Abstract
It is widely accepted that regions within the dorsal medial frontal cortex are involved in the control of voluntary action. However, recent evidence suggests that a subset of these regions may also be important for unconscious and involuntary motor processes. Indeed, Sumner et al. (Neuron 54:697–711, 2007) showed that two patients with micro-lesions of the supplementary motor area (SMA) and supplementary eye field (SEF) demonstrated an absence of unconscious inhibition as evoked by masked-prime stimuli, while pre-SMA damage had no such effect. Here, we employ fMRI and a similar masked-prime task to test whether SMA and pre-SMA are similarly dissociated in healthy volunteers. Reaction times (RT) revealed that responses to compatible trials were slower than those to incompatible trials (negative compatibility effect, NCE), indicating automatic inhibition in every participant. BOLD signals in the SMA were modulated by prime compatibility, showing greater signal for compatible trials, but there was no change in pre-SMA. There was also no modulation in the hand motor cortex (HMC). These findings imply that the SMA is involved in automatic suppression of manual motor plans.
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Aron AR, Schlaghecken F, Fletcher PC, Bullmore ET, Eimer M, Barker R, Sahakian BJ, Robbins TW (2003) Inhibition of subliminally primed responses is mediated by the caudate and thalamus: evidence from functional MRI and Huntington’s disease. Brain 126:713–723
Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD (2001) Conflict monitoring and cognitive control. Psychol Rev 108(3):624–652
Bowman H, Schlaghecken F, Eimer M (2006) A neural network model of inhibitory processes in subliminal priming. Vis cogn 13:401–480
Boy F, Sumner P (2010) Tight coupling between positive and reversed priming in the masked prime paradigm. J Exp Psychol Hum Percept Perform 36(4):892–905
Boy F, Clarke K, Sumner P (2008) Mask stimulus triggers inhibition in subliminal visuomotor priming. Exp Brain Res 190:111–116
Boy F, Evans J, Edden RAE, Husain M, Singh KD, Husain M and Sumner P (in press) Individual differences in subconscious motor control predicted by GABA concentration in SMA. Curr Biol
Caulo M, Briganti C, Mattei PA, Perfetti B, Ferretti A, Romani GL, Tartaro A, Colosimo C (2007) New morphologic variants of the hand motor cortex as seen with MR imaging in a large study population. AJNR Am J Neuroradiol 28:1480–1485
D’Ostilio K and Garraux G (2010) Role of the medial frontal cortex in unconscious motor priming. Poster presented at the Warwick workshop on motor priming and cognitive control, University of Warwick, UK, 17–19 August 2010
Egner T (2007) Congruency sequence effects and cognitive control. Cogn Affect Behav Neurosci 7(4):380–390
Eimer M, Schlaghecken F (1998) Effects of masked stimuli on motor activation: behavioral and electrophysiological evidence. J Exp Psychol Hum Percept Perform 24:1737–1747
Eimer M, Schlaghecken F (2002) Links between conscious awareness and response inhibition: evidence from masked priming. Psychon Bull Rev 9:514–520
Eimer M, Schlaghecken F (2003) Response facilitation and inhibition in subliminal priming. Biol Psychol 64:7–26
Grèzes J, Decety J (2002) Does visual perception of object afford action? Evidence from a neuroimaging study. Neuropsychologia 40:212–222
Huber DE, Tian X, Curran T, O’Reilly RC, Woroch B (2008) The dynamics of integration and separation: ERP, MEG, and neural network studies of immediate repetition effects. J Exp Psychol Hum Percept Perform 34:1389–1416
Jaskowski P (2008a) Conscious contributions to subliminal priming. Conscious Cogn 17:72–83
Jaskowski P (2008b) The negative compatibility effect with nonmasking flankers: a case for mask-triggered inhibition. Conscious Cogn 17:765–777
Jaskowski P, Przekoracka-Krawczyk A (2005) On the role of mask structure in subliminal priming. Acta Neurobiol Exp 65:409–417
Jaskowski P, Bialunska A, Verleger R (2007) Mask- and distractor-triggered inhibitory processes in the priming of motor responses: an EEG study. Psychophysiology 45:70–85
Johansen-Berg H, Behrens TE, Robson MD, Drobnjak I, Rushworth MF, Brady JM, Smith SM, Higham DJ, Matthews PM (2004) Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. Proc Natl Acad Sci U S A 101:13335–13340
Kim JH, Lee JM, Jo HJ, Kim SH, Lee JH, Kim ST, Seo SW, Cox RW, Na DL, Kim SI, Saad ZS (2009) Defining functional SMA and pre-SMA subregions in human MFC using resting state fMRI: functional connectivity-based parcellation method. Neuroimage 49:2375–2386
Klapp ST (2005) Two versions of the negative compatibility effect: comment on Lleras and Enns (2004). J Exp Psychol Gen 134: 431–435; author reply 436–440
Klapp ST, Hinkley LB (2002) The negative compatibility effect: unconscious inhibition influences reaction time and response selection. J Exp Psychol Gen 131:255–269
Lehericy S, Ducros M, Krainik A, Francois C, van de Moortele PF, Ugurbil K, Kim DS (2004) 3-D diffusion tensor axonal tracking shows distinct SMA and pre-SMA projections to the human striatum. Cereb Cortex 14(12):1302–1309
Leuthold H, Kopp B (1998) Mechanisms of priming by masked stimuli: inferences from event-related potentials. Psychol Sci 9:263–269
Lleras A, Enns JT (2004) Negative compatibility or object updating? A cautionary tale of mask-dependent priming. J Exp Psychol Gen 133:475–493
Lleras A, Enns JT (2005) Updating a Cautionary Tale of Masked Priming: reply to Klapp (2005). J Exp Psychol Gen 134:436–440
Lleras A, Enns JT (2006) How much like a target can a mask be? Geometric, spatial, and temporal similarity in priming: a reply to Schlaghecken and Eimer (2006). J Exp Psychol Gen 135:495–500
Mazziotta J, Toga A, Evans A, Fox P, Lancaster J, Zilles K, Woods R, Paus T, Simpson G, Pike B, Holmes C, Collins L, Thompson P, MacDonald D, Iacoboni M, Schormann T, Amunts K, Palomero-Gallagher N, Geyer S, Parsons L, Narr K, Kabani N, Le Goualher G, Boomsma D, Cannon T, Kawashima R, Mazoyer B (2001) A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos Trans R Soc Lond B Biol Sci 356:1293–1322
Mitsis GD, Iannetti GD, Smart TS, Tracey I, Wise RG (2008) Regions of interest analysis in pharmacological fMRI: how do the definition criteria influence the inferred result? Neuroimage 40:121–132
Nachev P, Kennard C, Husain M (2008) Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 9:856–869
Nakamura K, Sakai K, Hikosaka O (1999) Effects of local inactivation of monkey medial frontal cortex in learning of sequential procedures. J Neurophysiol 82:1063–1068
Neumann O, Klotz W (1994) Motor responses to non-reportable, masked stimuli: Where is the limit of direct parameter specification? In: Umiltà C, Moskovitch M (eds) Attention and performance XV: conscious and nonconscious information processing. MIT Press, Cambridge, pp 123–150
Picard N, Strick PL (1996) Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex 6:342–353
Picard N, Strick PL (1997) Activation on the medial wall during remembered sequences of reaching movements in monkeys. J Neurophysiol 77:2197–2201
Picard N, Strick PL (2001) Imaging the premotor areas. Curr Opin Neurobiol 11:663–672
Picard N, Strick PL (2003) Activation of the supplementary motor area (SMA) during performance of visually guided movements. Cereb Cortex 13:977–986
Rizzolatti G, Luppino G, Matelli M (1996) The classic supplementary motor area is formed by two independent areas. Adv Neurol 70:45–56
Schlaghecken F, Eimer M (2002) Motor activation with and without inhibition: evidence for a threshold mechanism in motor control. Percept Psychophys 64:148–162
Schlaghecken F, Eimer M (2006) Active masks and active inhibition: a comment on Lleras and Enns (2004) and on Verleger, Jaskowski, Aydemir, van der Lubbe, and Groen (2004). J Exp Psychol Gen 135:484–494
Schlaghecken F, Maylor EA (2005) Motor control in old age: evidence of impaired low-level inhibition. J Gerontol B Psychol Sci Soc Sci 60:P158–P161
Schlaghecken F, Munchau A, Bloem BR, Rothwell J, Eimer M (2003) Slow frequency repetitive transcranial magnetic stimulation affects reaction times, but not priming effects, in a masked prime task. Clin Neurophysiol 114:1272–1277
Schlaghecken F, Blagrove E, Maylor EA (2006a) No difference between conscious and nonconscious visuomotor control: evidence from perceptual learning in the masked prime task. Conscious Cogn 17:84–93
Schlaghecken F, Bowman H, Eimer M (2006b) Dissociating local and global levels of perceptuo-motor control in masked priming. J Exp Psychol Hum Percept Perform 32:618–632
Seiss E, Praamstra P (2004) The basal ganglia and inhibitory mechanisms in response selection: evidence from subliminal priming of motor responses in Parkinson’s disease. Brain 127:330–339
Seiss E, Praamstra P (2006) Time-course of masked response priming and inhibition in Parkinson’s disease. Neuropsychologia 44:869–870
Shima K, Tanji J (1998) Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. J Neurophysiol 80:3247–3260
Sohrabi A, West RL, Smith AM (2005) An fMRI study of the effects of memory and goal setting in a risk taking task. In: 27th annual meeting of the cognitive science society, Stresa, Italy, p 2555
Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy R, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:208–219
Sumner P (2008) Mask-induced priming and the negative compatibility effect. Exp Psychol 55:133–141
Sumner P, Brandwood T (2008) Oscillations in motor priming: positive rebound follows inhibitory phase in the masked prime paradigm. J Mot Behav 40:484–489
Sumner P, Husain M (2008) At the edge of consciousness: automatic motor activation and voluntary control. Neuroscientist 14:474–486
Sumner P, Nachev P, Morris P, Peters AM, Jackson SR, Kennard C, Husain M (2007) Human medial frontal cortex mediates unconscious inhibition of voluntary action. Neuron 54:697–711
Tucker M, Ellis R (2004) Action priming by briefly presented objects. Acta Psychol (Amst) 116:185–203
Verleger R, Jaskowski P, Aydemir A, van der Lubbe RH, Groen M (2004) Qualitative differences between conscious and nonconscious processing? On inverse priming induced by masked arrows. J Exp Psychol Gen 133:494–515
Wager TD, Sylvester CY, Lacey SC, Nee DE, Franklin M, Jonides J (2005) Common and unique components of response inhibition revealed by fMRI. Neuroimage 27:323–340
Acknowledgments
This research was supported by the Welcome Trust and the Wales Institute of Cognitive Neuroscience (WICN). The authors wish to thank Richard Wise (Cardiff University Brain Research Imaging Center) for his expert advice on the data processing.
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Boy, F., Husain, M., Singh, K.D. et al. Supplementary motor area activations in unconscious inhibition of voluntary action. Exp Brain Res 206, 441–448 (2010). https://doi.org/10.1007/s00221-010-2417-x
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DOI: https://doi.org/10.1007/s00221-010-2417-x