Preliminary evidence for performance enhancement following parietal lobe stimulation in Developmental Dyscalculia

Teresa Iuculano, Roi Cohen Kadosh, Teresa Iuculano, Roi Cohen Kadosh

Abstract

Nearly 7% of the population exhibit difficulties in dealing with numbers and performing arithmetic, a condition named Developmental Dyscalculia (DD), which significantly affects the educational and professional outcomes of these individuals, as it often persists into adulthood. Research has mainly focused on behavioral rehabilitation, while little is known about performance changes and neuroplasticity induced by the concurrent application of brain-behavioral approaches. It has been shown that numerical proficiency can be enhanced by applying a small-yet constant-current through the brain, a non-invasive technique named transcranial electrical stimulation (tES). Here we combined a numerical learning paradigm with transcranial direct current stimulation (tDCS) in two adults with DD to assess the potential benefits of this methodology to remediate their numerical difficulties. Subjects learned to associate artificial symbols to numerical quantities within the context of a trial and error paradigm, while tDCS was applied to the posterior parietal cortex (PPC). The first subject (DD1) received anodal stimulation to the right PPC and cathodal stimulation to the left PPC, which has been associated with numerical performance's improvements in healthy subjects. The second subject (DD2) received anodal stimulation to the left PPC and cathodal stimulation to the right PPC, which has been shown to impair numerical performance in healthy subjects. We examined two indices of numerical proficiency: (i) automaticity of number processing; and (ii) mapping of numbers onto space. Our results are opposite to previous findings with non-dyscalculic subjects. Only anodal stimulation to the left PPC improved both indices of numerical proficiency. These initial results represent an important step to inform the rehabilitation of developmental learning disabilities, and have relevant applications for basic and applied research in cognitive neuroscience, rehabilitation, and education.

Keywords: Developmental Dyscalculia; learning; neural compensation; rehabilitation; transcranial electrical stimulation.

Figures

Figure 1
Figure 1
Artificial digits. Symbols used as stimuli during the learning phase and the numerical Stroop task and their equivalent as everyday digitsadapted from Tzelgov et al. (2000). Reprinted from Cohen Kadosh et al. (2010), with permission from Elsevier.
Figure 2
Figure 2
Schematic outline of the experimental design in a typical daily session. (A) tDCS was delivered for 20 min from the start of the training. In this example, anodal stimulation is applied to the right parietal lobe (red arrow), whereas cathodal stimulation is delivered to the left parietal lobe (blue arrow). (B) The training continued after the termination of the stimulation. (C) Once the training ended, the subjects performed the numerical Stroop task and (D) the number line task. The time next to each image reflects the elapsed time from the beginning of the daily session until its termination in a cumulative fashion. Please note that on Day 1 only, the session ended after the learning phase—thereby it did not include the experimental tasks (i.e., Stroop-task and number line task). Reprinted from Cohen Kadosh et al. (2010), with permission from Elsevier.
Figure 3
Figure 3
Number Line task. Subjects were asked to map the given symbol, which appeared randomly at the left upper corner—as in the current example—or at the right upper corner, on the physical line. Subjects were instructed to place each symbol on the line according to its magnitude. Reprinted from Cohen Kadosh et al. (2010), with permission from Elsevier.
Figure 4
Figure 4
Learning functions for the two DD individuals. DD1 received Right Anodal—Left Cathodal (RA-LC) stimulation to the PPC (dotted red line); DD2 received Left Anodal—Right Cathodal (RC-LA) stimulation to the PPC (solid blue line). The improvement in the learning task over blocks (x-axis) was modeled using a power law function. Non-linear regression showed an equivalent fit for both participants (RA-LC, R = 0.9; RC-LA, R = 0.96).
Figure 5
Figure 5
Numerical Stroop task. Congruency effect (measured in terms of accuracy) for the two DD individuals. DD1 did not exhibit the canonical Congruency effect (Congruent > Neutral > Incongruent), while DD2 showed a clear Congruency pattern in the predicted direction. For DD1: Neutral > Congruent (p < 0.05); Congruent vs. Incongruent (p = 0.13); Incongruent vs. Neutral (p = 0.08). For DD2: Congruent > Incongruent (p < 0.05); Congruent vs. Neutral (p = 0.07); Incongruent vs. Neutral (p = 0.16). Data are mean ± standard error (SE) of the mean. *p < 0.05.
Figure 6
Figure 6
Numerical distance by congruency effects. Effects measured in terms of RTs for each DD individual. DD1 did not exhibit the canonical Congruency effect (Incongruent > Neutral > Congruent), while DD2 showed a Congruency pattern related to the numerical distance between stimuli. For DD1 both Congruent as well as Incongruent trials were slower than Neutral trials (p < 0.001) and no effect of numerical distance was evident [F < 1]. In DD2, the canonical pattern typical of the Congruency effect (Incongruent > Congruent) was only present for small distances (e.g., 2–4) (p < 0.05); while the reverse pattern (Congruent > Incongruent) characterized DD2's performance with large numerical distances (e.g., 2–7) (p < 0.05). Main effects are shown in black (DD1's profile). Interaction is shown in shades of green (DD2's profile). Data are mean ± standard error (SE) of the mean. *p < 0.05; ***p < 0.001.
Figure 7
Figure 7
Average location of subjective responses on the number line task plotted for each type of stimulation. Linear regression lines and equations are indicated for each type of stimulation (Red line—Right Anodal-Left Cathodal stimulation received by DD1; Blue line—Left Anodal-Right Cathodal stimulation received by DD2).

References

    1. Albert N. B., Robertson E. M., Miall R. C. (2009). The resting human brain and motor learning. Curr. Biol. 19, 1023–1027 10.1016/j.cub.2009.04.028
    1. Ansari D. (2008). Effects of development and enculturation on number representation in the brain. Nat. Rev. Neurosci. 9, 278–291 10.1038/nrn2334
    1. Ansari D., Dhital B. (2006). Age-related changes in the activation of the intraparietal sulcus during nonsymbolic magnitude processing: an event-related functional magnetic resonance imaging study. J. Cogn. Neurosci. 18, 1820–1828 10.1162/jocn.2006.18.11.1820
    1. Ansari D., Garcia N., Lucas E., Hamon K., Dhital B. (2005). Neural correlates of symbolic number processing in children and adults. Neuroreport 16, 1769–1773 10.1097/01.wnr.0000183905.23396.f1
    1. Battelli L., Alvarez G. A., Carlson T., Pascual-Leone A. (2009). The role of the parietal lobe in visual extinction studies with transcranial magnetic stimulation. J. Cogn. Neurosci. 21, 1946–1955 10.1162/jocn.2008.21149
    1. Booth J. L., Siegler R. S. (2008). Numerical magnitude representations influence arithmetic learning. Child Dev. 79, 1016–1031 10.1111/j.1467-8624.2008.01173.x
    1. Butterworth B. (2003). Dyscalculia Screener. London: nferNelson Publishing Company, Ltd
    1. Butterworth B. (2005). Developmental Dyscalculia, in Handbook of Mathematical Cognition, ed Campbell J. I. D. (Hove: Psychology Press; ), 455–467
    1. Butterworth B., Reigosa-Crespo V. (2007). Information processing deficits in dyscalculia, in Why is Math so Hard for Some Children? The Nature and Origins of Mathematical Learning Difficulties and Disabilities, eds Berch D. B., Mazzocco M. M. M. (Baltimore, MD: Paul H. Brookes Publishing Co.), 65–81
    1. Butterworth B., Varma S., Laurillard D. (2011). Dyscalculia: from brain to education. Science 332, 1049–1053 10.1126/science.1201536
    1. Bynner J., Parsons S. (1997). Does Numeracy Matter? London: The Basic Skills Agency
    1. Cantlon J. F., Brannon E. M., Carter E. J., Pelphrey K. A. (2006). Functional imaging of numerical processing in adults and 4-y-old children. PLoS Biol. 4:e125 10.1371/journal.pbio.0040125
    1. Cohen Kadosh R. (2013). Using transcranial electrical stimulation to enhance cognitive functions in the typical and atypical brain. Transl. Neurosci. 4, 20–33 10.2478/s13380-013-0104-7
    1. Cohen Kadosh R., Cohen Kadosh K., Schuhmann T., Kaas A., Goebel R., Henik A., et al. (2007a). Virtual dyscalculia induced by parietal-lobe TMS impairs automatic magnitude processing. Curr. Biol. 17, 689–693 10.1016/j.cub.2007.02.056
    1. Cohen Kadosh R., Cohen Kadosh K., Linden D. E. J., Gevers W., Berger A., Henik A. (2007b). The brain locus of interaction between number and size: a combined functional magnetic resonance imaging and event-related potential study. J. Cogn. Neurosci. 19, 957–970 10.1162/jocn.2007.19.6.957
    1. Cohen Kadosh R., Dowker A., Heine A., Kaufmann L., Kucian K. (2013). Interventions for improving numerical abilities: present and future. Trends Neurosci. Educ. 2, 85–93 10.1016/j.tine.2013.04.001
    1. Cohen Kadosh R., Henik A., Rubinsten O. (2008). Are Arabic and verbal numbers processed in different ways?. J. Exp. Psychol. Learn. Mem. Cogn. 34, 1377–1391 10.1037/a0013413
    1. 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, 2016–2020 10.1016/j.cub.2010.10.007
    1. Cohen Kadosh R., Walsh V. (2009). Numerical representation in the parietal lobes: abstract or not abstract? Behav. Brain Sci. 32, 313–373 10.1017/S0140525X09990938
    1. Dehaene S., Izard V., Spelke E., Pica P. (2008). Log or linear? Distinct intuitions of the number scale in Western and Amazonian indigene cultures. Science 320, 1217–1220 10.1126/science.1156540
    1. Dehaene S., Piazza M., Pinel P., Cohen L. (2003). Three parietal circuits for number processing. Cogn. Neuropsychol. 20, 487–506 10.1080/02643290244000239
    1. Dowker A. (2009). What Works for Children with Mathematical Difficulties? The effectiveness of intervention schemes. Department for Children, Schools and Families. Available online at:
    1. Duncan J. (2001). An adaptive coding model of neural function in prefrontal cortex. Nat. Rev. Neurosci. 2, 820–829 10.1038/35097575
    1. Ferbert A., Priori A., Rothwell J. C., Day B. L., Colebatch J. G., Marsden C. D. (1992). Interhemispheric inhibition of the human motor cortex. J. Physiol. 453, 525–546
    1. Gibson E. J., Gibson J. J., Pick A. D., Osser H. (1962). A developmental study of the discrimination of letter-like forms. J. Comp. Physiol. Psychol. 55, 897–906 10.1037/h0043190
    1. Girelli L., Lucangeli D., Butterworth B. (2000). The development of automaticity in accessing number magnitude. J. Exp. Child Psychol. 76, 104–122 10.1006/jecp.2000.2564
    1. Halberda J., Ly R., Wilmer J. B., Naiman D. Q., Germine L. (2012). Number sense across the lifespan as revealed by a massive Internet-based sample. Proc. Natl. Acad. Sci. U.S.A. 109, 11116–11120 10.1073/pnas.1200196109
    1. Halberda J., Mazzocco M. M., Feigenson L. (2008). Individual differences in non-verbal number acuity correlate with maths achievement. Nature 455, 665–668 10.1038/nature07246
    1. Hauser T. U., Rotzer S., Grabner R. H., Mèrillat S., Jancke L. (2013). Enhancing performance in numerical magnitude processing and mental arithmetic using transcranial Direct Current Stimulation (tDCS). Front. Hum. Neurosci. 7:244 10.3389/fnhum.2013.00244
    1. Hyde D. C., Boas D. A., Blair C., Carey S. (2010). Near-infrared spectroscopy shows right parietal specialization for number in pre-verbal infants. Neuroimage 53, 647–652 10.1016/j.neuroimage.2010.06.030
    1. Isaacs E. B., Edmonds C. J., Lucas A., Gadian D. G. (2001). Calculation difficulties in children of very low birthweight - a neural correlate. Brain 124, 1701–1707 10.1093/brain/124.9.1701
    1. Iuculano T., Butterworth B. (2011). Understanding the real value of fractions and decimals. Q. J. Exp. Psychol. (Hove) 64, 2088–2098 10.1080/17470218.2011.604785
    1. Iuculano T., Cohen Kadosh R. (2013). The mental cost of cognitive enhancement. J. Neurosci. 33, 4482–4486 10.1523/JNEUROSCI.4927-12.2013
    1. Iuculano T., Tang J., Hall C. W. B., Butterworth B. (2008). Core information processing deficits in developmental dyscalculia and low numeracy. Dev. Sci. 11, 669–680 10.1111/j.1467-7687.2008.00716.x
    1. Jackson M., Warrington E. K. (1986). Arithmetic skills in patients with unilateral cerebral lesions. Cortex 22, 611–620 10.1016/S0010-9452(86)80020-X
    1. Jacobson L., Koslowsky N., Lavidor M. (2012). tDCS polarity effects in motor and cognitive domains: a meta-analytical review. Exp. Brain Res. 216, 1–10 10.1007/s00221-011-2891-9
    1. Kaufmann L., Vogel S. E., Starke M., Kremser C., Schocke M., Wood G. (2009). Developmental dyscalculia: compensatory mechanisms in left intraparietal regions in response to nonsymbolic magnitudes. Behav. Brain Funct. 5, 1–6 10.1186/1744-9081-5-35
    1. Kaufmann L., Wood G., Rubinsten O., Henik A. (2011). Meta-analyses of developmental fMRI studies investigating typical and atypical trajectories of number processing and calculation. Dev. Neuropsychol. 36, 763–787 10.1080/87565641.2010.549884
    1. Krause B., Màrquez-Ruiz J., Cohen Kadosh R. (2013). The effect of transcranial direct current stimulation: a role for cortical excitation/inhibition balance? Front. Hum. Neurosci. 7:602 10.3389/fnhum.2013.00602
    1. Kucian K., Grond U., Rotzer S., Henzi B., Schonmann C., Plangger F., et al. (2011). Mental number line training in children with developmental dyscalculia. Neuroimage 57, 782–795 10.1016/j.neuroimage.2011.01.070
    1. Lindenberg R., Renga V., Zhu L. L., Nair D., Schlaug G. (2010). Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology 75, 2176–2184 10.1212/WNL.0b013e318202013a
    1. Marquez-Ruiz J., Leal-Campanario R., Sanchez-Campusano R., Molaee-Ardekani B., Wendling F., Miranda P. C., et al. (2012). Transcranial direct-current stimulation modulates synaptic mechanisms involved in associative learning in behaving rabbits. Proc. Natl. Acad. Sci. U.S.A. 109, 6710–6715 10.1073/pnas.1121147109
    1. Murase N., Duque J., Mazzocchio R., Cohen L. G. (2004). Influence of interhemispheric interactions on motor function in chronic stroke. Ann. Neurol. 55, 400–409 10.1002/ana.10848
    1. Nathan S. S., Sinha S. R., Gordon B., Lesser R. P., Thakor N. V. (1993). Determination of current density distributions generated by electrical stimulation of the human cerebral cortex. Electroencephalogr. Clin. Neurophysiol. 86, 183–192 10.1016/0013-4694(93)90006-H
    1. Newell A., Rosenbloom P. (1981). Mechanisms of skill acqusition and the law of practice, in Cognitive Skills and their Acquisition, ed Anderson J. R. (Hillsdale, NJ: Erlbaum; ), 1–55
    1. Nichelli P., Rinaldi M., Cubelli R. (1989). Selective spatial attention and length representation in normal subjects and in patients with unilateral spatial neglect. Brain Cogn. 9, 57–70 10.1016/0278-2626(89)90044-4
    1. Parsons S., Bynner J. (2005). Does Numeracy Matter More? London: National Research and Development Centre for Adult Literacy and Numeracy, Institute od Education
    1. Paulus W. (2011). Transcranial electrical stimulation (tES - tDCS; tRNS, tACS) methods. Neuropsychol. Rehabil. 21, 602–617 10.1080/09602011.2011.557292
    1. Piazza M., Facoetti A., Trussardi A. N., Berteletti I., Conte S., Lucangeli D., et al. (2010). Developmental trajectory of number acuity reveals a severe impairment in developmental dyscalculia. Cognition 116, 33–41 10.1016/j.cognition.2010.03.012
    1. Price G. R., Holloway I., Rasanen P., Vesterinen M., Ansari D. (2007). Impaired parietal magnitude processing in developmental dyscalculia. Curr. Biol. 17, R1042–R1043 10.1016/j.cub.2007.10.013
    1. Reigosa-Crespo V., Valdes-Sosa M., Butterworth B., Estevez N., Rodriguez M., Santos E., et al. (2012). Basic numerical capacities and prevalence of developmental dyscalculia: the Havana Survey. Dev. Psychol. 48, 123–135 10.1037/a0025356
    1. Rivera S. M., Reiss A. L., Eckert M. A., Menon V. (2005). Developmental changes in mental arithmetic: evidence for increased functional specialization in the left inferior parietal cortex. Cereb. Cortex 15, 1779–1790 10.1093/cercor/bhi055
    1. Rotzer S., Kucian K., Martin E., von Aster M., Klaver P., Loenneker T. (2008). Optimized voxel-based morphometry in children with developmental dyscalculia. Neuroimage 39, 417–422 10.1016/j.neuroimage.2007.08.045
    1. Rubinsten O., Henik A. (2006). Double dissociation of functions in developmental dyslexia and dyscalculia. J. Educ. Psychol. 98, 854–867 10.1037/0022-0663.98.4.854
    1. Rubinsten O., Henik A., Berger A., Shahar-Shalev S. (2002). The development of internal representations of magnitude and their association with Arabic numerals. J. Exp. Child Psychol. 81, 74–92 10.1006/jecp.2001.2645
    1. Schwarz W., Ischebeck A. (2003). On the relative speed account of number-size interference in comparative judgments of numerals. J. Exp. Psychol. Hum. Percept. Perform. 29, 507–522 10.1037/0096-1523.29.3.507
    1. Shalev R. S. (2007). Prevalence of developmental dyscalculia, in Why is Math so Hard for Some Children? The Nature and Origins of Mathematical Learning Difficulties and Disabilities, eds Berch D. B., Mazzocco M. M. M. (Baltimore, MD: Paul H. Brookes Publishing Co.), 49–60
    1. Shalev R. S., Manor O., Gross-Tsur V. (2005). Developmental dyscalculia: a prospective six year follow up. Dev. Med. Child Psychol. 47, 121–125 10.1111/j.1469-8749.2005.tb01100.x
    1. Snowball A., Tachtsidis I., Popescu T., Thompson J., Delazer M., Zamarian L., et al. (2013). Long-term enhancement of brain function and cognition using cognitive training and brain stimulation. Curr. Biol. 23, 987–992 10.1016/j.cub.2013.04.045
    1. Takatsuru Y., Fukumoto D., Yoshitomo M., Nemoto T., Tsukada H., Nabekura J. (2009). Neuronal circuit remodeling in the contralateral cortical hemisphere during functional recovery from cerebral infarction. J. Neurosci. 29, 10081–10086 10.1523/JNEUROSCI.1638-09.2009
    1. Truong D., Minhas P., Nair A., Bikson M. (in press). Computational modelling assisted design of optimize and individualized transcranial direct current stimulation protocols, in The Stimulated Brain, ed Cohen Kadosh R. (Amsterdam: Elsevier; ).
    1. Tzelgov J., Meyer J., Henik A. (1992). Automatic and intentional processing of numerical information. J. Exp. Psychol. Learn. Mem. Cogn. 18, 166–179 10.1037/0278-7393.18.1.166
    1. Tzelgov J., Yehene V., Kotler L., Alon A. (2000). Automatic comparisons of artificial digits never compared: learning linear ordering relations. J. Exp. Psychol. Learn. Mem. Cogn. 26, 103–120 10.1037/0278-7393.26.1.103
    1. Vines B. W., Nair D., Schlaug G. (2006). Contralateral and ipsi-lateral motor effects after transcranial direct current stimulation. Neuroreport 17, 671–674 10.1097/00001756-200604240-00023
    1. Wagner T., Valero-Cabre A., Pascual-Leone A. (2007). Noninvasive human brain stimulation. Annu. Rev. Biomed. Eng. 9, 527–565 10.1146/annurev.bioeng.9.061206.133100
    1. Wechsler D. (1986). Wechsler Adult Intelligence Scale-Revised. New York, NY: The Psychological Corporation
    1. Zimerman M., Hummel F. C. (in press). Brain stimulation and its role in neurological diseases, in The Stimulated Brain, ed Cohen Kadosh R. (Amsterdam: Elsevier; ).

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