Paired-pulse transcranial magnetic stimulation reveals probability-dependent changes in functional connectivity between right inferior frontal cortex and primary motor cortex during go/no-go performance

Frontiers in Human Neuroscience

Volumn , Issue NOV, 2013, Pages

  van Campen, A Dilene ^a   Neubert, Franz Xaver ^b   van den Wildenberg, Wery P M ^a   Richard Ridderinkhof, K ^a   Mars, Rogier B ^b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Go no go task; Inhibition; Motor cortex; Paired pulse; Prediction; rIFC; TMS

Indexed keywords

ADULT; ARTICLE; BRAIN FUNCTION; BRAIN REGION; EXECUTIVE FUNCTION; FACILITATION; FEMALE; FRONTAL CORTEX; HUMAN; HUMAN EXPERIMENT; MALE; MENTAL PERFORMANCE; NORMAL HUMAN; PRIMARY MOTOR CORTEX; PROBABILITY; RIGHT INFERIOR FRONTAL CORTEX; STIMULUS RESPONSE; TASK PERFORMANCE; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84888087313     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00736     Document Type: Article

References (50)

1. Aron, A. R., Behrens, T. E., Smith, S., Frank, M. J., and Poldrack, R. A. (2007). Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. J. Neurosci. 27, 3743-3752. doi: 10.1523/JNEUROSCI.0519-07.2007
2. Aron, A. R., Fletcher, P. C., Bullmore, E. T., Sahakian, B. J., and Robbins, T. W. (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat. Neurosci.6, 115-116. doi: 10.1038/nn1003
3. Aron, A. R., and Poldrack, R. A. (2006). Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. J. Neurosci. 26, 2424-2433. doi: 10.1523/JNEUROSCI.4682-05.2006
4. Bestmann, S., Harrison, L. M., Blankenburg, F., Mars, R. B., Haggard, P., Friston, K. J., et al. (2008). Influence of uncertainty and surprise on human corticospinal excitability during preparation for action. Curr. Biol. 18, 775-780. doi: 10.1016/j.cub.2008.04.051
5. Buch, E. R., Johnen, V. M., Nelissen, N., O'Shea, J., and Rushworth, M. F. S. (2011). Noninvasive associative plasticity induction in a corticocortical pathway of the human brain. J. Neurosci. 31, 17669-17679. doi: 10.1523/JNEUROSCI.1513-11.2011
6. Buch, E. R., Mars, R. B., Boorman, E. D., and Rushworth, M. F. S. (2010). A network centered on ventral premotor cortex exerts both facilitatory and inhibitory control over primary motor cortex during action reprogramming. J. Neurosci. 30, 1395-1401. doi: 10.1523/JNEUROSCI.4882-09.2010
7. Burle, B., Bonnet, M., Vidal, F., Possamaï, C.-A., and Hasbroucq, T. (2002). A transcranial magnetic stimulation study of information processing in the motor cortex: relationship between the silent period and the reaction time delay. Psychophysiology 39, 207-217. doi: 10.1111/1469-8986.3920207
8. Catmur, C., Mars, R. B., Rushworth, M. F., and Heyes, C. (2011). Making mirrors: premotor cortex stimulation enhances mirror and counter-mirror motor facilitation. J. Cogn. Neurosci.23, 2352-2362. doi: 10.1162/jocn.2010.21590
9. Civardi, C., Cantello, R., Asselman, P., and Rothwell, J. C. (2001). Transcranial magnetic stimulation can be used to test connections to primary motor areas from frontal and medial cortex in humans. Neuroimage 14, 1444-1453. doi: 10.1006/nimg.2001.0918
10. Clark A. (2013). Whatever next? Predictive brains, situated agents, and the future of cognitive science. Behav. Brain Sci. 36,181-204. doi: 10.1017/S0140525X12000477
11. Coxon, J. P., Stinear, C. M., and Byblow, W. D. (2006). Intracortical inhibition during volitional inhibition of prepared action. J. Neurophysiol. 95, 3371-3383. doi: 10.1152/jn.01334.2005
12. den Ouden, H. E. M., Kok, P., and de Lange, F. P. (2012). How prediction errors shape perception, attention, and motivation. Front. Psychol. 3:548. doi: 10.3389/fpsyg.2012.00548
13. Duque, J., and Ivry, R. B. (2009). Role of corticospinal suppression during motor preparation. Cereb. Cortex 19, 2013-2024. doi: 10.1093/cercor/bhn230
14. Forstmann, B. U., Jahfari, S., Scholte, H. S., Wolfensteller, U., van den Wildenberg, W. P. M., and Ridderinkhof, K. R. (2008). Function and structure of the right inferior frontal cortex predict individual differences in response inhibition: a model-based approach. J. Neurosci.28, 9790-9796. doi: 10.1523/JNEUROSCI.1465-08.2008
15. Friston, K. (2005). A theory of cortical responses. Philos. Trans. R. Soc. Lond. B Biol. Sci.360, 815-836. doi: 10.1098/rstb.2005.1622
16. Fujiyama, H., Tandonnet, C., and Summers, J. J. (2011). Age-related differences in corticospinal excitability during a Go/NoGo task. Psychophysiology 48, 1448-1455. doi: 10.1111/j.1469-8986.2011.01201.x
17. Garavan, H., Ross, T. J., and Stein, E. A. (1999). Right hemispheric dominance of inhibitory control: an event-related functional MRI study. Proc. Natl. Acad. Sci. U.S.A. 96, 8301-8306. doi: 10.1073/pnas.96.14.8301
18. Hasbroucq, T., Osman, A., Possamaï, C. A., Burle, B., Carron, S., Dépy, D., et al. (1999). Cortico-spinal inhibition reflects time but not event preparation: neural mechanisms of preparation dissociated by transcranial magnetic stimulation. Acta Psychol. (Amst.) 101, 243-266. doi: 10.1016/S0001-6918(99)00007-4
19. Huettel, S. A., Song, A. W., and McCarthy, G. (2005). Decisions under uncertainty: probabilistic context influences activation of prefrontal and parietal cortices. J. Neurosci. 25, 3304-3311. doi: 10.1523/JNEUROSCI.5070-04.2005
20. Isoda, M., and Hikosaka, O. (2007). Switching from automatic to controlled action by monkey medial frontal cortex. Nat. Neurosci. 10, 240-248. doi: 10.1038/nn1830
21. Koch, G., Franca, M., Mochizuki, H., Marconi, B., Caltagirone, C., and Rothwell, J. C. (2006). Interactions between pairs of transcranial magnetic stimuli over the human left dorsal premotor cortex differ from those seen in primary motor cortex. J. Physiol. 578, 551-562. doi: 10.1113/jphysiol.2006.123562
22. Kouneiher, F., Charron, S., and Koechlin, E. (2009). Motivation and cognitive control in the human prefrontal cortex. Nat. Neurosci. 12, 939-945. doi: 10.1038/nn.2321
23. Leocani, L., Cohen, L. G., wassermann, E. M., Ikoma, K., and Hallett, M. (2000). Human corticospinal excitability evaluated with transcranial magnetic stimulation during different reaction time paradigms. Brain 123, 1161-1173. doi: 10.1093/brain/123.6.1161
24. Logan, G. D., Cowan, W. B., and Davis, K. A. (1984). On the ability to inhibit simple and choice reaction time responses: a model and a method. J. Exp. Psychol. Hum. Percept. Perform. 10, 276-291. doi: 10.1037/0096-1523.10.2.276
25. Mars, R. B., Bestmann, S., Rothwell, J. C., and Haggard, P. (2007a). Effects of motor preparation and spatial attention on corticospinal excitability in a delayed-response paradigm. Exp. Brain Res. 182, 125-129. doi: 10.1007/s00221-007-1055-4
26. Mars, R. B., Debener, S., Gladwin, T. E., Harrison, L. M., Haggard, P., Rothwell, J. C., et al. (2008). Trial-by-trial fluctuations in the event-related electroencephalogram reflect dynamic changes in the degree of surprise. J. Neurosci. 28, 12539-12545. doi: 10.1523/JNEUROSCI.2925-08.2008
27. Mars, R. B., Klein, M. C., Neubert, F.-X., Olivier, E., Buch, E. R., Boorman, E. D., et al. (2009). Short-latency influence of medial frontal cortex on primary motor cortex during action selection under conflict. J. Neurosci. 29, 6926-6931. doi: 10.1523/JNEUROSCI.1396-09.2009
28. Mars, R. B., Neubert, F. X., and Rushworth, M. F. S (2011). "Top-down control over the motor cortex, " in Neural Basis of Motivational and Cognitive Control, eds R. B. Mars, J. Sallet, M. F. S. Rushworth, and N. Yeung (Cambridge: MIT Press), 425-439.
29. Mars, R. B., Piekema, C., Coles, M. G. H., Hulstijn, W., and Toni, I. (2007b). On the programming and reprogramming of actions. Cereb. Cortex 17, 2972-2979. doi: 10.1093/cercor/bhm022
30. Miller, E. K. (2000). The prefrontal cortex and cognitive control. Nat. Rev. Neurosci. 1, 59-65. doi: 10.1038/35036228
31. Mostofsky, S. H., and Simmonds, D. J. (2008). Response inhibition and response selection: two sides of the same coin. J. Cogn. Neurosci. 20, 751-761. doi: 10.1162/jocn.2008.20500
32. Nachev, P., Wydell, H., O'Neill, K., Husain, M., and Kennard, C. (2007). The role of the pre-supplementary motor area in the control of action. Neuroimage 36(Suppl. 2), T155-63. doi: 10.1016/j.neuroimage.2007.03.034
33. Neubert, F. X., Mars, R. B., Buch, E. R., Olivier, E., and Rushworth, M. F. S. (2010). Cortical and subcortical interactions during action reprogramming and their related white matter pathways. Proc. Natl. Acad. Sci. U.S.A. 107, 13240-13245. doi: 10.1073/pnas.1000674107
34. Nieuwenhuis, S., Yeung, N., van den Wildenberg, W., and Ridderinkhof, K. R. (2003). Electrophysiological correlates of anterior cingulate function in a go/no-go task: effects of response conflict and trial type frequency. Cogn. Affect. Behav. Neurosci. 3, 17-26. doi: 10.3758/CABN.3.1.17
35. O'Shea, J., Sebastian, C., Boorman, E. D., Johansen-Berg, H., and Rushworth, M. F. S. (2007). Functional specificity of human premotor-motor cortical interactions during action selection. Eur. J. Neurosci. 26, 2085-2095. doi: 10.1111/j.1460-9568.2007.05795.x
36. Ridderinkhof, K. R., Forstmann, B. U., Wylie, S. A., Burle, B., and van den Wildenberg, W. P. M. (2011). Neurocognitive mechanisms of action control: resisting the call of the Sirens. Wiley Interdiscip. Rev. Cogn. Sci. 2, 174-192. doi: 10.1002/wcs.99
37. Ridderinkhof, K. R., van den Wildenberg, W. P. M., Segalowitz, S. J., and Carter, C. S. (2004). Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain Cogn. 56, 129-140. doi: 10.1016/j.bandc.2004.09.016
38. Rubia, K., Smith, A. B., Brammer, M. J., and Taylor, E. (2003). Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection. Neuroimage 20, 351-358. doi: 10.1016/S1053-8119(03)00275-1
39. Rushworth, M. F. S., Walton, M. E., Kennerley, S. W., and Bannerman, D. M. (2004). Action sets and decisions in the medial frontal cortex. Trends Cogn. Sci. (Regul. Ed.) 8, 410-417. doi: 10.1016/j.tics.2004.07.009
40. Schmider E., Ziegler M., Danay E., Beyer L., and Bühner M. (2010). Is it really robust? Reinvestigating the robustness of ANOVA against violations of normal distribution assumption. Methodology 6, 147-151.
41. Strange, B. A., Duggins, A., Penny, W., Dolan, R. J., and Friston, K. J. (2005). Information theory, novelty and hippocampal responses: unpredicted or unpredictable? Neural Netw. 18, 225-230. doi: 10.1016/j.neunet.2004.12.004
42. van Campen, A. D., Keuken, M. C., van den Wildenberg, W. P. M., and Ridderinkhof, K. R. (in press). TMS over M1 reveals expression and selective suppression of conflicting action impulses. J. Cogn. Neurosci. doi: 10.1162/jocn_a_00482
43. van den Wildenberg, W. P. M., Wylie, S. A., Forstmann, B. U., Burle, B., Hasbroucq, T., and Ridderinkhof, K. R. (2010a). To head or to heed? Beyond the surface of selective action inhibition: a review. Front. Hum. Neurosci. 4:222. doi: 10.3389/fnhum.2010.00222
44. van den Wildenberg, W. P. M., Burle, B., Vidal, F., van der Molen, M. W., Ridderinkhof, K. R., and Hasbroucq, T. (2010b). Mechanisms and dynamics of cortical motor inhibition in the stop-signal paradigm: A transcranial magnetic stimulation study. J. Cogn. Neurosci. 22, 225-239. doi: 10.1162/jocn.2009.21248
45. Verbruggen, F., Aron, A. R., Stevens, M. A., and Chambers, C. D. (2010). Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex. Proc. Natl. Acad. Sci. U.S.A. 107, 13966-13971. doi: 10.1073/pnas.1001957107
46. Verbruggen, F., and Logan, G. D. (2008). Response inhibition in the stop-signal paradigm. Trends Cogn. Sci. (Regul. Ed.) 12, 418-424. doi: 10.1016/j.tics.2008.07.005
47. Verguts, T., and Notebaert, W. (2009). Adaptation by binding: a learning account of cognitive control. Trends Cogn. Sci. (Regul. Ed.) 13, 252-257. doi: 10.1016/j.tics.2009.02.007
48. Vossel, S., Weidner, R., and Fink, G. R. (2011). Dynamic coding of events within the inferior frontal gyrus in a probabilistic selective attention task. J. Cogn. Neurosci. 23, 414-424. doi: 10.1162/jocn.2010.21441
49. Wylie, S. A., Ridderinkhof, K. R., Elias, W. J., Frysinger, R. C., Bashore, T. R., Downs, K. E., et al. (2010). Subthalamic nucleus stimulation influences expression and suppression of impulsive behavior in Parkinson's Disease. Brain 133, 3611-3624. doi: 10.1093/brain/awq239
50. Yamanaka, K., Kimura, T., Miyazaki, M., Kawashima, N., Nozaki, D., Nakazawa, K., et al. (2002). Human cortical activities during Go/NoGo tasks with opposite motor control paradigms. Exp. Brain Res. 142, 301-307. doi: 10.1007/s00221-001-0943-2