Top

Published in:

01-06-2019 | Original Article

Neuronal networks underlying the conjoint modulation of response selection by subliminal and consciously induced cognitive conflicts

Authors: Wiebke Bensmann, Nicolas Zink, Moritz Mückschel, Christian Beste, Ann-Kathrin Stock

Published in: Brain Structure and Function | Issue 5/2019

Abstract

Goal-directed behavior has been shown to be affected by consciously and subliminally induced conflicts. Both types of conflict conjointly modulate behavioral performance, but the underlying neuronal mechanisms have remained unclear. While cognitive control is linked to oscillations in the theta frequency band, there are several mechanisms via which theta oscillations may enable cognitive control: via the coordination and synchronization of a large and complex neuronal network and/or via local processes within the medial frontal cortex. We, therefore, investigated this issue with a focus on theta oscillations and the underlying neuronal networks. For this purpose, n = 40 healthy young participants performed a conflict paradigm that combines conscious and subliminal distractors while an EEG was recorded. The data show that separate processes modulate the theta-based activation and organization of cognitive control networks: EEG beamforming analyses showed that variations in theta band power generated in the supplementary motor area reflected the need for control and task-relevant goal shielding, as both conflicts as well as their conjoint effect on behavior increased theta power. Yet, large networks were not modulated by this and graph theoretical analyses of the efficiency (i.e. small worldness) of theta-driven networks did not reflect the need for control. Instead, theta network efficiency was decreased by subliminal conflicts only. This dissociation suggests that while both kinds of conflict require control and goal shielding, which are induced by an increase in theta band power and modulate processes in the medial frontal cortex, only non-conscious conflicts diminish the efficiency of theta-driven large-scale networks.

Available only for authorised users

Achard S, Bullmore E (2007) Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3:e17. https://doi.org/10.1371/journal.pcbi.0030017 CrossRefPubMedPubMedCentral

Bassett DS, Bullmore E (2006) Small-world brain networks. Neuroscientist 12:512–523. https://doi.org/10.1177/1073858406293182 CrossRefPubMed

Battaglia-Mayer A, Babicola L, Satta E (2016) Parieto-frontal gradients and domains underlying eye and hand operations in the action space. Neuroscience 334:76–92. https://doi.org/10.1016/j.neuroscience.2016.07.009 CrossRefPubMed

Bauer M, Oostenveld R, Peeters M, Fries P (2006) Tactile spatial attention enhances gamma-band activity in somatosensory cortex and reduces low-frequency activity in parieto-occipital areas. J Neurosci Off J Soc Neurosci 26:490–501. https://doi.org/10.1523/JNEUROSCI.5228-04.2006 CrossRef

Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300

Beste C, Willemssen R, Saft C, Falkenstein M (2010) Response inhibition subprocesses and dopaminergic pathways: basal ganglia disease effects. Neuropsychologia 48:366–373. https://doi.org/10.1016/j.neuropsychologia.2009.09.023 CrossRefPubMed

Beste C, Ness V, Lukas C et al (2012) Mechanisms mediating parallel action monitoring in fronto-striatal circuits. NeuroImage 62:137–146. https://doi.org/10.1016/j.neuroimage.2012.05.019 CrossRefPubMed

Beste C, Mückschel M, Rosales R et al (2017) The basal ganglia striosomes affect the modulation of conflicts by subliminal information-evidence from X-linked dystonia parkinsonism. Cereb Cortex 1991:1–10. https://doi.org/10.1093/cercor/bhx125 CrossRef

Bielczyk NZ, Walocha F, Ebel PW et al (2018) Thresholding functional connectomes by means of mixture modeling. NeuroImage 171:402–414. https://doi.org/10.1016/j.neuroimage.2018.01.003 CrossRefPubMedPubMedCentral

Botvinick MM, Braver TS, Barch DM et al (2001) Conflict monitoring and cognitive control. Psychol Rev 108:624–652CrossRefPubMed

Boy F, Husain M, Sumner P (2010) Unconscious inhibition separates two forms of cognitive control. Proc Natl Acad Sci 107:11134–11139. https://doi.org/10.1073/pnas.1001925107 CrossRefPubMed

Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198. https://doi.org/10.1038/nrn2575 CrossRefPubMed

Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929. https://doi.org/10.1126/science.1099745 CrossRefPubMed

Cavanagh JF, Frank MJ (2014) Frontal theta as a mechanism for cognitive control. Trends Cogn Sci 18:414–421. https://doi.org/10.1016/j.tics.2014.04.012 CrossRefPubMedPubMedCentral

Cavanagh JF, Zambrano-Vazquez L, Allen JJB (2012) Theta lingua franca: a common mid-frontal substrate for action monitoring processes. Psychophysiology 49:220–238. https://doi.org/10.1111/j.1469-8986.2011.01293.x CrossRefPubMed

Chmielewski WX, Mückschel M, Dippel G, Beste C (2016) Concurrent information affects response inhibition processes via the modulation of theta oscillations in cognitive control networks. Brain Struct Funct 221:3949–3961. https://doi.org/10.1007/s00429-015-1137-1 CrossRefPubMed

Cohen MX (2014) A neural microcircuit for cognitive conflict detection and signaling. Trends Neurosci 37:480–490. https://doi.org/10.1016/j.tins.2014.06.004 CrossRefPubMed

Cohen MX, Donner TH (2013) Midfrontal conflict-related theta-band power reflects neural oscillations that predict behavior. J Neurophysiol 110:2752–2763. https://doi.org/10.1152/jn.00479.2013 CrossRefPubMed

Colebatch JG (2007) Bereitschaftspotential and movement-related potentials: origin, significance, and application in disorders of human movement. Mov Disord 22:601–610. https://doi.org/10.1002/mds.21323 CrossRefPubMed

De Blasio FM, Barry RJ (2013) Prestimulus delta and theta determinants of ERP responses in the Go/NoGo task. Int J Psychophysiol Off J Int Organ Psychophysiol 87:279–288. https://doi.org/10.1016/j.ijpsycho.2012.09.016 CrossRef

Deecke L, Kornhuber HH (1978) An electrical sign of participation of the mesial ‘supplementary’ motor cortex in human voluntary finger movement. Brain Res 159:473–476. https://doi.org/10.1016/0006-8993(78)90561-9 CrossRefPubMed

Diamond A (2013) Executive functions. Annu Rev Psychol 64:135–168. https://doi.org/10.1146/annurev-psych-113011-143750 CrossRefPubMed

Eimer M, Schlaghecken F (2003) Response facilitation and inhibition in subliminal priming. Biol Psychol 64:7–26. https://doi.org/10.1016/S0301-0511(03)00100-5 CrossRefPubMed

Evans AC, Collins DL, Milner B, Milner B (1992) An MRI-based stereotactic atlas from 250 young normal subjects. Soc Neurosci Abstr 18:408

Fassbender C, Hester R, Murphy K et al (2009) Prefrontal and midline interactions mediating behavioural control. Eur J Neurosci 29:181–187. https://doi.org/10.1111/j.1460-9568.2008.06557.x CrossRefPubMedPubMedCentral

Gohil K, Bluschke A, Roessner V et al (2017) ADHD patients fail to maintain task goals in face of subliminally and consciously induced cognitive conflicts. Psychol Med 47:1771–1783. https://doi.org/10.1017/s0033291717000216 CrossRefPubMed

Goschke T, Bolte A (2014) Emotional modulation of control dilemmas: the role of positive affect, reward, and dopamine in cognitive stability and flexibility. Neuropsychologia 62:403–423. https://doi.org/10.1016/j.neuropsychologia.2014.07.015 CrossRefPubMed

Goschke T, Dreisbach G (2008) Conflict-triggered goal shielding: response conflicts attenuate background monitoring for prospective memory cues. Psychol Sci 19:25–32. https://doi.org/10.1111/j.1467-9280.2008.02042.x CrossRefPubMed

Gross J, Kujala J, Hamalainen M et al (2001) Dynamic imaging of coherent sources: studying neural interactions in the human brain. Proc Natl Acad Sci 98:694–699. https://doi.org/10.1073/pnas.98.2.694 CrossRefPubMed

Halsband U, Matsuzaka Y, Tanji J (1994) Neuronal activity in the primate supplementary, pre-supplementary and premotor cortex during externally and internally instructed sequential movements. Neurosci Res 20:149–155. https://doi.org/10.1016/0168-0102(94)90032-9 CrossRefPubMed

Hampshire A, Sharp DJ (2015) Contrasting network and modular perspectives on inhibitory control. Trends Cogn Sci 19:445–452. https://doi.org/10.1016/j.tics.2015.06.006 CrossRefPubMed

Harper J, Malone SM, Bernat EM (2014) Theta and delta band activity explain N2 and P3 ERP component activity in a go/no-go task. Clin Neurophysiol Off J Int Fed Clin Neurophysiol 125:124–132. https://doi.org/10.1016/j.clinph.2013.06.025 CrossRef

Hoogenboom N, Schoffelen J-M, Oostenveld R et al (2006) Localizing human visual gamma-band activity in frequency, time and space. NeuroImage 29:764–773. https://doi.org/10.1016/j.neuroimage.2005.08.043 CrossRefPubMed

Jin S-H, Lin P, Hallett M (2012) Reorganization of brain functional small-world networks during finger movements. Hum Brain Mapp 33:861–872. https://doi.org/10.1002/hbm.21253 CrossRefPubMed

Keller I, Heckhausen H (1990) Readiness potentials preceding spontaneous motor acts: voluntary vs. involuntary control. Electroencephalogr Clin Neurophysiol 76:351–361CrossRefPubMed

Keye D, Wilhelm O, Oberauer K, Stürmer B (2013) Individual differences in response conflict adaptations. Front Psychol 4:947. https://doi.org/10.3389/fpsyg.2013.00947 CrossRefPubMedPubMedCentral

Langer N, von Bastian CC, Wirz H et al (2013) The effects of working memory training on functional brain network efficiency. Cortex 49:2424–2438. https://doi.org/10.1016/j.cortex.2013.01.008 CrossRefPubMed

Li Y, Chen Y, Lv X et al (2015) EEG functional network properties related to visually induced unrecognized spatial disorientation. Biomed Mater Eng 26:S1115–S1124. https://doi.org/10.3233/BME-151408 CrossRefPubMed

Maris E, Oostenveld R (2007) Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 164:177–190. https://doi.org/10.1016/j.jneumeth.2007.03.024 CrossRefPubMed

Masson MEJ (2011) A tutorial on a practical Bayesian alternative to null-hypothesis significance testing. Behav Res Methods 43:679–690. https://doi.org/10.3758/s13428-010-0049-5 CrossRefPubMed

Matsuzaka Y, Aizawa H, Tanji J (1992) A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: neuronal activity during a learned motor task. J Neurophysiol 68:653–662CrossRefPubMed

McBride J, Boy F, Husain M, Sumner P (2012) Automatic motor activation in the executive control of action. Front Hum Neurosci 6:82. https://doi.org/10.3389/fnhum.2012.00082 CrossRefPubMedPubMedCentral

Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202. https://doi.org/10.1146/annurev.neuro.24.1.167 CrossRefPubMed

Mückschel M, Stock A-K, Dippel G et al (2016) Interacting sources of interference during sensorimotor integration processes. NeuroImage 125:342–349. https://doi.org/10.1016/j.neuroimage.2015.09.075 CrossRefPubMed

Nolte G, Bai O, Wheaton L et al (2004) Identifying true brain interaction from EEG data using the imaginary part of coherency. Clin Neurophysiol 115:2292–2307. https://doi.org/10.1016/j.clinph.2004.04.029 CrossRefPubMed

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

O’Connell RG, Dockree PM, Bellgrove MA et al (2007) The role of cingulate cortex in the detection of errors with and without awareness: a high-density electrical mapping study: error awareness. Eur J Neurosci 25:2571–2579. https://doi.org/10.1111/j.1460-9568.2007.05477.x CrossRefPubMed

Oostenveld R, Stegeman DF, Praamstra P, van Oosterom A (2003) Brain symmetry and topographic analysis of lateralized event-related potentials. Clin Neurophysiol Off J Int Fed Clin Neurophysiol 114:1194–1202CrossRef

Oostenveld R, Fries P, Maris E, Schoffelen J-M (2011) FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:156869. https://doi.org/10.1155/2011/156869 CrossRefPubMed

Parkinson J, Haggard P (2014) Subliminal priming of intentional inhibition. Cognition 130:255–265. https://doi.org/10.1016/j.cognition.2013.11.005 CrossRefPubMed

Perrin F, Pernier J, Bertrand O, Echallier JF (1989) Spherical splines for scalp potential and current density mapping. Electroencephalogr Clin Neurophysiol 72:184–187CrossRefPubMed

Picard N (2003) Activation of the supplementary motor area (SMA) during performance of visually guided movements. Cereb Cortex 13:977–986. https://doi.org/10.1093/cercor/13.9.977 CrossRefPubMed

Roland PE, Larsen B, Lassen NA, Skinhøj E (1980a) Supplementary motor area and other cortical areas in organization of voluntary movements in man. J Neurophysiol 43:118–136CrossRefPubMed

Roland PE, Skinhøj E, Lassen NA, Larsen B (1980b) Different cortical areas in man in organization of voluntary movements in extrapersonal space. J Neurophysiol 43:137–150CrossRefPubMed

Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. NeuroImage 52:1059–1069. https://doi.org/10.1016/j.neuroimage.2009.10.003 CrossRefPubMed

Salvador R, Suckling J, Coleman MR et al (2005) Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb Cortex 15:1332–1342. https://doi.org/10.1093/cercor/bhi016 CrossRefPubMed

Schiffer A-M, Waszak F, Yeung N (2015) The role of prediction and outcomes in adaptive cognitive control. J Physiol-Paris 109:38–52. https://doi.org/10.1016/j.jphysparis.2015.02.001 CrossRefPubMed

Schlaghecken F, Eimer M (2004) Masked prime stimuli can bias “free” choices between response alternatives. Psychon Bull Rev 11:463–468. https://doi.org/10.3758/BF03196596 CrossRefPubMed

Schneider TR, Debener S, Oostenveld R, Engel AK (2008) Enhanced EEG gamma-band activity reflects multisensory semantic matching in visual-to-auditory object priming. NeuroImage 42:1244–1254. https://doi.org/10.1016/j.neuroimage.2008.05.033 CrossRefPubMed

Sporns O, Chialvo D, Kaiser M, Hilgetag C (2004) Organization, development and function of complex brain networks. Trends Cogn Sci 8:418–425. https://doi.org/10.1016/j.tics.2004.07.008 CrossRef

Sporns O, Tononi G, Kötter R (2005) The human connectome: a structural description of the human brain. PLoS Comput Biol 1:e42. https://doi.org/10.1371/journal.pcbi.0010042 CrossRefPubMedPubMedCentral

Stock A-K, Friedrich J, Beste C (2016) Subliminally and consciously induced cognitive conflicts interact at several processing levels. Cortex J Devoted Study Nerv Syst Behav 85:75–89. https://doi.org/10.1016/j.cortex.2016.09.027 CrossRef

Tallon-Baudry C, Bertrand O, Delpuech C, Permier J (1997) Oscillatory gamma-band (30–70 Hz) activity induced by a visual search task in humans. J Neurosci Off J Soc Neurosci 17:722–734CrossRef

Telesford QK, Joyce KE, Hayasaka S et al (2011) The ubiquity of small-world networks. Brain Connect 1:367–375. https://doi.org/10.1089/brain.2011.0038 CrossRefPubMedPubMedCentral

Ulrich R, Schröter H, Leuthold H, Birngruber T (2015) Automatic and controlled stimulus processing in conflict tasks: superimposed diffusion processes and delta functions. Cogn Psychol 78:148–174. https://doi.org/10.1016/j.cogpsych.2015.02.005 CrossRefPubMed

Wagenmakers E (2007) A practical solution to the pervasive problems of p values. Psychon Bull Rev 14:779–804CrossRefPubMed

Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393:440–442. https://doi.org/10.1038/30918 CrossRef

Womelsdorf T, Vinck M, Leung LS, Everling S (2010) Selective theta-synchronization of choice-relevant information subserves goal-directed behavior. Front Hum Neurosci 4:210. https://doi.org/10.3389/fnhum.2010.00210 CrossRefPubMedPubMedCentral

Yordanova J, Falkenstein M, Hohnsbein J, Kolev V (2004) Parallel systems of error processing in the brain. NeuroImage 22:590–602. https://doi.org/10.1016/j.neuroimage.2004.01.040 CrossRefPubMed

Yu S, Huang D, Singer W, Nikolić D (2008) A small world of neuronal synchrony. Cereb Cortex 18:2891–2901. https://doi.org/10.1093/cercor/bhn047 CrossRefPubMedPubMedCentral

Title: Neuronal networks underlying the conjoint modulation of response selection by subliminal and consciously induced cognitive conflicts
Authors: Wiebke Bensmann
Nicolas Zink
Moritz Mückschel
Christian Beste
Ann-Kathrin Stock
Publication date: 01-06-2019
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 5/2019
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-019-01866-0

At a glance: The STEP trials

Springer Medicine

Neuronal networks underlying the conjoint modulation of response selection by subliminal and consciously induced cognitive conflicts

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 5/2019

Dissociable effects of dopamine D1 and D2 receptors on compulsive ingestion and pivoting movements elicited by disinhibiting the ventral pallidum

Validity expectancies shape the interplay of cueing and task demands during inhibitory control associated with right inferior frontal regions

The motor cortex of the sheep: laminar organization, projections and diffusion tensor imaging of the intracranial pyramidal and extrapyramidal tracts

In vivo high-resolution diffusion tensor imaging of the developing neonatal rat cortex and its relationship to glial and dendritic maturation

Common and distinct neural correlates of dual-tasking and task-switching: a meta-analytic review and a neuro-cognitive processing model of human multitasking

Absolute and relative pitch processing in the human brain: neural and behavioral evidence