Abstract
The role of the visuospatial network in mathematical processing has been established, but the role of the semantic neural network in mathematical processing is still poorly understood. The current study used high-definition transcranial direct current stimulation (HD-tDCS) to examine whether the semantic network supports mathematical processing. Using a single-blind, randomized, sham-controlled experimental design, 48 participants were randomly assigned to receive either anodal or sham HD-tDCS on the left middle temporal gyrus (LMTG), a core region of the semantic network. A number series completion task was used to measure mathematical reasoning and an arithmetical computation task was used as a control condition. Both tasks were administered before and after the 20 min HD-tDCS. The results showed that anodal HD-tDCS on the LMTG enhanced performance on the number series completion task, but not on the arithmetical computation task. Trial-level analysis further showed greater improvement at the more difficult problems of the number series completion task. These results demonstrate that the semantic network plays an important role in mathematical processing.
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Data Availability
The data are currently not publicly available due to participant privacy, but they are available from the corresponding author on reasonable request. Every request will be reviewed by the institutional review board of the State Key Laboratory of Cognitive Neuroscience and Learning at Beijing Normal University.
References
Amalric M, Dehaene S (2016) Origins of the brain networks for advanced mathematics in expert mathematicians. P Natl Acad Sci USA 113(18):4909–4917. https://doi.org/10.1073/pnas.1603205113
Amalric M, Dehaene S (2018) Cortical circuits for mathematical knowledge: evidence for a major subdivision within the brain’s semantic networks. Philos T R Soc B 373(1740). https://doi.org/10.1098/rstb.2016.0515
Amalric M, Dehaene S (2019) A distinct cortical network for mathematical knowledge in the human brain. NeuroImage 189:19–31. https://doi.org/10.1016/j.neuroimage.2019.01.001
Arsalidou M, Taylor MJ (2011) Is 2 + 2 = 4? Meta-analyses of brain areas needed for numbers and calculations. NeuroImage 54(3):2382–2393. https://doi.org/10.1016/j.neuroimage.2010.10.009
Ashkenazi S, Henik A, Ifergane G, Shelef I (2008) Basic numerical processing in left intraparietal sulcus (IPS) acalculia. Cortex 44(4):439–448. https://doi.org/10.1016/j.cortex.2007.08.008
Baldo JV, Dronkers NF (2007) Neural correlates of arithmetic and language comprehension: a common substrate? Neuropsychologia 45. 2229–235. https://doi.org/10.1016/j.neuropsychologia.2006.07.014
Bieck SM, Artemenko C, Moeller K, Klein E (2018) Low to no effect: application of tRNS during two-digit addition. https://doi.org/10.3389/fnins.2018.00176. Front Neurosci-Switz 12
Binder JR, Desai RH, Graves WW, Conant LL (2009) Where is the Semantic System? A critical review and Meta-analysis of 120 functional neuroimaging studies. Cereb Cortex 19(12):2767–2796. https://doi.org/10.1093/cercor/bhp055
Butterworth B, Cappelletti M, Kopelman M (2001) Category specificity in reading and writing: the case of number words. Nat Neurosci 4(8):784–786. https://doi.org/10.1038/90484
Cappelletti M, Butterworth B, Kopelman M (2012) Numeracy skills in patients with degenerative Disorders and focal brain lesions: a neuropsychological investigation. Neuropsychology 26(1):1–19. https://doi.org/10.1037/a0026328
Cheng DZ, Li MY, Cui JX, Wang L, Wang NY, Ouyang LY, Wang XZ, Bai XJ, Zhou XL (2022) Algebra dissociates from arithmetic in the brain semantic network. Behav Brain Funct 18(1). https://doi.org/10.1186/s12993-022-00186-4
Christmann A, Van Aelst S (2006) Robust estimation of Cronbach’s alpha. J Multivar Anal 97(7):1660–1674. https://doi.org/10.1016/j.jmva.2005.05.012
Cirino PT, Morris MK, Morris RD (2007) Semantic, executive, and visuospatial abilities in mathematical reasoning of referred college students. Assessment 14(1):94–104. https://doi.org/10.1177/1073191106291487
Cohen Kadosh R, Soskic S, Iuculano T, Kanai R, Walsh V (2010) Modulating neuronal activity produces specific and long-lasting changes in Numerical competence. Curr Biol 20(22):2016–2020. https://doi.org/10.1016/j.cub.2010.10.007
Cohen Kadosh R, Dowker A, Heine A, Kaufmann L, Kucian K (2013) Interventions for improving numerical abilities: Present and future. Trends in Neuroscience and Education 2(2):85–93. https://doi.org/10.1016/j.tine.2013.04.001
Cronbach LJ (1951) Coefficient alpha and the Internal structure of tests. Psychometrika 16(3):297–334
Cui JX, Yu XD, Yang H, Chen CS, Liang PP, Zhou XL (2013) Neural Correlates of Quantity Processing of Numeral Classifiers. Neuropsychology 27(5):583–594. https://doi.org/10.1037/a0033630
Daitch AL, Foster BL, Schrouff J, Rangarajan V, Kasikici I, Gattas S, Parvizi J (2016) Mapping human temporal and parietal neuronal population activity and functional coupling during mathematical cognition. P Natl Acad Sci USA 113(46):E7277–E7286. https://doi.org/10.1073/pnas.1608434113
Datta A, Bansal V, Diaz J, Patel J, Reato D, Bikson M (2009) Gyri-precise head model of transcranial direct current stimulation: improved spatial focality using a ring electrode versus conventional rectangular pad. Brain Stimul 2(4):201–207. https://doi.org/10.1016/j.brs.2009.03.005
Dehaene S, Spelke E, Pinel P, Stanescu R, Tsivkin S (1999) Sources of mathematical thinking: behavioral and brain-imaging evidence. Science 284(5416):970–974. https://doi.org/10.1126/science.284.5416.970
Dehaene S, Piazza M, Pinel P, Cohen L (2003) Three parietal circuits for number processing. Cogn Neuropsychol 20(3–6):487–506. https://doi.org/10.1080/02643290244000239
Delazer M, Gasperi A, Bartha L, Trinka E, Benke T (2004) Number processing in temporal lobe epilepsy. J Neurol Neurosur Ps 75(6):901–903. https://doi.org/10.1136/jnnp.2003.023614
Ding Y, Liu RD, Liu HY, Wang J, Zhen R, Jiang RH (2019) Effects of Working Memory, Strategy Use, and single-step Mental Addition on Multi-Step Mental Addition in Chinese Elementary Students. https://doi.org/10.3389/fpsyg.2019.00148. Front Psychol 10
Eger E, Sterzer P, Russ MO, Giraud AL, Kleinschmidt A (2003) A supramodal number representation in human intraparietal cortex. Neuron 37(4):719–725. https://doi.org/10.1016/S0896-6273(03)00036-9
Garcia-Sanz S, Ghotme KA, Hedmont D, Arevalo-Jaimes MY, Kadosh RC, Serra-Grabulosa JM, Redolar-Ripoll D (2022) Use of transcranial magnetic stimulation for studying the neural basis of numerical cognition: a systematic review. J Neurosci Meth 369. https://doi.org/10.1016/j.jneumeth.2022.109485
Girelli L, Semenza C, Delazer M (2004) Inductive reasoning and implicit memory: evidence from intact and impaired memory systems. Neuropsychologia 42(7):926–938. https://doi.org/10.1016/j.neuropsychologia.2003.11.016
Grabner RH, Moser J, Halverscheid S, Cohen Kadosh R, Mosbacher J (2023) Effects of slow-oscillating transcranial direct current stimulation (so-tDCS) on early memory consolidation of mathematical information. Brain Stimul 16(1):263–264. https://doi.org/10.1016/j.brs.2023.01.437
Hartmann M, Singer S, Savic B, Muri RM, Mast FW (2020) Anodal High-definition Transcranial Direct Current Stimulation over the posterior parietal cortex modulates approximate Mental arithmetic. J Cogn Neurosci 32(5):862–876. https://doi.org/10.1162/jocn_a_01514
Hawes Z, Sokolowski HM, Ononye CB, Ansari D (2019) Neural underpinnings of numerical and spatial cognition: an fMRI meta-analysis of brain regions associated with symbolic number, arithmetic, and mental rotation. Neurosci Biobehav R 103:316–336. https://doi.org/10.1016/j.neubiorev.2019.05.007
Holzman TG, Pellegrino JW, Glaser R (1983) Cognitive variables in Series Completion. J Educ Psychol 75(4):603–618. https://doi.org/10.1037/0022-0663.75.4.603
Jackson RL (2021) The neural correlates of semantic control revisited. Neuroimage 224. https://doi.org/10.1016/j.neuroimage.2020.117444
Jefferies E (2013) The neural basis of semantic cognition: converging evidence from neuropsychology, neuroimaging and TMS. Cortex 49(3):611–625. https://doi.org/10.1016/j.cortex.2012.10.008
Julien CL, Thompson JC, Neary D, Snowden JS (2010) Understanding quantity in semantic dementia. Cogn Neuropsychol 27(1):3–29. https://doi.org/10.1080/02643294.2010.487727
Kim H-Y (2013) Statistical notes for clinical researchers: assessing normal distribution (2) using skewness and kurtosis. Restor Dent Endod 38(1):52–54. https://doi.org/10.5395/rde.2013.38.1.52
Kleemans T, Segers E, Verhoeven L (2018) Role of linguistic skills in fifth-grade mathematics. J Exp Child Psychol 167:404–413. https://doi.org/10.1016/j.jecp.2017.11.012
Klessinger N, Szczerbinski M, Varley R (2007) Algebra in a man with severe aphasia. Neuropsychologia 45(8):1642–1648. https://doi.org/10.1016/j.neuropsychologia.2007.01.005
Kuo HI, Bikson M, Datta A, Minhas P, Paulus W, Kuo MF, Nitsche MA (2013) Comparing Cortical Plasticity Induced by Conventional and High-Definition 4 x 1 Ring tDCS: A Neurophysiological Study. Brain Stimul 6(4):644–648. https://doi.org/10.1016/j.brs.2012.09.010
Lang S, Gan LS, Alrazi T, Monchi O (2019) Theta band high definition transcranial alternating current stimulation, but not transcranial direct current stimulation, improves associative memory performance. Sci Rep-Uk 9. https://doi.org/10.1038/s41598-019-44680-8
Lazzaro G, Battisti A, Varuzza C, Costanzo F, Vicari S, Cohen Kadosh R, Menghini D (2023) Specific effect of high frequency tRNS over parietal cortex combined with cognitive training on numerical cognition in children and adolescents with dyscalculia. Brain Stimul 16(1):364–365. https://doi.org/10.1016/j.brs.2023.01.712
Lee TL, Ding ZH, Chan AS (2023) Can transcranial photobiomodulation improve cognitive function? A systematic review of human studies. Ageing Res Rev 83. https://doi.org/10.1016/j.arr.2022.101786
Li MY, Tan YX, Cui JX, Chen CS, Dong Q, Zhou XL (2019) The Semantic Network supports approximate computation. Neuropsychology 33(6):842–854. https://doi.org/10.1037/neu0000548
Li L, Zhou X, Gao XL, Tu DB (2020) The development and influencing factors of Kindergarteners’ mathematics problem solving based on cognitive diagnosis assessment. Zdm-Math Educ 52(4):677–690. https://doi.org/10.1007/s11858-020-01153-x
Li MY, Lu YJ, Zhou XL (2023) The involvement of the semantic neural network in rule identification of mathematical processing. Cortex 164:11–20. https://doi.org/10.1016/j.cortex.2023.03.010
Liu J, Zhang H, Chen CS, Chen H, Cui JX, Zhou XL (2017) The neural circuits for arithmetic principles. NeuroImage 147:432–446. https://doi.org/10.1016/j.neuroimage.2016.12.035
Liu J, Yuan L, Chen CS, Cui JX, Zhang H, Zhou XL (2019) The Semantic System supports the Processing of Mathematical Principles. Neuroscience 404:102–118. https://doi.org/10.1016/j.neuroscience.2019.01.043
Monti MM, Parsons LM, Osherson DN (2012) Thought Beyond Language: neural dissociation of Algebra and Natural Language. Psychol Sci 23(8):914–922. https://doi.org/10.1177/0956797612437427
Noonan KA, Jefferies E, Visser M, Ralph MAL (2013) Going beyond Inferior Prefrontal involvement in Semantic Control: evidence for the additional contribution of dorsal angular gyrus and posterior middle temporal cortex. J Cogn Neurosci 25(11):1824–1850. https://doi.org/10.1162/jocn_a_00442
Numssen O, van der Burght CL, Hartwigsen G (2023) Revisiting the focality of non-invasive brain stimulation-implications for studies of human cognition. Neurosci Biobehav R 149. https://doi.org/10.1016/j.neubiorev.2023.105154
Pasqualotto A (2016) Transcranial random noise stimulation benefits arithmetic skills. Neurobiol Learn Mem 133:7–12. https://doi.org/10.1016/j.nlm.2016.05.004
Price AR, Peelle JE, Bonner MF, Grossman M, Hamilton RH (2016) Causal evidence for a mechanism of semantic integration in the angular Gyrus as revealed by high-definition Transcranial Direct Current Stimulation. J Neurosci 36(13):3829–3838. https://doi.org/10.1523/Jneurosci.3120-15.2016
Ralph MAL, Jefferies E, Patterson K, Rogers TT (2017) The neural and computational bases of semantic cognition. Nat Rev Neurosci 18(1):42–55. https://doi.org/10.1038/nrn.2016.150
Reber TP, Mackay S, Bausch M, Kehl MS, Borger V, Surges R, Mormann F (2023) Single-neuron mechanisms of neural adaptation in the human temporal lobe. Nat Commun 14(2496). https://doi.org/10.1038/s41467-023-38190-5
Rottschy C, Langner R, Dogan I, Reetz K, Laird AR, Schulz JB, Fox PT, Eickhoff SB (2012) Modelling neural correlates of working memory: a coordinate-based meta-analysis. NeuroImage 60(1):830–846. https://doi.org/10.1016/j.neuroimage.2011.11.050
Schroeder PA, Dresler T, Bahnmueller J, Artemenko C, Cohen Kadosh R, Nuerk HC (2017) Cognitive enhancement of Numerical and arithmetic capabilities: a mini-review of available Transcranial Electric Stimulation Studies. J Cogn Enhancement 1(1):39–47. https://doi.org/10.1007/s41465-016-0006-z
Seghier ML (2023) Multiple functions of the angular gyrus at high temporal resolution. Brain Struct Funct 228(1):7–46. https://doi.org/10.1007/s00429-022-02512-y
Smith P, Fernandes C, Strand S (2001) Cognitive abilities test 3: technical manual and pupil book. NFER-Nelson, Windsor
Thioux M, Pesenti M, Costes N, De Volder A, Seron X (2005) Task-independent semantic activation for numbers and animals. Cogn Brain Res 24(2):284–290. https://doi.org/10.1016/j.cogbrainres.2005.02.009
Tomasino B, Gremese M (2016) Effects of stimulus type and strategy on Mental Rotation Network: an activation likelihood estimation Meta-analysis. Front Hum Neurosci 9. https://doi.org/10.3389/fnhum.2015.00693
van der Burght CL, Numssen O, Schlaak B, Goucha T, Hartwigsen G (2023) Differential contributions of inferior frontal gyrus subregions to sentence processing guided by intonation. Hum Brain Mapp 44(2):585–598. https://doi.org/10.1002/hbm.26086
Wang L, Li MY, Yang T, Wang L, Zhou XL (2022) Mathematics meets Science in the brain. Cereb Cortex 32(1):123–136. https://doi.org/10.1093/cercor/bhab198
Wei W, Yuan HB, Chen CS, Zhou XL (2012) Cognitive correlates of performance in advanced mathematics. Brit J Educ Psychol 82(1):157–181. https://doi.org/10.1111/j.2044-8279.2011.02049.x
West SG, Finch JF, Curran PJ (1995) Structural equation models with nonnormal variables: problems and remedies. Structural equation modeling: concepts, issues, and applications. Sage Publications, Inc, pp 56–75
Xiao F, Wang ZD, Yuan SQ, Liang K, Chen QF (2022) Relational integration predicted numerical inductive reasoning: ERP evidence from the N400 and LNC. Psychophysiology 59(9). https://doi.org/10.1111/psyp.14046
Xue HL, Zhao LB, Wang YP, Dong Q, Chen CS, Xue G (2017) Anodal transcranial direct current stimulation over the left temporoparietal cortex facilitates assembled phonology. Trends in Neuroscience and Education 8–9:10–17. https://doi.org/10.1016/j.tine.2017.08.001
Yao YZ, Jia XQ, Luo J, Chen FY, Liang PP (2020) Involvement of the right Dorsolateral Prefrontal Cortex in Numerical Rule induction: a transcranial Direct Current Stimulation Study. Front Hum Neurosci 14. https://doi.org/10.3389/fnhum.2020.566675
Zacks JM (2008) Neuroimaging studies of mental rotation: a meta-analysis and review. J Cogn Neurosci 20(1):1–19. https://doi.org/10.1162/jocn.2008.20013
Zhang H, Chen CS, Zhou XL (2012) Neural correlates of numbers and mathematical terms. NeuroImage 60(1):230–240. https://doi.org/10.1016/j.neuroimage.2011.12.006
Zhang L, Gan JQ, Wang HX (2015) Localization of neural efficiency of the mathematically gifted brain through a feature subset selection method. Cogn Neurodyn 9(5):495–508. https://doi.org/10.1007/s11571-015-9345-1
Zhang YY, Chen CS, Liu H, Cui JX, Zhou XL (2016) Both non-symbolic and symbolic quantity processing are important for arithmetical computation but not for mathematical reasoning. J Cogn Psychol 28(7):807–824. https://doi.org/10.1080/20445911.2016.1205074
Zhao WY, Li YC, Du Y (2021) TMS reveals Dynamic Interaction between Inferior Frontal Gyrus and posterior middle temporal Gyrus in Gesture-Speech Semantic Integration. J Neurosci 41(50):10356–10364. https://doi.org/10.1523/Jneurosci.1355-21.2021
Zhou XL, Zeng JY (2022) Three-component mathematics for students. Infant Child Dev 31(1). https://doi.org/10.1002/icd.2283
Zhou XL, Chen CS, Zang YF, Dong Q, Chen CH, Qiao SB, Gong QY (2007) Dissociated brain organization for single-digit addition and multiplication. NeuroImage 35(2):871–880. https://doi.org/10.1016/j.neuroimage.2006.12.017
Zhou XL, Li MY, Li LNA, Zhang YY, Cui JX, Liu J, Chen CS (2018) The semantic system is involved in mathematical problem solving. NeuroImage 166:360–370. https://doi.org/10.1016/j.neuroimage.2017.11.017
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This work was supported by the National Natural Science Foundation of China [grant number: 31700977, 31671151], the Natural Science Foundation of Beijing [grant number: 5212004], the 111 Project [grant number: BP0719032], and the Advanced Innovation Center for Future Education [grant number: 27900-110631111].
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Mengyi Li. The first draft of the manuscript was written by Mengyi Li and Dazhi Cheng, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Li, M., Cheng, D., Chen, C. et al. High-definition transcranial direct current stimulation (HD-tDCS) of the left middle temporal gyrus (LMTG) improves mathematical reasoning. Brain Topogr 36, 890–900 (2023). https://doi.org/10.1007/s10548-023-00996-3
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DOI: https://doi.org/10.1007/s10548-023-00996-3