Journal of Cognitive Enhancement

, Volume 2, Issue 1, pp 97–105 | Cite as

Without Blinking an Eye: Proactive Motor Control Enhancement

  • Asaf YanivEmail author
  • Michal Lavidor
Brief Report


While most cognitive control enhancement studies have focused on reactive inhibition paradigms, enhancement of proactive control of urge-driven behaviors has been relatively neglected. With the aim of focusing on the proactive components of cognitive control over motor output, we designed a simple, ecologically valid eye blinking suppression task and applied transcranial direct current stimulation (tDCS) over the right inferior frontal gyrus (rIFG). Fifty-three subjects randomly allocated to three different stimulation groups underwent active or sham stimulation, subsequently performing eye blinking and stop signal tasks. Results showed that anodal stimulation over the rIFG increased the ability to suppress blinks compared to sham and active control stimulation. In addition, the rIFG group demonstrated a general slowdown of the stop signal reaction time, implying proactive control enhancement. Herein, we discuss our results with regard to previous findings as well as possible interventions in clinical populations.


Cognitive control Cognitive enhancement Proactive inhibition tDCS rIFG Eye blink 



The authors thank Mrs. Phyllis Curchack Kornspan for her editorial assistance.

Funding Information

This study was supported by the Israel Science Foundation, grant no. 367/14, and the Israeli Center of Research Excellence (I-CORE) in Cognition (I-CORE Program 51/11).

Compliance with Ethical Standards

All participants completed consent forms prior to their inclusion. The study was approved by the local ethics committee and was conducted in accordance with the Declaration of Helsinki guidelines.

Conflict of Interest

The authors declare that they have no conflict of interests.


  1. Aron, A. R. (2011). From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biological Psychiatry, 69(12), e55–e68.CrossRefPubMedGoogle Scholar
  2. Aron, A. R., Fletcher, P. C., Bullmore, E. T., Sahakian, B. J., & Robbins, T. W. (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nature Neuroscience, 6(2), 115–116.CrossRefPubMedGoogle Scholar
  3. Aron, A. R., Robbins, T. W., & Poldrack, R. A. (2004). Inhibition and the right inferior frontal cortex. Trends in Cognitive Sciences, 8(4), 170–177.CrossRefPubMedGoogle Scholar
  4. Aron, A. R., Robbins, T. W., & Poldrack, R. A. (2014). Inhibition and the right inferior frontal cortex: one decade on. Trends in Cognitive Sciences, 18(4), 177–185.CrossRefPubMedGoogle Scholar
  5. Barkley, R. A. (1997). Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychological Bulletin, 121(1), 65–94.CrossRefPubMedGoogle Scholar
  6. Batsikadze, G., Moliadze, V., Paulus, W., Kuo, M. F., & Nitsche, M. A. (2013). Partially non-linear stimulation intensity-dependent effects of direct current stimulation on motor cortex excitability in humans. The Journal of Physiology, 591(7), 1987–2000.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bentivoglio, A. R., Bressman, S. B., Cassetta, E., Carretta, D., Tonali, P., & Albanese, A. (1997). Analysis of blink rate patterns in normal subjects. Movement Disorders, 12(6), 1028–1034.CrossRefPubMedGoogle Scholar
  8. Berman, B. D., Horovitz, S. G., Morel, B., & Hallett, M. (2012). Neural correlates of blink suppression and the buildup of a natural bodily urge. NeuroImage, 59(2), 1441–1450.CrossRefPubMedGoogle Scholar
  9. Berryhill, M. E., Wencil, E. B., Coslett, H. B., & Olson, I. R. (2010). A selective working memory impairment after transcranial direct current stimulation to the right parietal lobe. Neuroscience Letters, 479(3), 312–316.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bikson, M., Datta, A., Rahman, A., & Scaturro, J. (2010). Electrode montages for tDCS and weak transcranial electrical stimulation: role of “return” electrode’s position and size. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 121(12), 1976.CrossRefGoogle Scholar
  11. Boggio, P. S., Campanhã, C., Valasek, C. A., Fecteau, S., Pascual-Leone, A., & Fregni, F. (2010). Modulation of decision-making in a gambling task in older adults with transcranial direct current stimulation. European Journal of Neuroscience, 31(3), 593–597.CrossRefPubMedGoogle Scholar
  12. Bolognini, N., Fregni, F., Casati, C., Olgiati, E., & Vallar, G. (2010). Brain polarization of parietal cortex augments training-induced improvement of visual exploratory and attentional skills. Brain Research, 1349, 76–89.CrossRefPubMedGoogle Scholar
  13. Campanella, S., Schroder, E., Monnart, A., Vanderhasselt, M. A., Duprat, R., Rabijns, M., & Baeken, C. (2017). Transcranial direct current stimulation over the right frontal inferior cortex decreases neural activity needed to achieve inhibition: a double-blind ERP study in a male population. Clinical EEG and Neuroscience, 48(3), 176–188.CrossRefPubMedGoogle Scholar
  14. Cerruti, C., & Schlaug, G. (2009). Anodal transcranial direct current stimulation of the prefrontal cortex enhances complex verbal associative thought. Journal of Cognitive Neuroscience, 21(10), 1980–1987.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Chi, R. P., Fregni, F., & Snyder, A. W. (2010). Visual memory improved by non-invasive brain stimulation. Brain Research, 1353, 168–175.CrossRefPubMedGoogle Scholar
  16. Chikazoe, J., Jimura, K., Hirose, S., Yamashita, K. I., Miyashita, Y., & Konishi, S. (2009). Preparation to inhibit a response complements response inhibition during performance of a stop-signal task. Journal of Neuroscience, 29(50), 15870–15877.CrossRefPubMedGoogle Scholar
  17. Chikazoe, J., Jimura, K., Asari, T., Yamashita, K. I., Morimoto, H., Hirose, S., Konishi, S., et al. (2008). Functional dissociation in right inferior frontal cortex during performance of go/no-go task. Cerebral Cortex, 19(1), 146–152.CrossRefPubMedGoogle Scholar
  18. Colzato, L. S., Slagter, H. A., Spapé, M. M., & Hommel, B. (2008). Blinks of the eye predict blinks of the mind. Neuropsychologia, 46(13), 3179–3183.CrossRefPubMedGoogle Scholar
  19. Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3(3), 215–229.CrossRefGoogle Scholar
  20. Cunillera, T., Fuentemilla, L., Brignani, D., Cucurell, D., & Miniussi, C. (2014). A simultaneous modulation of reactive and proactive inhibition processes by anodal tDCS on the right inferior frontal cortex. PLoS One, 9(11), e113537.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Cunillera, T., Brignani, D., Cucurell, D., Fuentemilla, L., & Miniussi, C. (2016). The right inferior frontal cortex in response inhibition: a tDCS-ERP co-registration study. NeuroImage, 140, 66–75.CrossRefPubMedGoogle Scholar
  22. De Berker, A. O., Bikson, M., & Bestmann, S. (2013). Predicting the behavioral impact of transcranial direct current stimulation: issues and limitations. Frontiers in Human Neuroscience, 7, 613.CrossRefPubMedPubMedCentralGoogle Scholar
  23. DeVito, E. E., Blackwell, A. D., Clark, L., Kent, L., Dezsery, A. M., Turner, D. C., et al. (2009). Methylphenidate improves response inhibition but not reflection–impulsivity in children with attention deficit hyperactivity disorder (ADHD). Psychopharmacology, 202(1–3), 531–539.CrossRefPubMedGoogle Scholar
  24. Doane, M. G. (1980). Interactions of eyelids and tears in corneal wetting and the dynamics of the normal human eyeblink. American Journal of Ophthalmology, 89(4), 507–516.CrossRefPubMedGoogle Scholar
  25. Doughty, M. J. (2001). Consideration of three types of spontaneous eyeblink activity in normal humans: during reading and video display terminal use, in primary gaze, and while in conversation. Optometry & Vision Science, 78(10), 712–725.CrossRefGoogle Scholar
  26. Flöel, A., Rösser, N., Michka, O., Knecht, S., & Breitenstein, C. (2008). Noninvasive brain stimulation improves language learning. Journal of Cognitive Neuroscience, 20(8), 1415–1422.CrossRefPubMedGoogle Scholar
  27. Fregni, F., Boggio, P. S., Nitsche, M., Bermpohl, F., Antal, A., Feredoes, E., et al. (2005). Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Experimental Brain Research, 166(1), 23–30.CrossRefPubMedGoogle Scholar
  28. Frühholz, S., & Grandjean, D. (2012). NeuroImage towards a fronto-temporal neural network for the decoding of angry vocal expressions. NeuroImage, 62(3), 1658–1666.CrossRefPubMedGoogle Scholar
  29. Jacobson, L., Ezra, A., Berger, U., & Lavidor, M. (2012a). Modulating oscillatory brain activity correlates of behavioral inhibition using transcranial direct current stimulation. Clinical Neurophysiology, 123(5), 979–984.CrossRefPubMedGoogle Scholar
  30. Jacobson, L., Javitt, D. C., & Lavidor, M. (2011). Activation of inhibition: diminishing impulsive behavior by direct current stimulation over the inferior frontal gyrus. Journal of Cognitive Neuroscience, 23(11), 3380–3387.CrossRefPubMedGoogle Scholar
  31. Jacobson, L., Koslowsky, M., & Lavidor, M. (2012b). tDCS polarity effects in motor and cognitive domains: a meta-analytical review. Experimental Brain Research, 216(1), 1–10.CrossRefPubMedGoogle Scholar
  32. Jaffard, M., Longcamp, M., Velay, J. L., Anton, J. L., Roth, M., Nazarian, B., & Boulinguez, P. (2008). Proactive inhibitory control of movement assessed by event-related MRI. NeuroImage, 42(3), 1196–1206.CrossRefPubMedGoogle Scholar
  33. Jahfari, S., Stinear, C. M., Claffey, M., Verbruggen, F., & Aron, A. R. (2010). Responding with restraint: what are the neurocognitive mechanisms? Journal of Cognitive Neuroscience, 22(7), 1479–1492.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Juan, C. H., & Muggleton, N. G. (2012). Brain stimulation and inhibitory control. Brain Stimulation, 5(2), 63–69.CrossRefPubMedGoogle Scholar
  35. Jung, H. Y., Chung, S. J., & Hwang, J. M. (2004). Tic disorders in children with frequent eye blinking. Journal of AAPOS, 8(2), 171–174.CrossRefPubMedGoogle Scholar
  36. Kaminer, J., Powers, A. S., Horn, K. G., Hui, C., & Evinger, C. (2011). Characterizing the spontaneous blink generator: an animal model. Journal of Neuroscience, 31(31), 11256–11267.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Karson, C. N., Dykman, R. A., & Paige, S. R. (1990). Blink rates in schizophrenia. Schizophrenia Bulletin, 16(2), 345–354.CrossRefPubMedGoogle Scholar
  38. Korb, D. R., Baron, D. F., Herman, J. P., Finnemore, V. M., Exford, J. M., Hermosa, J. L., et al. (1994). Tear film lipid layer thickness as a function of blinking. Cornea, 13(4), 354–359.CrossRefPubMedGoogle Scholar
  39. Koster, E. H., Hoorelbeke, K., Onraedt, T., Owens, M., & Derakshan, N. (2017). Cognitive control interventions for depression: a systematic review of findings from training studies. Clinical Psychology Review, 53, 79–92.Google Scholar
  40. Kraft, A., Roehmel, J., Olma, M. C., Schmidt, S., Irlbacher, K., & Brandt, S. A. (2010). Transcranial direct current stimulation affects visual perception measured by threshold perimetry. Experimental Brain Research, 207(3–4), 283–290.CrossRefPubMedGoogle Scholar
  41. Kringelbach, M. L. (2005). The human orbitofrontal cortex: linking reward to hedonic experience. Nature Reviews Neuroscience, 6(9), 691–702.CrossRefPubMedGoogle Scholar
  42. Kwon, Y. H., & Kwon, J. W. (2013). Response inhibition induced in the stop-signal task by transcranial direct current stimulation of the pre-supplementary motor area and primary sensoriomotor cortex. Journal of Physical Therapy Science, 25(9), 1083–1086.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Ladas, A., Frantzidis, C., Bamidis, P., & Vivas, A. B. (2014). Eye blink rate as a biological marker of mild cognitive impairment. International Journal of Psychophysiology, 93(1), 12–16.CrossRefPubMedGoogle Scholar
  44. Lerner, A., Bagic, A., Hanakawa, T., Boudreau, E. A., Pagan, F., Mari, Z., et al. (2008). Involvement of insula and cingulate cortices in control and suppression of natural urges. Cerebral Cortex, 19(1), 218–223.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Li, C. S. R., Huang, C., Yan, P., Paliwal, P., Constable, R. T., & Sinha, R. (2008). Neural correlates of post-error slowing during a stop signal task: a functional magnetic resonance imaging study. Journal of Cognitive Neuroscience, 20(6), 1021–1029.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Lipszyc, J., & Schachar, R. (2010). Inhibitory control and psychopathology: a meta-analysis of studies using the stop signal task. Journal of the International Neuropsychological Society: JINS, 16(6), 1064–1076.CrossRefPubMedGoogle Scholar
  47. Logan, G.D. (1994). On the ability to inhibit thought and action: a users’ guide to the stop signal paradigm. In Inhibitory processes in attention, memory, and language. pp. 189–239.Google Scholar
  48. Logan, G. D., Cowan, W. B., & Davis, K. A. (1984). On the ability to inhibit simple and choice reaction time responses: a model and a method. Journal of Experimental Psychology Human Perception and Performance, 10(2), 276–291.CrossRefPubMedGoogle Scholar
  49. Maraver, M. J., Bajo, M. T., & Gomez-Ariza, C. J. (2016). Training on working memory and inhibitory control in young adults. Frontiers in Human Neuroscience, 10, 276–291.CrossRefGoogle Scholar
  50. Mazzone, L., Yu, S., Blair, C., Gunter, B. C., Wang, Z., Marsh, R., & Peterson, B. S. (2010). An FMRI study of frontostriatal circuits during the inhibition of eye blinking in persons with Tourette syndrome. American Journal of Psychiatry, 167(3), 341–349.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Monsell, S. (1996). Control of mental processes. In Unsolved mysteries of the mind: Tutorial essays in cognition. pp. 93–148.Google Scholar
  52. Moraitis, T., & Ghosh, A. (2014). Withdrawal of voluntary inhibition unravels the off state of the spontaneous blink generator. Neuropsychologia, 65, 279–286.CrossRefPubMedGoogle Scholar
  53. Müller-Vahl, K. R., Kaufmann, J., Grosskreutz, J., Dengler, R., Emrich, H. M., & Peschel, T. (2009). Prefrontal and anterior cingulate cortex abnormalities in Tourette syndrome: evidence from voxel-based morphometry and magnetization transfer imaging. BMC Neuroscience, 10(1), 47.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Nakano, T., Kato, M., Morito, Y., Itoi, S., & Kitazawa, S. (2013). Blink-related momentary activation of the default mode network while viewing videos. Proceedings of the National Academy of Sciences, 110(2), 702–706.CrossRefGoogle Scholar
  55. Nakano, T., & Kitazawa, S. (2010). Eyeblink entrainment at breakpoints of speech. Experimental Brain Research, 205(4), 577–581.CrossRefPubMedGoogle Scholar
  56. Nitsche, M. A., & Paulus, W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. The Journal of Physiology, 527(3), 633–639.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Pani, P., Menghini, D., Napolitano, C., Calcagni, M., Armando, M., Sergeant, J. A., & Vicari, S. (2013). Proactive and reactive control of movement are differently affected in attention deficit hyperactivity disorder children. Research in Developmental Disabilities, 34(10), 3104–3111.CrossRefPubMedGoogle Scholar
  58. Pierce, J. W. (2007). PsychoPy—psychophysics software in Python. Journal of Neuroscience Methods, 162(1–2), 8–13.CrossRefGoogle Scholar
  59. Peterson, B. S., & Leckman, J. F. (1998). The temporal dynamics of tics in Gilles de la Tourette syndrome. Society of Biological Psychiatry, 44(1), 1337–1348.CrossRefGoogle Scholar
  60. Schmeichel, B. J., & Zell, A. (2007). Trait self-control predicts performance on behavioral tests of self-control. Journal of Personality, 75(4), 743–756.CrossRefPubMedGoogle Scholar
  61. Schoenbaum, G., Takahashi, Y., Liu, T. L., & McDannald, M. A. (2011). Does the orbitofrontal cortex signal value? Annals of the New York Academy of Sciences, 1239(1), 87–99.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Slagter, H. A., Georgopoulou, K., & Frank, M. J. (2015). Spontaneous eye blink rate predicts learning from negative, but not positive, outcomes. Neuropsychologia, 71, 126–132.CrossRefPubMedGoogle Scholar
  63. Sparing, R., Thimm, M., Hesse, M. D., Küst, J., Karbe, H., & Fink, G. R. (2009). Bidirectional alterations of interhemispheric parietal balance by non-invasive cortical stimulation. Brain, 132(11), 3011–3020.CrossRefPubMedGoogle Scholar
  64. Spierer, L., Chavan, C. F., & Manuel, A. L. (2013). Training-induced behavioral and brain plasticity in inhibitory control. Frontiers in Human Neuroscience, 7, 427.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Stalnaker, T. A., Cooch, N. K., & Schoenbaum, G. (2015). What the orbitofrontal cortex does not do. Nature Neuroscience, 18(5), 620–627.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Stramaccia, D. F., Penolazzi, B., Sartori, G., Braga, M., Mondini, S., & Galfano, G. (2015). Assessing the effects of tDCS over a delayed response inhibition task by targeting the right inferior frontal gyrus and right dorsolateral prefrontal cortex. Experimental brain research, 233(8), 2283–2290.‏ Google Scholar
  67. Thomalla, G., Jonas, M., Bäumer, T., Siebner, H. R., Biermann-Ruben, K., Ganos, et al. (2013). Costs of control: decreased motor cortex engagement during a Go/NoGo task in Tourette’s syndrome. Brain, 137(1), 122–136.CrossRefPubMedGoogle Scholar
  68. Verbruggen, F., Aron, A. R., Stevens, M. A., & Chambers, C. D. (2010). Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex. Proceedings of the National Academy of Sciences, 107(31), 13966–13971.CrossRefGoogle Scholar
  69. Verbruggen, F., & Logan, G. D. (2009). Proactive adjustments of response strategies in the stop-signal paradigm. Journal of Experimental Psychology Human Perception and Performance, 35(3), 835–854.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Verbruggen, F., & Logan, G. D. (2008). Response inhibition in the stop-signal paradigm. Trends in Cognitive Sciences, 12(11), 418–424.CrossRefPubMedPubMedCentralGoogle Scholar
  71. Wallis, J. D. (2007). Orbitofrontal cortex and its contribution to decision-making. Annual Review of Neuroscience, 30, 31–56.CrossRefPubMedGoogle Scholar
  72. Wessel, J. R., Conner, C. R., Aron, A. R., & Tandon, N. (2013). Chronometric electrical stimulation of right inferior frontal cortex increases motor braking. Journal of Neuroscience, 33(50), 19611–19619.CrossRefPubMedPubMedCentralGoogle Scholar
  73. Worbe, Y., Gerardin, E., Hartmann, A., Valabrégue, R., Chupin, M., Tremblay, L., et al. (2010). Distinct structural changes underpin clinical phenotypes in patients with Gilles de la Tourette syndrome. Brain, 133(12), 3649–3660.CrossRefPubMedGoogle Scholar
  74. Zandbelt, B. B., van Buuren, M., Kahn, R. S., & Vink, M. (2011). Reduced proactive inhibition in schizophrenia is related to corticostriatal dysfunction and poor working memory. Biological Psychiatry, 70(12), 1151–1158.CrossRefPubMedGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of PsychologyBar-Ilan UniversityRamat GanIsrael
  2. 2.The Gonda Brain Research CenterBar-Ilan UniversityRamat GanIsrael

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