) Finite element Modelling based on a normal adult brain template (HD-Targets software) demonstrating a high focality of electric field in the right fusiform cortex (model based on anodal direct current stimulation).
Figure 5
Figure 5
Immediate Memory Performance. TACS is the reference group. (A) Correct Associative Memory: Significant condition*group interaction, with TACS demonstrating improved memory performance compared to TDCS. (B) Incorrect Associative Memory: No difference between groups. (C) False Memory: Significant condition*group interaction, with TACS demonstrating less errors compared to TDCS. (D) Forgetting: Significant condition*group interaction, with TACS demonstrating demonstrating less errors compared to TDCS and compared to Sham. (E) Correct Rejection: Significant condition*group interaction, with TACS demonstrating improved rejection compared to TDCS.
Figure 6
Figure 6
Delayed Memory Performance. TACS is the reference group. (A) Correct Associative Memory. (B) Incorrect Associative Memory. (C) False Memory. (D) Forgetting. (E) Correct Rejection. No statistically signficiant interactions between group and condition at 24 hours.

References

    1. Squire LR. Memory systems of the brain: A brief history and current perspective. Neurobiol. Learn. Mem. 2004;82:171–177. doi: 10.1016/j.nlm.2004.06.005.
    1. SUZUKI W. A. Making New Memories: The Role of the Hippocampus in New Associative Learning. Annals of the New York Academy of Sciences. 2007;1097(1):1–11. doi: 10.1196/annals.1379.007.
    1. Reitz C, Brayne C, Mayeux R. Epidemiology of alzheimer disease. Nat. Rev. Neurol. 2011;7:137–152. doi: 10.1038/nrneurol.2011.2.
    1. Kim H. Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies. Neuroimage. 2011;54:2446–2461. doi: 10.1016/j.neuroimage.2010.09.045.
    1. Wagner AD, Shannon BJ, Kahn I, Buckner RL. Parietal lobe contributions to episodic memory retrieval. Trends Cogn. Sci. 2005;9:445–453. doi: 10.1016/j.tics.2005.07.001.
    1. Eichenbaum H. Prefrontal–hippocampal interactions in episodic memory. Nat. Rev. Neurosci. 2017;18:547–558. doi: 10.1038/nrn.2017.74.
    1. Kuskowski MA, Pardo JV. The role of the fusiform gyrus in successful encoding of face stimuli. Neuroimage. 1999;9:599–610. doi: 10.1006/nimg.1999.0442.
    1. Miyashita Y. Inferior temporal cortex: Where visual perception meets memory. Annu. Rev. Neurosci. 1993;16:263. doi: 10.1146/annurev.ne.16.030193.001333.
    1. Garoff RJ, Slotnick SD, Schacter DL. The neural origins of specific and general memory: the role of the fusiform cortex. Neuropsychologia. 2005;43:847–859. doi: 10.1016/j.neuropsychologia.2004.09.014.
    1. McGugin RW, Gatenby JC, Gore JC, Gauthier I. High-resolution imaging of expertise reveals reliable object selectivity in the fusiform face area related to perceptual performance. Proc. Natl. Acad. Sci. 2012;109:17063 LP–17068. doi: 10.1073/pnas.1116333109.
    1. Whitwell JL, et al. MRI patterns of atrophy associated with progression to AD in amnestic mild cognitive impairment. Neurology. 2008;70:512 LP–520. doi: 10.1212/01.wnl.0000280575.77437.a2.
    1. Burton EJ, McKeith IG, Burn DJ, Williams ED, O’Brien JT. Cerebral atrophy in Parkinson’s disease with and without dementia: A comparison with Alzheimer’s disease, dementia with Lewy bodies and controls. Brain. 2004;127:791–800. doi: 10.1093/brain/awh088.
    1. Pagonabarraga J, et al. Pattern of regional cortical thinning associated with cognitive deterioration in parkinson’s disease. PLoS One. 2013;8:e54980. doi: 10.1371/journal.pone.0054980.
    1. Biundo R, et al. Anatomical correlates of cognitive functions in early parkinson’s disease patients. PLoS One. 2013;8:e64222. doi: 10.1371/journal.pone.0064222.
    1. Klimesch W. EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res. Rev. 1999;29:169–195. doi: 10.1016/S0165-0173(98)00056-3.
    1. Osipova D, et al. Theta and gamma oscillations predict encoding and retrieval of declarative memory. J. Neurosci. 2006;26:7523 LP–7531. doi: 10.1523/JNEUROSCI.1948-06.2006.
    1. Nakahara K, et al. Associative-memory representations emerge as shared spatial patterns of theta activity spanning the primate temporal cortex. Nat. Commun. 2016;7:1–9. doi: 10.1038/ncomms11827.
    1. Portoles Oscar, Borst Jelmer P., van Vugt Marieke K. Characterizing synchrony patterns across cognitive task stages of associative recognition memory. European Journal of Neuroscience. 2018;48(8):2759–2769. doi: 10.1111/ejn.13817.
    1. Köster M, Finger H, Graetz S, Kater M, Gruber T. Theta-gamma coupling binds visual perceptual features in an associative memory task. Sci. Rep. 2018;8:17688. doi: 10.1038/s41598-018-35812-7.
    1. Fertonani A, Miniussi C. Transcranial electrical stimulation: What we know and do not know about mechanisms. Neuroscientist. 2017;23:109–123. doi: 10.1177/1073858416631966.
    1. Coffman BA, Clark VP, Parasuraman R. Battery powered thought: Enhancement of attention, learning, and memory in healthy adults using transcranial direct current stimulation. Neuroimage. 2014;85:895–908. doi: 10.1016/j.neuroimage.2013.07.083.
    1. Villamar, M. F. et al. Technique and Considerations in the Use of 4x1 Ring High-definition Transcranial Direct Current Stimulation (HD-tDCS). J. Vis. Exp. 10.3791/50309 (2013).
    1. Alam M, Truong DQ, Khadka N, Bikson M. Spatial and polarity precision of concentric high-definition transcranial direct current stimulation (HD-tDCS) Phys. Med. Biol. 2016;61:4506–4521. doi: 10.1088/0031-9155/61/12/4506.
    1. Dmochowski, J. P., Datta, A., Bikson, M. & Su, Y. Optimized multi-electrode stimulation increases focality and intensity at target. J. Neural Eng. 8 (2011).
    1. Leach RC, McCurdy MP, Trumbo MC, Matzen LE, Leshikar ED. Differential age effects of transcranial direct current stimulation on associative memory. Journals Gerontol. Ser. B. 2018;00:1–11.
    1. Leshikar ED, et al. Transcranial direct current stimulation of dorsolateral prefrontal cortex during encoding improves recall but not recognition memory. Neuropsychologia. 2017;106:390–397. doi: 10.1016/j.neuropsychologia.2017.10.022.
    1. Matzen LE, Trumbo MC, Leach RC, Leshikar ED. Effects of non-invasive brain stimulation on associative memory. Brain Res. 2015;1624:286–296. doi: 10.1016/j.brainres.2015.07.036.
    1. Gaynor AM, Chua EF. tDCS over the prefrontal cortex alters objective but not subjective encoding. Cogn. Neurosci. 2017;8:156–161. doi: 10.1080/17588928.2016.1213713.
    1. Leach Ryan C., McCurdy Matthew P., Trumbo Michael C., Matzen Laura E., Leshikar Eric D. Transcranial stimulation over the left inferior frontal gyrus increases false alarms in an associative memory task in older adults. Healthy Aging Research. 2016;5:1–6. doi: 10.1097/01.HXR.0000491108.83234.85.
    1. Galli G, Vadillo MA, Sirota M, Feurra M, Medvedeva A. A systematic review and meta-analysis of the effects of transcranial direct current stimulation (tDCS) on episodic memory. Brain Stimul. 2019;12:231–241. doi: 10.1016/j.brs.2018.11.008.
    1. Pergolizzi D, Chua EF. Transcranial direct current stimulation over the parietal cortex alters bias in item and source memory tasks. Brain Cogn. 2016;108:56–65. doi: 10.1016/j.bandc.2016.06.009.
    1. Perceval G, Martin AK, Copland DA, Laine M, Meinzer M. High-definition tDCS of the temporo-parietal cortex enhances access to newly learned words. Sci. Rep. 2017;7:17023. doi: 10.1038/s41598-017-17279-0.
    1. Jacobson L, Goren N, Lavidor M, Levy DA. Oppositional transcranial direct current stimulation (tDCS) of parietal substrates of attention during encoding modulates episodic memory. Brain Res. 2012;1439:66–72. doi: 10.1016/j.brainres.2011.12.036.
    1. England HB, Fyock C, Meredith Gillis M, Hampstead BM. Transcranial direct current stimulation modulates spatial memory in cognitively intact adults. Behav. Brain Res. 2015;283:191–195. doi: 10.1016/j.bbr.2015.01.044.
    1. Bjekić J, et al. The immediate and delayed effects of single tDCS session over posterior parietal cortex on face-word associative memory. Behav. Brain Res. 2019;366:88–95. doi: 10.1016/j.bbr.2019.03.023.
    1. Bjekić J, Čolić MV, Živanović M, Milanović SD, Filipović SR. Transcranial direct current stimulation (tDCS) over parietal cortex improves associative memory. Neurobiol. Learn. Mem. 2019;157:114–120. doi: 10.1016/j.nlm.2018.12.007.
    1. Antal A, Paulus W. Transcranial alternating current stimulation (tACS) Front. Hum. Neurosci. 2013;7:1–4. doi: 10.3389/fnhum.2013.00317.
    1. Ali MM, Sellers KK, Fröhlich F. Transcranial alternating current stimulation modulates large-scale cortical network activity by network resonance. J. Neurosci. 2013;33:11262 LP–11275. doi: 10.1523/JNEUROSCI.5867-12.2013.
    1. Helfrich RF, et al. Entrainment of brain oscillations by transcranial alternating current stimulation. Curr. Biol. 2014;24:333–339. doi: 10.1016/j.cub.2013.12.041.
    1. Tavakoli AV, Yun K. Transcranial alternating current stimulation (tACS) mechanisms and protocols. Front. Cell. Neurosci. 2017;11:1–10. doi: 10.3389/fncel.2017.00214.
    1. Weinrich CA, et al. Modulation of long-range connectivity patterns via frequency-specific stimulation of human cortex. Curr. Biol. 2017;27:3061–3068.e3. doi: 10.1016/j.cub.2017.08.075.
    1. Zaehle T, Rach S, Herrmann CS. Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PLoS One. 2010;5:e13766. doi: 10.1371/journal.pone.0013766.
    1. Bächinger M, et al. Concurrent tACS-fMRI reveals causal influence of power synchronized neural activity on resting state fMRI connectivity. J. Neurosci. 2017;37:4766–4777. doi: 10.1523/JNEUROSCI.1756-16.2017.
    1. Moisa M, Polania R, Grueschow M, Ruff CC. Brain network mechanisms underlying motor enhancement by transcranial entrainment of gamma oscillations. J. Neurosci. 2016;36:12053–12065. doi: 10.1523/JNEUROSCI.2044-16.2016.
    1. Kasten FH, Dowsett J, Herrmann CS. Sustained aftereffect of α-tACS lasts up to 70 min after stimulation. Frontiers in Human. Neuroscience. 2016;10:245.
    1. Polanía R, Nitsche MA, Korman C, Batsikadze G, Paulus W. The importance of timing in segregated theta phase-coupling for cognitive performance. Curr. Biol. 2012;22:1314–1318. doi: 10.1016/j.cub.2012.05.021.
    1. Röhner F, et al. Modulation of working memory using transcranial electrical stimulation: a direct comparison between TACS and TDCS. Frontiers in Neuroscience. 2018;12:761. doi: 10.3389/fnins.2018.00761.
    1. Rangarajan V, et al. Electrical stimulation of the left and right human fusiform gyrus causes different effects in conscious face perception. J. Neurosci. 2014;34:12828–12836. doi: 10.1523/JNEUROSCI.0527-14.2014.
    1. Brunyé TT, Moran JM, Holmes A, Mahoney CR, Taylor HA. Non-invasive brain stimulation targeting the right fusiform gyrus selectively increases working memory for faces. Brain Cogn. 2017;113:32–39. doi: 10.1016/j.bandc.2017.01.006.
    1. Becker N, et al. Structural brain correlates of associative memory in older adults. Neuroimage. 2015;118:146–153. doi: 10.1016/j.neuroimage.2015.06.002.
    1. Dennis NA, et al. Effects of aging on the neural correlates of successful item and source memory encoding. J. Exp. Psychol. Learn. Mem. Cogn. 2008;34:791–808. doi: 10.1037/0278-7393.34.4.791.
    1. Dennis NA, Johnson CE, Peterson KM. Brain and cognition neural correlates underlying true and false associative memories. Brain Cogn. 2014;88:65–72. doi: 10.1016/j.bandc.2014.04.009.
    1. Minear M, Park DC. A lifespan database of adult facial stimuli. Behav. Res. Methods, Instruments, Comput. 2004;36:630–633. doi: 10.3758/BF03206543.
    1. Ezzyat, Y. et al. Closed-loop stimulation of temporal cortex rescues functional networks and improves memory. Nat. Commun. 9 (2018).
    1. Nikolin S, Loo CK, Bai S, Dokos S, Martin DM. Focalised stimulation using high definition transcranial direct current stimulation (HD-tDCS) to investigate declarative verbal learning and memory functioning. Neuroimage. 2015;117:11–19. doi: 10.1016/j.neuroimage.2015.05.019.
    1. Neuling T, Wagner S, Wolters CH, Zaehle T, Herrmann CS. Finite-element model predicts current density distribution for clinical applications of tDCS and tACS. Front. psychiatry. 2012;3:83. doi: 10.3389/fpsyt.2012.00083.
    1. Ruffini G, et al. Transcranial current brain stimulation (tCS): models and technologies. IEEE Trans. Neural Syst. Rehabil. Eng. 2013;21:333–345. doi: 10.1109/TNSRE.2012.2200046.
    1. Pergolizzi D, Chua EF. Increased contextual cue utilization with tDCS over the prefrontal cortex during a recognition task. Brain Res. 2017;1655:1–9. doi: 10.1016/j.brainres.2016.11.008.
    1. Lara GAde, et al. Perturbation of theta-gamma coupling at the temporal lobe hinders verbal declarative memory. Brain Stimul. 2018;11:509–517. doi: 10.1016/j.brs.2017.12.007.
    1. Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. 2000;527:633–639. doi: 10.1111/j.1469-7793.2000.t01-1-00633.x.
    1. Stanislaw H, Todorov N. Calculation of signal detection theory measures. Behav. Res. Methods, Instruments, Comput. 1999;31:137–149. doi: 10.3758/BF03207704.
    1. Tanji J, Hoshi E. Role of the lateral prefrontal cortex in executive behavioral control. Physiol. Rev. 2008;88:37–57. doi: 10.1152/physrev.00014.2007.
    1. Haist F, Lee K, Stiles J. Individuating faces and common objects produces equal responses in putative face-processing areas in the ventral occipitotemporal cortex. Front. Hum. Neurosci. 2010;4:1–15. doi: 10.3389/fnhum.2010.00181.
    1. Fries P. Rhythms for cognition: communication through coherence. Neuron. 2015;88:220–235. doi: 10.1016/j.neuron.2015.09.034.
    1. Varela F, Lachaux JP, Rodriguez E, Martinerie J. The brainweb: Phase synchronization and large-scale integration. Nat. Rev. Neurosci. 2001;2:229–239. doi: 10.1038/35067550.
    1. Bressler SL, Menon V. Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn. Sci. 2010;14:277–290. doi: 10.1016/j.tics.2010.04.004.
    1. Sarnthein J, Petsche H, Rappelsberger P, Shaw GL, von Stein A. Synchronization between prefrontal and posterior association cortex during human working memory. Proc. Natl. Acad. Sci. USA. 1998;95:7092–7096. doi: 10.1073/pnas.95.12.7092.
    1. Onoda K, Kawagoe T, Zheng H, Yamaguchi S. Theta band transcranial alternating current stimulations modulates network behavior of dorsal anterior cingulate cortex. Sci. Rep. 2017;7:3607. doi: 10.1038/s41598-017-03859-7.
    1. Huang, Y. & Parra, L. C. Can transcranial electric stimulation with multiple electrodes reach deep targets? Brain Stimul. 10.1101/382598 (2018).
    1. Kreidler SM, et al. GLIMMPSE: Online Power Computation for Linear Models with and without a Baseline Covariate. J. Stat. Softw. 2013;54:i10. doi: 10.18637/jss.v054.i10.

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