Motor inhibitory control is a central executive function, but only recently the importance of perceptual mechanisms for these processes has been focused. It is elusive whether basic mechanisms governing sensory perception affect motor inhibitory control. We examine whether sensory lateral inhibition (LI) processes modulate motor inhibitory control using a system neurophysiological approach combining EEG signal decomposition with source localization methods in a somatosensory GO/NOGO task. The results show that inter-individual variations in the strength of LI effects predominantly affect processes when information needs to be integrated between cerebral hemispheres. If information needs to be integrated between hemispheres, strong sensory suppression will lead to more impulsive errors. Importantly, the neurophysiological data suggest that not purely perceptual or motor processes are affected. Rather, LI affects the response selection level and modulates processes of stimulus categorization. This is associated with activity modulations in the posterior parietal cortex. The results suggest that when sensory suppression is high and when information needs to be integrated across hemispheres, these processes are less efficient, which likely leads to worse motor inhibitory control. The results show how basis principles modulating perceptual processes affect subsequent motor inhibitory control processes.

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

Experimental Neurobiology National Institute of Mental Health Klecany Czech Republic

MS Centre Dresden Faculty of Medicine of the TU Dresden TU Dresden Germany

Zobrazit více v PubMed

Diamond A. Executive functions. Annu. Rev. Psychol. 2013;64:135–168. doi: 10.1146/annurev-psych-113011-143750. PubMed DOI PMC

Bari A, Robbins TW. Inhibition and impulsivity: behavioral and neural basis of response control. Prog. Neurobiol. 2013;108:44–79. doi: 10.1016/j.pneurobio.2013.06.005. PubMed DOI

Chmielewski WX, Mückschel M, Stock A-K, Beste C. The impact of mental workload on inhibitory control subprocesses. NeuroImage. 2015;112:96–104. doi: 10.1016/j.neuroimage.2015.02.060. PubMed DOI

Boehler CN, et al. Sensory MEG responses predict successful and failed inhibition in a stop-signal task. Cereb. Cortex N. Y. N 1991. 2009;19:134–145. PubMed

Chmielewski WX, Beste C. Perceptual conflict during sensorimotor integration processes - a neurophysiological study in response inhibition. Sci. Rep. 2016;6:26289. doi: 10.1038/srep26289. PubMed DOI PMC

Chmielewski, W. X. & Beste, C. Testing interactive effects of automatic and conflict control processes during response inhibition - A system neurophysiological study. NeuroImage, doi:10.1016/j.neuroimage.2016.10.015 (2016). PubMed

Stock A-K, Popescu F, Neuhaus AH, Beste C. Single-subject prediction of response inhibition behavior by event-related potentials. J. Neurophysiol. 2016;115:1252–1262. doi: 10.1152/jn.00969.2015. PubMed DOI PMC

Cardini F, Longo MR, Haggard P. Vision of the body modulates somatosensory intracortical inhibition. Cereb. Cortex N. Y. N 1991. 2011;21:2014–2022. PubMed

Jerath R, Cearley SM, Barnes VA, Nixon-Shapiro E. How lateral inhibition and fast retinogeniculo-cortical oscillations create vision: A new hypothesis. Med. Hypotheses. 2016;96:20–29. doi: 10.1016/j.mehy.2016.09.015. PubMed DOI

Urban NN. Lateral inhibition in the olfactory bulb and in olfaction. Physiol. Behav. 2002;77:607–612. doi: 10.1016/S0031-9384(02)00895-8. PubMed DOI

Bodmer B, Beste C. On the dependence of response inhibition processes on sensory modality: Response Inhibition Processes and Sensory Modality. Hum. Brain Mapp. 2017;38:1941–1951. doi: 10.1002/hbm.23495. PubMed DOI PMC

Pang CY, Mueller MM. Competitive interactions in somatosensory cortex for concurrent vibrotactile stimulation between and within hands. Biol. Psychol. 2015;110:91–99. doi: 10.1016/j.biopsycho.2015.07.002. PubMed DOI

Severens M, Farquhar J, Desain P, Duysens J, Gielen C. Transient and steady-state responses to mechanical stimulation of different fingers reveal interactions based on lateral inhibition. Clin. Neurophysiol. Off. J. Int. Fed. Clin. Neurophysiol. 2010;121:2090–2096. doi: 10.1016/j.clinph.2010.05.016. PubMed DOI

Hoechstetter K, et al. Interaction of Tactile Input in the Human Primary and Secondary Somatosensory Cortex–A Magnetoencephalographic Study. NeuroImage. 2001;14:759–767. doi: 10.1006/nimg.2001.0855. PubMed DOI

Ishibashi H, et al. Differential interaction of somatosensory inputs in the human primary sensory cortex: a magnetoencephalographic study. Clin. Neurophysiol. Off. J. Int. Fed. Clin. Neurophysiol. 2000;111:1095–1102. doi: 10.1016/S1388-2457(00)00266-2. PubMed DOI

Tanosaki M, et al. Neural mechanisms for generation of tactile interference effects on somatosensory evoked magnetic fields in humans. Clin. Neurophysiol. Off. J. Int. Fed. Clin. Neurophysiol. 2002;113:672–680. doi: 10.1016/S1388-2457(02)00052-4. PubMed DOI

Dippel, G., Chmielewski, W., Mückschel, M. & Beste, C. Response mode-dependent differences in neurofunctional networks during response inhibition: an EEG-beamforming study. Brain Struct. Funct. doi:10.1007/s00429-015-1148-y (2015). PubMed

Quetscher C, et al. Striatal GABA-MRS predicts response inhibition performance and its cortical electrophysiological correlates. Brain Struct. Funct. 2015;220:3555–3564. doi: 10.1007/s00429-014-0873-y. PubMed DOI PMC

Beste, C., Stock, A.-K., Epplen, J. T. & Arning, L. Dissociable electrophysiological subprocesses during response inhibition are differentially modulated by dopamine D1 and D2 receptors. Eur. Neuropsychopharmacol. J. Eur. Coll. Neuropsychopharmacol. doi:10.1016/j.euroneuro.2016.03.002 (2016). PubMed

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

Ouyang G, Sommer W, Zhou C. Updating and validating a new framework for restoring and analyzing latency-variable ERP components from single trials with residue iteration decomposition (RIDE) Psychophysiology. 2015;52:839–856. doi: 10.1111/psyp.12411. PubMed DOI

Ouyang G, Schacht A, Zhou C, Sommer W. Overcoming limitations of the ERP method with Residue Iteration Decomposition (RIDE): A demonstration in go/no-go experiments. Psychophysiology. 2013;50:253–265. doi: 10.1111/psyp.12004. PubMed DOI

Ouyang G, Herzmann G, Zhou C, Sommer W. Residue iteration decomposition (RIDE): A new method to separate ERP components on the basis of latency variability in single trials. Psychophysiology. 2011;48:1631–1647. doi: 10.1111/j.1469-8986.2011.01269.x. PubMed DOI

Wolff, N., Mückschel, M. & Beste, C. Neural mechanisms and functional neuroanatomical networks during memory and cue-based task switching as revealed by residue iteration decomposition (RIDE) based source localization. Brain Struct. Funct. doi:10.1007/s00429-017-1437-8 (2017). PubMed

Mückschel M, Chmielewski W, Ziemssen T, Beste C. The norepinephrine system shows information-content specific properties during cognitive control - Evidence from EEG and pupillary responses. NeuroImage. 2017;149:44–52. doi: 10.1016/j.neuroimage.2017.01.036. PubMed DOI

Verleger R, Metzner MF, Ouyang G, Śmigasiewicz K, Zhou C. Testing the stimulus-to-response bridging function of the oddball-P3 by delayed response signals and residue iteration decomposition (RIDE) NeuroImage. 2014;100:271–280. doi: 10.1016/j.neuroimage.2014.06.036. PubMed DOI

Mückschel, M., Gohil, K., Ziemssen, T. & Beste, C. The norepinephrine system and its relevance for multi-component behavior. NeuroImage doi:10.1016/j.neuroimage.2016.10.007 (2016). PubMed

Wessel JR, Aron AR. It’s not too late: the onset of the frontocentral P3 indexes successful response inhibition in the stop-signal paradigm. Psychophysiology. 2015;52:472–480. doi: 10.1111/psyp.12374. PubMed DOI PMC

Andersen RA, Buneo CA. Intentional maps in posterior parietal cortex. Annu. Rev. Neurosci. 2002;25:189–220. doi: 10.1146/annurev.neuro.25.112701.142922. PubMed DOI

Gottlieb J. From thought to action: the parietal cortex as a bridge between perception, action, and cognition. Neuron. 2007;53:9–16. doi: 10.1016/j.neuron.2006.12.009. PubMed DOI

Fokin VA, et al. Localization of human cortical areas activated on perception of ordered and chaotic images. Neurosci. Behav. Physiol. 2008;38:677–685. doi: 10.1007/s11055-008-9033-2. PubMed DOI

Ocklenburg S, Güntürkün O, Beste C. Lateralized neural mechanisms underlying the modulation of response inhibition processes. NeuroImage. 2011;55:1771–1778. doi: 10.1016/j.neuroimage.2011.01.035. PubMed DOI

Takeichi H, et al. Comprehension of degraded speech sounds with m-sequence modulation: an fMRI study. NeuroImage. 2010;49:2697–2706. doi: 10.1016/j.neuroimage.2009.10.063. PubMed DOI

Borich MR, Brodie SM, Gray WA, Ionta S, Boyd LA. Understanding the role of the primary somatosensory cortex: Opportunities for rehabilitation. Neuropsychologia. 2015;79:246–255. doi: 10.1016/j.neuropsychologia.2015.07.007. PubMed DOI PMC

Ouyang G, Sommer W, Zhou C. A toolbox for residue iteration decomposition (RIDE)–A method for the decomposition, reconstruction, and single trial analysis of event related potentials. J. Neurosci. Methods. 2015;250:7–21. doi: 10.1016/j.jneumeth.2014.10.009. PubMed DOI

Barber AD, Caffo BS, Pekar JJ, Mostofsky SH. Developmental changes in within- and between-network connectivity between late childhood and adulthood. Neuropsychologia. 2013;51:156–167. doi: 10.1016/j.neuropsychologia.2012.11.011. PubMed DOI PMC

Fan L-Y, Gau SS-F, Chou T-L. Neural correlates of inhibitory control and visual processing in youths with attention deficit hyperactivity disorder: a counting Stroop functional MRI study. Psychol. Med. 2014;44:2661–2671. doi: 10.1017/S0033291714000038. PubMed DOI

Aron AR, Robbins TW, Poldrack RA. Inhibition and the right inferior frontal cortex: one decade on. Trends Cogn. Sci. 2014;18:177–185. doi: 10.1016/j.tics.2013.12.003. PubMed DOI

Yeterian EH, Pandya DN, Tomaiuolo F, Petrides M. The cortical connectivity of the prefrontal cortex in the monkey brain. Cortex. 2012;48:58–81. doi: 10.1016/j.cortex.2011.03.004. PubMed DOI PMC

Kaas JH. The functional organization of somatosensory cortex in primates. Ann. Anat. - Anat. Anz. 1993;175:509–518. doi: 10.1016/S0940-9602(11)80212-8. PubMed DOI

Ackerley R, Kavounoudias A. The role of tactile afference in shaping motor behaviour and implications for prosthetic innovation. Neuropsychologia. 2015;79:192–205. doi: 10.1016/j.neuropsychologia.2015.06.024. PubMed DOI

Francis ST, et al. fMRI of the Responses to Vibratory Stimulation of Digit Tips. NeuroImage. 2000;11:188–202. doi: 10.1006/nimg.2000.0541. PubMed DOI

Harrington GS, Hunter Downs J., III FMRI mapping of the somatosensory cortex with vibratory stimuli. Brain Res. 2001;897:188–192. doi: 10.1016/S0006-8993(01)02139-4. PubMed DOI

Dieckhöfer A, et al. Transcranial direct current stimulation applied over the somatosensory cortex – Differential effect on low and high frequency SEPs. Clin. Neurophysiol. 2006;117:2221–2227. doi: 10.1016/j.clinph.2006.07.136. PubMed DOI

Vaseghi B, Zoghi M, Jaberzadeh S. Differential effects of cathodal transcranial direct current stimulation of prefrontal, motor and somatosensory cortices on cortical excitability and pain perception - a double-blind randomised sham-controlled study. Eur. J. Neurosci. 2015;42:2426–2437. doi: 10.1111/ejn.13043. PubMed DOI

Hilgenstock R, Weiss T, Huonker R, Witte OW. Behavioural and neurofunctional impact of transcranial direct current stimulation on somatosensory learning: tDCS and Somatosensory Learning. Hum. Brain Mapp. 2016;37:1277–1295. doi: 10.1002/hbm.23101. PubMed DOI PMC

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

Tenke CE, Kayser J. Generator localization by current source density (CSD): Implications of volume conduction and field closure at intracranial and scalp resolutions. Clin. Neurophysiol. 2012;123:2328–2345. doi: 10.1016/j.clinph.2012.06.005. PubMed DOI PMC

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

Marco-Pallarés J, Grau C, Ruffini G. Combined ICA-LORETA analysis of mismatch negativity. NeuroImage. 2005;25:471–477. doi: 10.1016/j.neuroimage.2004.11.028. PubMed DOI

Sekihara K, Sahani M, Nagarajan SS. Localization bias and spatial resolution of adaptive and non-adaptive spatial filters for MEG source reconstruction. NeuroImage. 2005;25:1056–1067. doi: 10.1016/j.neuroimage.2004.11.051. PubMed DOI PMC

Fuchs M, Kastner J, Wagner M, Hawes S, Ebersole JS. A standardized boundary element method volume conductor model. Clin. Neurophysiol. Off. J. Int. Fed. Clin. Neurophysiol. 2002;113:702–712. doi: 10.1016/S1388-2457(02)00030-5. PubMed DOI

Mazziotta J, et al. A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM) Philos. Trans. R. Soc. Lond. Ser. B. 2001;356:1293–1322. doi: 10.1098/rstb.2001.0915. PubMed DOI PMC

Dippel G, Beste C. A causal role of the right inferior frontal cortex in implementing strategies for multi-component behaviour. Nat. Commun. 2015;6:6587. doi: 10.1038/ncomms7587. PubMed DOI