Common and unique neural networks for proactive and reactive response inhibition revealed by independent component analysis of functional MRI data

Response inhibition involves proactive and reactive modes. Proactive inhibition is goal-directed, triggered by warning cues, and serves to restrain actions. Reactive inhibition is stimulus-driven, triggered by salient stop-signals, and used to stop actions completely. Functional MRI studies have identified brain regions that activate during proactive and reactive inhibition. It remains unclear how these brain regions operate in functional networks, and whether proactive and reactive inhibition depend on common networks, unique networks, or a combination. To address this we analyzed a large fMRI dataset (N=65) of a stop-signal task designed to measure proactive and reactive inhibition, using independent component analysis (ICA). We found 1) three frontal networks that were associated with both proactive and reactive inhibition, 2) one network in the superior parietal lobe, which also included dorsal premotor cortex and left putamen, that was specifically associated with proactive inhibition, and 3) two right-lateralized frontal and fronto-parietal networks, including the right inferior frontal gyrus and temporoparietal junction as well as a bilateral fronto-temporal network that were uniquely associated with reactive inhibition. Overlap between networks was observed in dorsolateral prefrontal and parietal cortices. Taken together, we offer a new perspective on the neural underpinnings of inhibitory control, by showing that proactive inhibition and reactive inhibition are supported by a group of common and unique networks that appear to integrate and interact in frontoparietal areas.

[1]  T. Adali,et al.  Unmixing fMRI with independent component analysis , 2006, IEEE Engineering in Medicine and Biology Magazine.

[2]  Frederick Verbruggen,et al.  Responding with Restraint: What Are the Neurocognitive Mechanisms? , 2010, Journal of Cognitive Neuroscience.

[3]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[4]  D. Pandya,et al.  Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. , 2007, Brain : a journal of neurology.

[5]  G. Logan On the ability to inhibit thought and action , 1984 .

[6]  Arthur W. Toga,et al.  Construction of a 3D probabilistic atlas of human cortical structures , 2008, NeuroImage.

[7]  Tor D. Wager,et al.  Common and unique components of response inhibition revealed by fMRI , 2005, NeuroImage.

[8]  D. Pandya,et al.  Striatal connections of the parietal association cortices in rhesus monkeys , 1993, The Journal of comparative neurology.

[9]  B. Mesquita,et al.  Adjustment to Chronic Diseases and Terminal Illness Health Psychology : Psychological Adjustment to Chronic Disease , 2006 .

[10]  M. Vink,et al.  Expectations and violations: Delineating the neural network of proactive inhibitory control , 2013, Human brain mapping.

[11]  R. Dolan,et al.  Preparing for Selective Inhibition within Frontostriatal Loops , 2013, The Journal of Neuroscience.

[12]  Etienne Olivier,et al.  Short-Latency Influence of Medial Frontal Cortex on Primary Motor Cortex during Action Selection under Conflict , 2009, The Journal of Neuroscience.

[13]  Christian F. Beckmann,et al.  Modelling with independent components , 2012, NeuroImage.

[14]  J. Haxby,et al.  Parallel Visual Motion Processing Streams for Manipulable Objects and Human Movements , 2002, Neuron.

[15]  A. Turken,et al.  Left inferior frontal gyrus is critical for response inhibition , 2008, BMC Neuroscience.

[16]  A. T. Slater-Hammel,et al.  Reliability, Accuracy, and Refractoriness of a Transit Reaction , 1960 .

[17]  Tülay Adali,et al.  Estimating the number of independent components for functional magnetic resonance imaging data , 2007, Human brain mapping.

[18]  Tülay Adali,et al.  Comparison of multi‐subject ICA methods for analysis of fMRI data , 2010, Human brain mapping.

[19]  Sheng Zhang,et al.  Functional networks for cognitive control in a stop signal task: Independent component analysis , 2012, Human brain mapping.

[20]  Adam P. Morris,et al.  Executive Brake Failure following Deactivation of Human Frontal Lobe , 2006 .

[21]  Diane Swick,et al.  Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks , 2011, NeuroImage.

[22]  S Makeig,et al.  Analysis of fMRI data by blind separation into independent spatial components , 1998, Human brain mapping.

[23]  Patrick G. Bissett,et al.  Post-stop-signal adjustments: inhibition improves subsequent inhibition. , 2012, Journal of experimental psychology. Learning, memory, and cognition.

[24]  V. Esposito,et al.  Stop-event-related potentials from intracranial electrodes reveal a key role of premotor and motor cortices in stopping ongoing movements , 2012, Front. Neuroeng..

[25]  T. Robbins,et al.  Inhibition and impulsivity: Behavioral and neural basis of response control , 2013, Progress in Neurobiology.

[26]  EFFECTIVE CONNECTIVITY REVEALS IMPORTANT ROLES FOR BOTH THE HYPERDIRECT AND THE INDIRECT FRONTO-BASAL GANGLIA PATHWAYS DURING RESPONSE INHIBITION , 2014 .

[27]  R. Constable,et al.  Imaging Response Inhibition in a Stop-Signal Task: Neural Correlates Independent of Signal Monitoring and Post-Response Processing , 2006, The Journal of Neuroscience.

[28]  Gordon D. Logan,et al.  Dependence and Independence in Responding to Double Stimulation : A Comparison of Stop , Change , and Dual-Task Paradigms , 1986 .

[29]  Ji Heon Hong,et al.  The anatomical characteristics of superior longitudinal fasciculus I in human brain: Diffusion tensor tractography study , 2012, Neuroscience Letters.

[30]  Matthijs Vink,et al.  Frontostriatal activity and connectivity increase during proactive inhibition across adolescence and early adulthood , 2014, Human brain mapping.

[31]  R. Kahn,et al.  Reduced Proactive Inhibition in Schizophrenia Is Related to Corticostriatal Dysfunction and Poor Working Memory , 2011, Biological Psychiatry.

[32]  T. Sejnowski,et al.  Human Brain Mapping 6:368–372(1998) � Independent Component Analysis of fMRI Data: Examining the Assumptions , 2022 .

[33]  Aapo Hyvärinen,et al.  Validating the independent components of neuroimaging time series via clustering and visualization , 2004, NeuroImage.

[34]  W. Byblow,et al.  Selective inhibition of movement. , 2007, Journal of neurophysiology.

[35]  Russell A. Poldrack,et al.  Engagement of large-scale networks is related to individual differences in inhibitory control , 2010, NeuroImage.

[36]  Tadeusz Marek,et al.  Contributive sources analysis: A measure of neural networks' contribution to brain activations , 2013, NeuroImage.

[37]  Ethan R. Buch,et al.  A Network Centered on Ventral Premotor Cortex Exerts Both Facilitatory and Inhibitory Control over Primary Motor Cortex during Action Reprogramming , 2010, The Journal of Neuroscience.

[38]  H. Duvernoy The Human Brain Stem and Cerebellum: Surface, Structure, Vascularization, and Three-Dimensional Sectional Anatomy, with MRI , 2013 .

[39]  Rex E. Jung,et al.  A Baseline for the Multivariate Comparison of Resting-State Networks , 2011, Front. Syst. Neurosci..

[40]  Vince D. Calhoun,et al.  Task-related concurrent but opposite modulations of overlapping functional networks as revealed by spatial ICA , 2013, NeuroImage.

[41]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[42]  R. Kahn,et al.  Function of striatum beyond inhibition and execution of motor responses , 2005, Human brain mapping.

[43]  J. Pekar,et al.  A method for making group inferences from functional MRI data using independent component analysis , 2001, Human brain mapping.

[44]  Vince D. Calhoun,et al.  A review of group ICA for fMRI data and ICA for joint inference of imaging, genetic, and ERP data , 2009, NeuroImage.

[45]  Y. Miyashita,et al.  Preparation to Inhibit a Response Complements Response Inhibition during Performance of a Stop-Signal Task , 2009, The Journal of Neuroscience.

[46]  T. Braver,et al.  Explaining the many varieties of working memory variation: Dual mechanisms of cognitive control. , 2007 .

[47]  G. Logan,et al.  Proactive adjustments of response strategies in the stop-signal paradigm. , 2009, Journal of experimental psychology. Human perception and performance.

[48]  T. Robbins,et al.  Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans , 2003, Nature Neuroscience.

[49]  Ethan R. Buch,et al.  Cortical and subcortical interactions during action reprogramming and their related white matter pathways , 2010, Proceedings of the National Academy of Sciences.

[50]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[51]  박현욱,et al.  Independent component analysis를 이용한 fMRI 신호 분석 , 1999 .

[52]  A. Aron From Reactive to Proactive and Selective Control: Developing a Richer Model for Stopping Inappropriate Responses , 2011, Biological Psychiatry.

[53]  Vince D. Calhoun,et al.  Capturing inter-subject variability with group independent component analysis of fMRI data: A simulation study , 2012, NeuroImage.

[54]  Christo Pantev,et al.  Multimodal imaging of functional networks and event-related potentials in performance monitoring , 2011, NeuroImage.

[55]  M. Vink,et al.  On the Role of the Striatum in Response Inhibition , 2010, PloS one.

[56]  John C. Rothwell,et al.  Theta Burst Stimulation , 2007 .

[57]  P. Strick,et al.  Cerebellar Projections to the Prefrontal Cortex of the Primate , 2001, The Journal of Neuroscience.

[58]  J. Pekar,et al.  Different activation dynamics in multiple neural systems during simulated driving , 2002, Human brain mapping.

[59]  C. Eriksen,et al.  Use of a delayed signal to stop a visual reaction-time response. , 1966 .

[60]  Alex Martin,et al.  Grounding Object Concepts in Perception and Action: Evidence from FMRI Studies of Tools , 2007, Cortex.

[61]  G. Logan,et al.  On the ability to inhibit simple and choice reaction time responses: a model and a method. , 1984, Journal of experimental psychology. Human perception and performance.

[62]  S. Ferraina,et al.  Neural correlates of cognitive control of reaching movements in the dorsal premotor cortex of rhesus monkeys. , 2011, Journal of neurophysiology.

[63]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[64]  G. Logan,et al.  Response inhibition in the stop-signal paradigm , 2008, Trends in Cognitive Sciences.

[65]  Darryl W. Schneider,et al.  Automatic and Controlled Response Inhibition: Associative Learning in the Go/no-go and Stop-signal Paradigms the Go/no-go Paradigm and the Stop-signal Paradigm , 2022 .

[66]  G. Rizzolatti,et al.  Two different streams form the dorsal visual system: anatomy and functions , 2003, Experimental Brain Research.

[67]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[68]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[69]  R. Poldrack,et al.  Cortical and Subcortical Contributions to Stop Signal Response Inhibition: Role of the Subthalamic Nucleus , 2006, The Journal of Neuroscience.

[70]  René S. Kahn,et al.  Transcranial Magnetic Stimulation and Functional MRI Reveal Cortical and Subcortical Interactions during Stop-signal Response Inhibition , 2013, Journal of Cognitive Neuroscience.

[71]  A. Aron,et al.  Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex , 2010, Proceedings of the National Academy of Sciences.

[72]  V D Calhoun,et al.  Independent component analysis of fMRI data in the complex domain , 2002, Magnetic resonance in medicine.

[73]  Li Yao,et al.  Multiple neural networks supporting a semantic task: An fMRI study using independent component analysis , 2009, NeuroImage.

[74]  Gene A. Brewer,et al.  Variation in working memory capacity and episodic memory: examining the importance of encoding specificity. , 2011, Psychonomic bulletin & review.

[75]  Neil G. Muggleton,et al.  Control of prepotent responses by the superior medial frontal cortex , 2009, NeuroImage.

[76]  Andrew R. A. Conway,et al.  Variation in working memory , 2008 .

[77]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[78]  Seth A. Herd,et al.  A Unified Framework for Inhibitory Control Opinion , 2022 .

[79]  V. Calhoun,et al.  Spatial ICA reveals functional activity hidden from traditional fMRI GLM-based analyses , 2013, Front. Neurosci..

[80]  Thomas V. Wiecki,et al.  A computational model of inhibitory control in frontal cortex and basal ganglia. , 2011, Psychological review.

[81]  Nitin Tandon,et al.  Roles for the pre-supplementary motor area and the right inferior frontal gyrus in stopping action: Electrophysiological responses and functional and structural connectivity , 2012, NeuroImage.

[82]  J. Haxby,et al.  Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects , 1999, Nature Neuroscience.

[83]  Giovanni Mirabella,et al.  Effects of probability bias in response readiness and response inhibition on reaching movements , 2014, Experimental Brain Research.