Midline frontal cortex low-frequency activity drives subthalamic nucleus oscillations during conflict.
Making the right decision from conflicting information takes time. Recent computational, electrophysiological, and clinical studies have implicated two brain areas as being crucial in assuring sufficient time is taken for decision-making under conditions of conflict: the medial prefrontal cortex and the subthalamic nucleus (STN). Both structures exhibit an elevation of activity at low frequencies (<10 Hz) during conflict that correlates with the amount of time taken to respond. This suggests that the two sites could become functionally coupled during conflict. To establish the nature of this interaction we recorded from deep-brain stimulation electrodes implanted bilaterally in the STN of 13 Parkinson's disease patients while they performed a sensory integration task involving randomly moving dots. By gradually increasing the number of dots moving coherently in one direction, we were able to determine changes in the STN associated with response execution. Furthermore, by occasionally having 10% of the dots move in the opposite direction as the majority, we were able to identify an independent increase in STN theta-delta activity triggered by conflict. Crucially, simultaneous midline frontal electroencephalographic recordings revealed an increase in the theta-delta band coherence between the two structures that was specific to high-conflict trials. Activity over the midline frontal cortex was Granger causal to that in STN. These results establish the cortico-subcortical circuit enabling successful choices to be made under conditions of conflict and provide support for the hypothesis that the brain uses frequency-specific channels of communication to convey behaviorally relevant information.
Experimental Neurology Group, Nuffield Department of Clinical Neurology, University of Oxford John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom, Surgical Neurology Branch, National Institutes of Health, Bethesda, Maryland 20814.
Baltazar A
BA
Zavala
Experimental Neurology Group, Nuffield Department of Clinical Neurology, University of Oxford John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom.
Huiling
H
Tan
Experimental Neurology Group, Nuffield Department of Clinical Neurology, University of Oxford John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom.
Simon
S
Little
Department of Neurosurgery, King's College Hospital, Kings College, London, SE5 9RS, United Kingdom, and.
Keyoumars
K
Ashkan
Sobell Department of Motor Neuroscience and Movement Disorders, University College London, Institute of Neurology, London, WC1 3BG, United Kingdom.
Marwan
M
Hariz
Sobell Department of Motor Neuroscience and Movement Disorders, University College London, Institute of Neurology, London, WC1 3BG, United Kingdom.
Thomas
T
Foltynie
Sobell Department of Motor Neuroscience and Movement Disorders, University College London, Institute of Neurology, London, WC1 3BG, United Kingdom.
Ludvic
L
Zrinzo
Surgical Neurology Branch, National Institutes of Health, Bethesda, Maryland 20814.
Kareem A
KA
Zaghloul
Experimental Neurology Group, Nuffield Department of Clinical Neurology, University of Oxford John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom, peter.brown@ndcn.ox.ac.uk.
Peter
P
Brown
D000328:Adult; D000368:Aged; D001931:Brain Mapping; D058256:Brain Waves / Q000502:physiology*; D002755:Choice Behavior / Q000502:physiology*; D003220:Conflict, Psychological; D046690:Deep Brain Stimulation / Q000379:methods; D004525:Efferent Pathways / Q000502:physiology*; D004569:Electroencephalography; D005260:Female; D005625:Frontal Lobe / Q000502:physiology*; D006801:Humans; D008279:Magnetic Resonance Imaging; D008297:Male; D008875:Middle Aged; D010300:Parkinson Disease / Q000503:physiopathology / Q000628:therapy; D020531:Subthalamic Nucleus / Q000502:physiology*
conflict; midline frontal cortex; subthalamic nucleus; theta oscillations