Abstract
Repetitive transcranial magnetic stimulation (rTMS) has the potential to be developed as a novel treatment for cognitive dysfunction. However, current methods of targeting rTMS for cognition fail to consider inter-individual functional variability. This study explored the use of a cognitive task to individualise the target site for rTMS administered to the left dorsolateral prefrontal cortex (L-DLPFC). Twenty-five healthy participants were enrolled in a sham-controlled, crossover study. Participants performed a random letter generation task under the following conditions: no stimulation, sham and active ‘online’ rTMS applied to F3 (International 10–20 System) and four standardised surrounding sites. Across all sites combined, active ‘online’ rTMS was associated with significantly reduced performance compared to sham rTMS for unique trigrams (p = 0.012), but not for unique digrams (p > 0.05). Using a novel localisation methodology based on performance outcomes from both measures, a single optimal individualised site was identified for 92% [n = 23] of participants. At the individualised site, performance was significantly poorer compared to a common standard site (F3) and both control conditions (ps < 0.01). The current results suggest that this localisation methodology using a cognitive task could be used to individualise the rTMS target site at the L-DLPFC for modulating and potentially enhancing cognitive functioning.
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References
Beam W, Borckardt JJ, Reeves ST, George MS (2009) An efficient and accurate new method for locating the F3 position for prefrontal TMS applications. Brain Stimul 2(1):50–54. https://doi.org/10.1016/j.brs.2008.09.006
Beynel L, Appelbaum LG, Luber B et al (2019a) Effects of online repetitive transcranial magnetic stimulation (rTMS) on cognitive processing: a meta-analysis and recommendations for future studies. Neurosci Biobehav Rev 107:47–58. https://doi.org/10.1016/j.neubiorev.2019.08.018
Beynel L, Davis SW, Crowell CA et al (2019b) Online repetitive transcranial magnetic stimulation during working memory in younger and older adults: a randomized within-subject comparison. PLoS ONE 14:e0213707. https://doi.org/10.1371/journal.pone.0213707
Borgomaneri S, Battaglia S, Garofalo S et al (2020) State-dependent TMS over prefrontal cortex disrupts fear-memory reconsolidation and prevents the return of fear. Curr Biol 30(18):3672–3679. https://doi.org/10.1016/j.cub.2020.06.091
Carmi L, Tendler A, Bystritsky A et al (2019) Efficacy and safety of deep transcranial magnetic stimulation for obsessive-compulsive disorder: a prospective multicenter randomized double-blind placebo-controlled trial. Am J Psychiatry 176(11):931–938. https://doi.org/10.1176/appi.ajp.2019.18101180
Cash RFH, Weigand A, Zalesky A et al (2020) Using brain imaging to improve spatial targeting of transcranial magnetic stimulation for depression. Biol Psychiatry. https://doi.org/10.1016/j.biopsych.2020.05.033
Chou YH, Ton That V, Sundman M (2020) A systematic review and meta-analysis of rTMS effects on cognitive enhancement in mild cognitive impairment and Alzheimer’s disease. Neurobiol Aging 86:1–10. https://doi.org/10.1016/j.neurobiolaging.2019.08.020
Cole EJ, Stimpson KH, Bentzley BS et al (2020) Stanford accelerated intelligent neuromodulation therapy for treatment-resistant depression. Am J Psychiatry 177:716–726. https://doi.org/10.1176/appi.ajp.2019.19070720
De Risio L, Borgi M, Pettorruso M et al (2020) Recovering from depression with repetitive transcranial magnetic stimulation (rTMS): a systematic review and meta-analysis of preclinical studies. Transl Psychiatry 10:393. https://doi.org/10.1038/s41398-020-01055-2
Dedoncker J, Brunoni AR, Baeken C, Vanderhasselt MA (2016) A systematic review and meta-analysis of the effects of transcranial direct current stimulation (tDCS) over the dorsolateral prefrontal cortex in healthy and neuropsychiatric samples: influence of stimulation parameters. Brain Stimul 9:501–517. https://doi.org/10.1016/j.brs.2016.04.006
Diamond A (2013) Executive functions. Annu Rev Psychol 64:135–168. https://doi.org/10.1146/annurev-psych-113011-143750
Dubreuil-Vall L, Chau P, Ruffini G, Widge AS, Camprodon JA (2019) tDCS to the left DLPFC modulates cognitive and physiological correlates of executive function in a state-dependent manner. Brain Stimul 12(6):1456–1463. https://doi.org/10.1016/j.brs.2019.06.006
Fitzgerald PB, Oxley TJ, Laird AR, Kulkarni J, Egan GF, Daskalakis ZJ (2006) An analysis of functional neuroimaging studies of dorsolateral prefrontal cortical activity in depression. Psychiatry Res Neuroimaging 148(1):33–45. https://doi.org/10.1016/j.pscychresns.2006.04.006
Fitzgerald PB, Hoy K, McQueen S et al (2009) A randomized trial of rTMS targeted with MRI based neuro-navigation in treatment-resistant depression. Neuropsychopharmacol 34:1255–1262. https://doi.org/10.1038/npp.2008.233
Fox MD, Buckner RL, White MP, Greicius MD, Pascual-Leone A (2012) Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate. Biol Psychiatry 72(7):595–603. https://doi.org/10.1016/j.biopsych.2012.04.028
Friedman NP, Miyake A (2017) Unity and diversity of executive functions: individual differences as a window on cognitive structure. Cortex 86:186–204. https://doi.org/10.1016/j.cortex.2016.04.023
Garofalo S, Battaglia S, di Pellegrino G (2019) Individual differences in working memory capacity and cue-guided behavior in humans. Sci Rep 9(1):1–14. https://doi.org/10.1038/s41598-019-43860-w
Garofalo S, Battaglia S, Starita F, di Pellegrino G (2021) Modulation of cue-guided choices by transcranial direct current stimulation. Cortex 137:124–137. https://doi.org/10.1016/j.cortex.2021.01.004
Ge R, Downar J, Blumberger DM, Daskalakis ZJ, Vila-Rodriguez F (2020) Functional connectivity of the anterior cingulate cortex predicts treatment outcome for rTMS in treatment-resistant depression at 3-month follow-up. Brain Stimul 13:206–214. https://doi.org/10.1016/j.brs.2019.10.012
Gescheider GA (2013) Psychophysics: the fundamentals. Psychology Press. https://doi.org/10.4324/9780203774458
Guse B, Falkai P, Gruber O et al (2013) The effect of long-term high frequency repetitive transcranial magnetic stimulation on working memory in schizophrenia and healthy controls—a randomized placebo-controlled, double-blind fMRI study. Behav Brain Res 237:300–307. https://doi.org/10.1016/j.bbr.2012.09.034
Hammer R, Paul EJ, Hillman CH et al (2019) Individual differences in analogical reasoning revealed by multivariate task-based functional brain imaging. Neuroimage 184:993–1004. https://doi.org/10.1016/j.neuroimage.2018.09.011
Hasan A, Guse B, Cordes J et al (2016) Cognitive effects of high-frequency rTMS in schizophrenia patients with predominant negative symptoms: results from a multicenter randomized sham-controlled trial. Schizophr Bull 42(3):608–618. https://doi.org/10.1093/schbul/sbv142
Hoffman RE, Hawkins KA, Gueorguieva R et al (2003) Transcranial magnetic stimulation of left temporoparietal cortex and medication-resistant auditory hallucinations. Arch Gen Psychiatry 60:49–56. https://doi.org/10.1001/archpsyc.60.1.49
Hwang JH, Kim SH, Park CS, Bang SA, Kim SE (2010) Acute high-frequency rTMS of the left dorsolateral prefrontal cortex and attentional control in healthy young men. Brain Res 1329:152–158. https://doi.org/10.1016/j.brainres.2010.03.013
Jahanshahi M, Dirnberger G (1999) The left dorsolateral prefrontal cortex and random generation of responses: studies with transcranial magnetic stimulation. Neuropsychologia 37(2):181–190. https://doi.org/10.1016/s0028-3932(98)00092-x
Jahanshahi M, Profice P, Brown RG, Ridding MC, Dirnberger G, Rothwell JC (1998) The effects of transcranial magnetic stimulation over the dorsolateral prefrontal cortex on suppression of habitual counting during random number generation. Brain J Neurol 121(8):1533–1544. https://doi.org/10.1093/brain/121.8.1533
Jahanshahi M, Dirnberger G, Fuller R, Frith CD (2000) The role of the dorsolateral prefrontal cortex in random number generation: a study with positron emission tomography. Neuroimage 12:713–725. https://doi.org/10.1006/nimg.2000.0647
Lang N, Hasan A, Sueske E, Paulus W, Nitsche MA (2008) Cortical hypoexcitability in chronic smokers? A transcranial magnetic stimulation study. Neuropsychopharmacol 33:2517–2523. https://doi.org/10.1038/sj.npp.1301645
Lefaucheur JP (2019) Transcranial magnetic stimulation. In: Aminoff MJ, Boller F, Swaab DF (eds) Handbook of clinical neurology. Elsevier, Amsterdam, pp 559–580. https://doi.org/10.1016/B978-0-444-64032-1.00037-0
Lefaucheur JP, Antal A, Ayache SS et al (2017) Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS). Clin Neurophysiol 128:56–92. https://doi.org/10.1016/j.clinph.2016.10.087
Loo CK, Martin DM (2018) Special issue on transcranial direct current stimulation. J ECT 34(3):135–136. https://doi.org/10.1097/YCT.0000000000000540
Luber B, Lisanby SH (2014) Enhancement of human cognitive performance using transcranial magnetic stimulation (TMS). Neuroimage 85(Pt 3):961–970. https://doi.org/10.1016/j.neuroimage.2013.06.007
Marra HLD, Myczkowski ML, Memória CM et al (2015) Transcranial magnetic stimulation to address mild cognitive impairment in the elderly: a randomized controlled study. Behav Neurol 2015:287843. https://doi.org/10.1155/2015/287843
Martin DM, McClintock SM, Forster J, Loo CK (2016) Does therapeutic repetitive transcranial magnetic stimulation cause cognitive enhancing effects in patients with neuropsychiatric conditions? A systematic review and meta-analysis of randomised controlled trials. Neuropsychol Rev 26:295–309. https://doi.org/10.1007/s11065-016-9325-1
Martin DM, McClintock SM, Forster JJ, Lo TY, Loo CK (2017) Cognitive enhancing effects of rTMS administered to the prefrontal cortex in patients with depression: a systematic review and meta-analysis of individual task effects. Dep Anxiety 34(11):1029–1039. https://doi.org/10.1002/da.22658
McClintock SM, Reti IM, Carpenter LL et al (2018) Consensus recommendations for the clinical application of repetitive transcranial magnetic stimulation (rTMS) in the treatment of depression. J Clin Psychiatry. https://doi.org/10.4088/JCP.16cs10905
McDonald JH (2014) Handbook of biological statistics, 3rd edn. Sparky House Publishing, Baltimore
Miyake A, Friedman NP (2012) The nature and organization of individual differences in executive functions: four general conclusions. Curr Dir Psychol Sci 21:8–14. https://doi.org/10.1177/0963721411429458
Moffa AH, Martin D, Alonzo A et al (2020) Efficacy and acceptability of transcranial direct current stimulation (tDCS) for major depressive disorder: an individual patient data meta-analysis. Prog Neuropsychopharmacol Biol Psychiatry 99:109836. https://doi.org/10.1016/j.pnpbp.2019.109836
Monchi O, Petrides M, Petre V, Worsley K, Dagher A (2001) Wisconsin card sorting revisited: distinct neural circuits participating in different stages of the task identified by event-related functional magnetic resonance imaging. J Neurosci 21:7733–7741. https://doi.org/10.1523/JNEUROSCI.21-19-07733.2001
Mylius V, Ayache SS, Ahdab R et al (2013) Definition of DLPFC and M1 according to anatomical landmarks for navigated brain stimulation: inter-rater reliability, accuracy, and influence of gender and age. Neuroimage 78:224–232. https://doi.org/10.1016/j.neuroimage.2013.03.061
Ning L, Makris N, Camprodon JA, Rathi Y (2019) Limits and reproducibility of resting-state functional MRI definition of DLPFC targets for neuromodulation. Brain Stimul 12(1):129–138. https://doi.org/10.1016/j.brs.2018.10.004
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113. https://doi.org/10.1016/0028-3932(71)90067-4
Parris BA, Wadsley MG, Arabaci G et al (2021) The effect of high-frequency rTMS of the left dorsolateral prefrontal cortex on the resolution of response, semantic and task conflict in the colour-word Stroop task. Brain Struct Funct 226(4):1241–1252. https://doi.org/10.1007/s00429-021-02237-4
Patel R, Silla F, Pierce S, Theule J, Girard TA (2020) Cognitive functioning before and after repetitive transcranial magnetic stimulation (rTMS): a quantitative meta-analysis in healthy adults. Neuropsychologia 141:107395. https://doi.org/10.1016/j.neuropsychologia.2020.107395
Rajkowska G, Goldman-Rakic PS (1995) Cytoarchitectonic definition of prefrontal areas in the normal human cortex: II. Variability in locations of areas 9 and 46 and relationship to the Talairach coordinate system. Cereb Cortex 5(4):323–337. https://doi.org/10.1093/cercor/5.4.323
Sack AT, Cohen Kadosh R, Schuhmann T, Moerel M, Walsh V, Goebel R (2009) Optimizing functional accuracy of TMS in cognitive studies: a comparison of methods. J Cog Neurosci 21(2):207–221. https://doi.org/10.1162/jocn.2009.21126
Sloan NP, Byrne LK, Enticott PG, Lum JAG (2021) Non-invasive brain stimulation does not improve working memory in schizophrenia: a meta-analysis of randomised controlled trials. Neuropsychol Rev 31:115–138. https://doi.org/10.1007/s11065-020-09454-4
Slotema CW, Blom JD, van Lutterveld R, Hoek HW, Sommer IE (2014) Review of the efficacy of transcranial magnetic stimulation for auditory verbal hallucinations. Biol Psychiatry 76(2):101–110. https://doi.org/10.1016/j.biopsych.2013.09.038
Valero-Cabre A, Amengual JL, Stengel C, Pascual-Leone A, Coubard OA (2017) Transcranial magnetic stimulation in basic and clinical neuroscience: a comprehensive review of fundamental principles and novel insights. Neurosci Biobehav Rev 83:381–404. https://doi.org/10.1016/j.neubiorev.2017.10.006
Vanderhasselt MA, De Raedt R, Baeken C, Leyman L, D’Haenen H (2006) The influence of rTMS over the left dorsolateral prefrontal cortex on Stroop task performance. Exper Brain Res 169(2):279–282. https://doi.org/10.1007/s00221-005-0344-z
Xu Y, Qiu Z, Zhu J et al (2019) The modulation effect of non-invasive brain stimulation on cognitive function in patients with mild cognitive impairment: a systematic review and meta-analysis of randomized controlled trials. BMC Neurosc 20:2. https://doi.org/10.1186/s12868-018-0484-2
Ziemann ULF (2004) TMS induced plasticity in human cortex. Rev Neurosci 15(4):253–266. https://doi.org/10.1515/REVNEURO.2004.15.4.253
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Wang, A., Nikolin, S., Moffa, A.H. et al. A novel approach for targeting the left dorsolateral prefrontal cortex for transcranial magnetic stimulation using a cognitive task. Exp Brain Res 240, 71–80 (2022). https://doi.org/10.1007/s00221-021-06233-2
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DOI: https://doi.org/10.1007/s00221-021-06233-2