A Role for the Subthalamic Nucleus in Response Inhibition during Conflict

The subthalamic nucleus (STN) is a key node in the network that supports response inhibition. It is suggested that the STN rapidly inhibits basal ganglia activity, to pause motor output during conflict until an appropriate motor plan is ready. Here, we recorded neural activity during a Stroop task from deep brain stimulation electrodes implanted in the human STN. We intended to determine whether cognitive psychological phenomena such as the Stroop effect can be explained via mechanisms of response inhibition involving the STN, or whether higher cognitive centers are alone responsible. We show stimulus-driven desychronization in the beta band (15–35 Hz) that lasts throughout the verbal response, in keeping with the idea that beta-band synchrony decreases to allow motor output to occur. During incongruent trials—in which response times were elongated due to the Stroop effect—a resynchronization was seen in the beta band before response. Crucially, in the incongruent trials during which the participant was unable to withhold the prepotent response, this resynchronization occurred after response onset. We suggest that this beta-band resynchronization pauses the motor system until conflict can be resolved.

[1]  P. Brown,et al.  Event-related beta desynchronization in human subthalamic nucleus correlates with motor performance. , 2004, Brain : a journal of neurology.

[2]  Nicola J. Ray,et al.  The role of the subthalamic nucleus in response inhibition: Evidence from deep brain stimulation for Parkinson's disease , 2009, Neuropsychologia.

[3]  Peter Brown,et al.  Boosting Cortical Activity at Beta-Band Frequencies Slows Movement in Humans , 2009, Current Biology.

[4]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[5]  P. Brown,et al.  Synchronous unit activity and local field potentials evoked in the subthalamic nucleus by cortical stimulation. , 2004, Journal of neurophysiology.

[6]  Thomas V. Wiecki,et al.  Subthalamic nucleus stimulation reverses mediofrontal influence over decision threshold , 2011, Nature Neuroscience.

[7]  Tipu Z. Aziz,et al.  Driving Oscillatory Activity in the Human Cortex Enhances Motor Performance , 2012, Current Biology.

[8]  A. Engel,et al.  Different Subtypes of Striatal Neurons Are Selectively Modulated by Cortical Oscillations , 2009, The Journal of Neuroscience.

[9]  Daniel K. Leventhal,et al.  Basal Ganglia Beta Oscillations Accompany Cue Utilization , 2012, Neuron.

[10]  A. Leuthold,et al.  Beta-Band Activity during Motor Planning Reflects Response Uncertainty , 2010, The Journal of Neuroscience.

[11]  Michael J. Frank,et al.  Hold Your Horses: Impulsivity, Deep Brain Stimulation, and Medication in Parkinsonism , 2007, Science.

[12]  A. Nambu,et al.  Functional significance of the cortico–subthalamo–pallidal ‘hyperdirect’ pathway , 2002, Neuroscience Research.

[13]  J. Deniau,et al.  Relationships between the Prefrontal Cortex and the Basal Ganglia in the Rat: Physiology of the Corticosubthalamic Circuits , 1998, The Journal of Neuroscience.

[14]  Andrea A. Kühn,et al.  The relationship between local field potential and neuronal discharge in the subthalamic nucleus of patients with Parkinson's disease , 2005, Experimental Neurology.

[15]  Richard G. Baraniuk,et al.  Multiple Window Time Varying Spectrum Estimation , 2000 .

[16]  P. Brown Abnormal oscillatory synchronisation in the motor system leads to impaired movement , 2007, Current Opinion in Neurobiology.

[17]  Michael J. Frank,et al.  Hold your horses: A dynamic computational role for the subthalamic nucleus in decision making , 2006, Neural Networks.

[18]  O. Hikosaka,et al.  Perceptual Learning, Motor Learning and Automaticity Switching from Automatic to Controlled Behavior: Cortico-basal Ganglia Mechanisms , 2022 .

[19]  M. Kahana,et al.  Neuronal Activity in the Human Subthalamic Nucleus Encodes Decision Conflict during Action Selection , 2012, The Journal of Neuroscience.

[20]  J. Ridley Studies of Interference in Serial Verbal Reactions , 2001 .

[21]  K. J. Miller,et al.  Transient and state modulation of beta power in human subthalamic nucleus during speech production and finger movement , 2012, Neuroscience.

[22]  B. Averbeck,et al.  Stroop test performance in impulsive and non impulsive patients with Parkinson's disease. , 2011, Parkinsonism & related disorders.

[23]  M. Merello,et al.  [Functional anatomy of the basal ganglia]. , 2000, Revista de neurologia.

[24]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

[25]  P. Brown,et al.  New insights into the relationship between dopamine, beta oscillations and motor function , 2011, Trends in Neurosciences.

[26]  J. Stein,et al.  Localisation of the Subthalamic Nucleus Using Radionics Image FusionTM and StereoplanTM Combined with Field Potential Recording , 2002, Stereotactic and Functional Neurosurgery.

[27]  Tipu Z. Aziz,et al.  The role of the subthalamic nucleus in response inhibition: Evidence from local field potential recordings in the human subthalamic nucleus , 2012, NeuroImage.

[28]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

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

[30]  A. Aron The Neural Basis of Inhibition in Cognitive Control , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[31]  Geert J. M. van Boxtel,et al.  Stimulation of the Subthalamic Region Facilitates the Selection and Inhibition of Motor Responses in Parkinson's Disease , 2006, Journal of Cognitive Neuroscience.

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

[33]  Michael A. DiSano,et al.  Intracranial EEG Reveals a Time- and Frequency-Specific Role for the Right Inferior Frontal Gyrus and Primary Motor Cortex in Stopping Initiated Responses , 2009, The Journal of Neuroscience.

[34]  Peter Brown,et al.  Intra-operative recordings of local field potentials can help localize the subthalamic nucleus in Parkinson's disease surgery , 2006, Experimental Neurology.

[35]  Marjan Jahanshahi,et al.  Deficits in inhibitory control and conflict resolution on cognitive and motor tasks in Parkinson’s disease , 2011, Experimental Brain Research.

[36]  R. Poldrack,et al.  Common neural substrates for inhibition of spoken and manual responses. , 2008, Cerebral cortex.

[37]  Claudio Lucchiari,et al.  Conflict-dependent dynamic of subthalamic nucleus oscillations during moral decisions , 2011, Social neuroscience.

[38]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[39]  J. Dostrovsky,et al.  Beta oscillatory activity in the subthalamic nucleus and its relation to dopaminergic response in Parkinson's disease. , 2006, Journal of neurophysiology.

[40]  Timothy Edward John Behrens,et al.  Triangulating a Cognitive Control Network Using Diffusion-Weighted Magnetic Resonance Imaging (MRI) and Functional MRI , 2007, The Journal of Neuroscience.

[41]  Nicole C. Swann,et al.  Deep Brain Stimulation of the Subthalamic Nucleus Alters the Cortical Profile of Response Inhibition in the Beta Frequency Band: A Scalp EEG Study in Parkinson's Disease , 2011, The Journal of Neuroscience.

[42]  K. Lovblad,et al.  A Technical Note , 2013, Interventional neuroradiology : journal of peritherapeutic neuroradiology, surgical procedures and related neurosciences.

[43]  John-Stuart Brittain,et al.  Single-Trial Multiwavelet Coherence in Application to Neurophysiological Time Series , 2007, IEEE Transactions on Biomedical Engineering.

[44]  M. Manfredi,et al.  Deep brain stimulation of subthalamic nuclei affects arm response inhibition in Parkinson's patients. , 2012, Cerebral cortex.

[45]  Peter Brown,et al.  A gamma band specific role of the subthalamic nucleus in switching during verbal fluency tasks in Parkinson’s disease , 2011, Experimental Neurology.

[46]  J. Yelnik Functional anatomy of the basal ganglia , 2002, Movement disorders : official journal of the Movement Disorder Society.