The ability to inhibit responses is a central sensorimotor function but only recently the importance of sensory processes for motor inhibition mechanisms went more into the research focus. In this regard it is elusive, whether there are differences between sensory modalities to trigger response inhibition processes. Due to functional neuroanatomical considerations strong differences may exist, for example, between the visual and the tactile modality. In the current study we examine what neurophysiological mechanisms as well as functional neuroanatomical networks are modulated during response inhibition. Therefore, a Go/NoGo-paradigm employing a novel combination of visual, tactile, and visuotactile stimuli was used. The data show that the tactile modality is more powerful than the visual modality to trigger response inhibition processes. However, the tactile modality loses its efficacy to trigger response inhibition processes when being combined with the visual modality. This may be due to competitive mechanisms leading to a suppression of certain sensory stimuli and the response selection level. Variations in sensory modalities specifically affected conflict monitoring processes during response inhibition by modulating activity in a frontal parietal network including the right inferior frontal gyrus, anterior cingulate cortex and the temporoparietal junction. Attentional selection processes are not modulated. The results suggest that the functional neuroanatomical networks involved in response inhibition critically depends on the nature of the sensory input. Hum Brain Mapp 38:1941-1951, 2017. © 2017 Wiley Periodicals, Inc.

Department of Child and Adolescent Psychiatry Cognitive Neurophysiology Faculty of Medicine of the TU Dresden Germnay

Experimental Neurobiology National Institute of Mental Health Klecany Czech Republic

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Andersen RA, Buneo CA (2002): Intentional maps in posterior parietal cortex. Annu Rev Neurosci 25:189–220. PubMed

Aron AR, Robbins TW, Poldrack RA (2004): Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170–177. PubMed

Bari A, Robbins TW (2013): Inhibition and impulsivity: behavioral and neural basis of response control. Prog Neurobiol 108:44–79. PubMed

Beste C, Dziobek I, Hielscher H, Willemssen R, Falkenstein M (2009): Effects of stimulus‐response compatibility on inhibitory processes in Parkinson's disease. Eur J Neurosci 29:855–860. PubMed

Beste C, Ness V, Falkenstein M, Saft C (2011): On the role of fronto‐striatal neural synchronization processes for response inhibition–evidence from ERP phase‐synchronization analyses in pre‐manifest Huntington's disease gene mutation carriers. Neuropsychologia 49:3484–3493. PubMed

Beste C, Stock A‐K, Epplen JT, Arning L (2016): Dissociable electrophysiological subprocesses during response inhibition are differentially modulated by dopamine D1 and D2 receptors. Eur Neuropsychopharmacol 26:1029‐1036. PubMed

Beste C, Willemssen R, Saft C, Falkenstein M (2010): Response inhibition subprocesses and dopaminergic pathways: Basal ganglia disease effects. Neuropsychologia 48:366–373. PubMed

Bohlhalter S, Goldfine A, Matteson S, Garraux G, Hanakawa T, Kansaku K, Wurzmann R, Hallett M (2006): Neural correlates of tic generation in Tourette syndrome: An event‐related functional MRI study. Brain 129:2029–2037. PubMed

Bonnefond A, Doignon‐Camus N, Touzalin‐Chretien P, Dufour A (2010): Vigilance and intrinsic maintenance of alert state: An ERP study. Behav Brain Res 211:185–190. PubMed

Borich MR, Brodie SM, Gray WA, Ionta S, Boyd LA (2015): Understanding the role of the primary somatosensory cortex: Opportunities for rehabilitation. Neuropsychologia 79:246–255. PubMed PMC

Cavina‐Pratesi C, Bricolo E, Prior M, Marzi CA (2001): Redundancy gain in the stop‐signal paradigm: implications for the locus of coactivation in simple reaction time. J Exp Psychol Hum Percept Perform 27:932–941. PubMed

Chmielewski WX, Mückschel M, Dippel G, Beste C (2015): Concurrent information affects response inhibition processes via the modulation of theta oscillations in cognitive control networks. Brain Struct Funct 221:3949–3961. PubMed

Coizet V, Graham JH, Moss J, Bolam JP, Savasta M, McHaffie JG, Redgrave P, Overton PG (2009): Short‐latency visual input to the subthalamic nucleus is provided by the midbrain superior colliculus. J Neurosci 29:5701–5709. PubMed PMC

Desimone R, Duncan J (1995): Neural mechanisms of selective visual attention. Annu Rev Neurosci 18:193–222. PubMed

Diamond A (2013): Executive functions. Annu Rev Psychol 64:135–168. PubMed PMC

Dippel G, Beste C (2015): A causal role of the right inferior frontal cortex in implementing strategies for multi‐component behaviour. Nat Commun 6:6587. PubMed

Dippel G, Chmielewski W, Mückschel M, Beste C (2016): Response mode‐dependent differences in neurofunctional networks during response inhibition: an EEG‐beamforming study. Brain Struct Funct 221:4091–4101. PubMed

Driver J, Noesselt T (2008): Multisensory interplay reveals crossmodal influences on “sensory‐specific” brain regions, neural responses, and judgments. Neuron 57:11–23. PubMed PMC

Fang P‐C, Stepniewska I, Kaas JH (2005): Ipsilateral cortical connections of motor, premotor, frontal eye, and posterior parietal fields in a prosimian primate, Otolemur garnetti. J Comp Neurol 490:305–333. PubMed

Fuchs M, Kastner J, Wagner M, Hawes S, Ebersole JS (2002): A standardized boundary element method volume conductor model. Clin Neurophysiol off J Int Fed Clin Neurophysiol 113:702–712. PubMed

Geng JJ, Vossel S (2013): Re‐evaluating the role of TPJ in attentional control: contextual updating?. Neurosci Biobehav Rev 37:2608–2620. PubMed PMC

Gondan M, Götze C, Greenlee MW (2010): Redundancy gains in simple responses and go/no‐go tasks. Atten Percept Psychophys 72:1692–1709. PubMed

Hagmann R, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O (2008): Mapping the structural core of the human cerebral cortex. PLoS Biol 6:e159. PubMed PMC

Huster RJ, Enriquez‐Geppert S, Lavallee CF, Falkenstein M, Herrmann CS (2013): Electroencephalography of response inhibition tasks: functional networks and cognitive contributions. Int J Psychophysiol off J Int Organ Psychophysiol 87:217–233. PubMed

Huster RJ, Westerhausen R, Pantev C, Konrad C (2010): The role of the cingulate cortex as neural generator of the N200 and P300 in a tactile response inhibition task. Hum Brain Mapp 31:1260–1271. PubMed PMC

Kropotov JD, Ponomarev VA, Hollup S, Mueller A (2011): Dissociating action inhibition, conflict monitoring and sensory mismatch into independent components of event related potentials in GO/NOGO task. Neuroimage 57:565–575. PubMed

Labrenz F, Themann M, Wascher E, Beste C, Pfleiderer B (2012): Neural correlates of individual performance differences in resolving perceptual conflict. PLoS One 7:e42849. PubMed PMC

Luppino G, Matelli M, Camarda R, Rizzolatti G (1993): Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey. J Comp Neurol 338:114–140. PubMed

Marco‐Pallarés J, Grau C, Ruffini G (2005): Combined ICA‐LORETA analysis of mismatch negativity. Neuroimage 25:471–477. PubMed

Miller J, Kühlwein E, Ulrich R (2004): Effects of redundant visual stimuli on temporal order judgments. Percept Psychophys 66:563–573. PubMed

Mückschel M, Stock A‐K, Beste C (2014): Psychophysiological mechanisms of interindividual differences in goal activation modes during action cascading. Cereb Cortex (NY, 1991) 24:2120–2129. PubMed

Nieuwenhuis S, Yeung N, Cohen JD (2004): Stimulus modality, perceptual overlap, and the go/no‐go N2. Psychophysiology 41:157–160. PubMed

Nunez PL, Pilgreen KL (1991): The spline‐Laplacian in clinical neurophysiology: A method to improve EEG spatial resolution. J Clin Neurophysiol Off Publ Am Electroencephalogr Soc 8:397–413. PubMed

Pandey AK, Kamarajan C, Tang Y, Chorlian DB, Roopesh BN, Manz N, Stimus A, Rangaswamy M, Porjesz B (2012): Neurocognitive deficits in male alcoholics: an ERP/sLORETA analysis of the N2 component in an equal probability Go/NoGo task. Biol Psychol 89:170–182. PubMed PMC

Pascual‐Marqui RD (2002): Standardized low‐resolution brain electromagnetic tomography (sLORETA): Technical details. Methods Find Exp Clin Pharmacol 24(Suppl D):5–12. PubMed

Redgrave P, Coizet V, Comoli E, McHaffie JG, Leriche M, Vautrelle N, Hayes LM, Overton P (2010): Interactions between the midbrain superior colliculus and the basal ganglia. Front Neuroanat 4:132. PubMed PMC

Rushworth MFS, Walton ME, Kennerley SW, Bannerman DM (2004): Action sets and decisions in the medial frontal cortex. Trends Cogn Sci 8:410–417. PubMed

Sekihara K, Sahani M, Nagarajan SS (2005): Localization bias and spatial resolution of adaptive and non‐adaptive spatial filters for MEG source reconstruction. Neuroimage 25:1056–1067. PubMed PMC

Shedden JM, Reid GS (2001): A variable mapping task produces symmetrical interference between global information and local information. Percept Psychophys 63:241–252. PubMed

Staub B, Doignon‐Camus N, Bacon É, Bonnefond A (2014): The effects of aging on sustained attention ability: an ERP study. Psychol Aging 29:684–695. PubMed

Stock A‐K, Popescu F, Neuhaus AH, Beste C (2015): Single‐subject prediction of response inhibition behavior by event‐related potentials. J Neurophysiol 115:1252–1262. PubMed PMC

Verbruggen F, Liefooghe B, Vandierendonck A (2006): The effect of interference in the early processing stages on response inhibition in the stop signal task. Q J Exp Psychol 59:190–203. PubMed

Wessel JR, Aron AR (2015): It's not too late: The onset of the frontocentral P3 indexes successful response inhibition in the stop‐signal paradigm. Psychophysiology 52:472–480. PubMed PMC

Westerhausen R, Moosmann M, Alho K, Belsby S‐O, Hämäläinen H, Medvedev S, Specht K, Hugdahl K (2010): Identification of attention and cognitive control networks in a parametric auditory fMRI study. Neuropsychologia 48:2075–2081. PubMed

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