Multi-areal neural dynamics encode human decision making

Value-based decision-making involves multiple cortical and subcortical brain areas, but the distributed nature of neurophysiological activity underlying economic choices in the human brain remains largely unexplored. Here, we use intracranial recordings from neurosurgical patients to show that risky choices are reflected in high frequency activity distributed across multiple prefrontal and subcortical brain regions, whereas reward-related computations are less widely represented and more modular. State space modeling reveals sub-second neural dynamics underlying choices during deliberation and allows high-accuracy trial-by-trial decoding of subjects’ choices robustly across patients despite differences in anatomical coverage. These results shed light into the neural basis of choice across brain areas and open the door to new intracranial approaches for brain state decoding.

[1]  S. Nagel,et al.  Memory formation. , 2023, The Journal of chemical physics.

[2]  Nicholas A. Steinmetz,et al.  A stable, distributed code for cue value in mouse cortex during reward learning , 2023, bioRxiv.

[3]  Salman E Qasim,et al.  Neuronal activity in the human amygdala and hippocampus enhances emotional memory encoding , 2021, bioRxiv.

[4]  A. Berthoz,et al.  Decoding the neural dynamics of free choice in humans , 2020, PLoS Biology.

[5]  N. H. Sabah Neurons , 2020, Neuromuscular Fundamentals.

[6]  Salman E Qasim,et al.  Phase precession in the human hippocampus and entorhinal cortex , 2020, Cell.

[7]  M. Pessiglione,et al.  Four core properties of the human brain valuation system demonstrated in intracranial signals , 2020, Nature Neuroscience.

[8]  Daeyeol Lee,et al.  Multiple timescales of neural dynamics and integration of task-relevant signals across cortex , 2020, Proceedings of the National Academy of Sciences.

[9]  M. Williams The Cingulate Cortex , 2020, The Neuropathology of Schizophrenia.

[10]  Nora A. Herweg,et al.  Theta Oscillations in Human Memory , 2020, Trends in Cognitive Sciences.

[11]  Nicholas A. Steinmetz,et al.  Distributed coding of choice, action, and engagement across the mouse brain , 2019, Nature.

[12]  Charles B. Mikell,et al.  Widespread temporal coding of cognitive control in human prefrontal cortex , 2019, Nature Neuroscience.

[13]  Stephen I. Ryu,et al.  Decoding and perturbing decision states in real time , 2019, Nature.

[14]  J. Parvizi,et al.  Intensity of affective experience is modulated by magnitude of intracranial electrical stimulation in human orbitofrontal, cingulate and insular cortices , 2019, Social cognitive and affective neuroscience.

[15]  R. Knight,et al.  Dissociation of broadband high-frequency activity and neuronal firing in the neocortex , 2019, Science Advances.

[16]  Heather E. Dawes,et al.  An Amygdala-Hippocampus Subnetwork that Encodes Variation in Human Mood , 2018, Cell.

[17]  Yuxiao Yang,et al.  Mood variations decoded from multi-site intracranial human brain activity , 2018, Nature Biotechnology.

[18]  Jack J. Lin,et al.  Encoding of Multiple Reward-Related Computations in Transient and Sustained High-Frequency Activity in Human OFC , 2018, Current Biology.

[19]  Jack J. Lin,et al.  Neural Mechanisms of Sustained Attention Are Rhythmic , 2018, Neuron.

[20]  Josef Parvizi,et al.  Promises and limitations of human intracranial electroencephalography , 2018, Nature Neuroscience.

[21]  E. Chang,et al.  Effect of neurostimulation on cognition and mood in refractory epilepsy , 2018, Epilepsia open.

[22]  Leland McInnes,et al.  UMAP: Uniform Manifold Approximation and Projection for Dimension Reduction , 2018, ArXiv.

[23]  Robert Oostenveld,et al.  Integrated analysis of anatomical and electrophysiological human intracranial data , 2017, Nature Protocols.

[24]  Laurence T. Hunt,et al.  Triple Dissociation of Attention and Decision Computations across Prefrontal Cortex , 2017, Nature Neuroscience.

[25]  M. Frank,et al.  The drift diffusion model as the choice rule in reinforcement learning , 2017, Psychonomic bulletin & review.

[26]  Thorsten Kahnt,et al.  A decade of decoding reward-related fMRI signals and where we go from here , 2017, NeuroImage.

[27]  Michael J. Jutras,et al.  Direct Brain Stimulation Modulates Encoding States and Memory Performance in Humans , 2017, Current Biology.

[28]  Erin L. Rich,et al.  Decoding subjective decisions from orbitofrontal cortex , 2016, Nature Neuroscience.

[29]  B. Postle,et al.  The Speed of Alpha-Band Oscillations Predicts the Temporal Resolution of Visual Perception , 2015, Current Biology.

[30]  Jose M Carmena,et al.  Neural oscillations: beta band activity across motor networks , 2015, Current Opinion in Neurobiology.

[31]  Sun I. Kim,et al.  Role of low‐ and high‐frequency oscillations in the human hippocampus for encoding environmental novelty during a spatial navigation task , 2014, Hippocampus.

[32]  Floris P. de Lange,et al.  Local Entrainment of Alpha Oscillations by Visual Stimuli Causes Cyclic Modulation of Perception , 2014, The Journal of Neuroscience.

[33]  P. Krack,et al.  Mood and behavioural effects of subthalamic stimulation in Parkinson's disease , 2014, The Lancet Neurology.

[34]  Michael X Cohen,et al.  Analyzing Neural Time Series Data: Theory and Practice , 2014 .

[35]  W. Schultz,et al.  Risk Prediction Error Coding in Orbitofrontal Neurons , 2013, The Journal of Neuroscience.

[36]  Arne D. Ekstrom,et al.  A comparative study of human and rat hippocampal low‐frequency oscillations during spatial navigation , 2013, Hippocampus.

[37]  A. Kohn,et al.  Gamma and the Coordination of Spiking Activity in Early Visual Cortex , 2013, Neuron.

[38]  G. Buzsáki,et al.  Memory, navigation and theta rhythm in the hippocampal-entorhinal system , 2013, Nature Neuroscience.

[39]  W. Klimesch Alpha-band oscillations, attention, and controlled access to stored information , 2012, Trends in Cognitive Sciences.

[40]  N. Daw,et al.  The ubiquity of model-based reinforcement learning , 2012, Current Opinion in Neurobiology.

[41]  P. Cisek Making decisions through a distributed consensus , 2012, Current Opinion in Neurobiology.

[42]  K. Preuschoff,et al.  Neural Correlates of Anticipation Risk Reflect Risk Preferences , 2012, The Journal of Neuroscience.

[43]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.

[44]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[45]  A. Engel,et al.  Spectral fingerprints of large-scale neuronal interactions , 2012, Nature Reviews Neuroscience.

[46]  S. Kennerley,et al.  Contrasting reward signals in the orbitofrontal cortex and anterior cingulate cortex , 2011, Annals of the New York Academy of Sciences.

[47]  Daeyeol Lee,et al.  Ubiquity and Specificity of Reinforcement Signals throughout the Human Brain , 2011, Neuron.

[48]  Timothy E. J. Behrens,et al.  Double dissociation of value computations in orbitofrontal and anterior cingulate neurons , 2011, Nature Neuroscience.

[49]  A. Rangel,et al.  Multialternative drift-diffusion model predicts the relationship between visual fixations and choice in value-based decisions , 2011, Proceedings of the National Academy of Sciences.

[50]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[51]  M Sahani,et al.  Modelling low-dimensional dynamics in recorded spiking populations , 2011 .

[52]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[53]  J. Kalaska,et al.  Neural mechanisms for interacting with a world full of action choices. , 2010, Annual review of neuroscience.

[54]  J. Parvizi,et al.  Human Neuroscience , 2022 .

[55]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[56]  J. Engelmann,et al.  Individual differences in risk preference predict neural responses during financial decision-making , 2009, Brain Research.

[57]  C. Pennartz,et al.  Single-Cell and Population Coding of Expected Reward Probability in the Orbitofrontal Cortex of the Rat , 2009, The Journal of Neuroscience.

[58]  Jonathan D. Wallis,et al.  Neurons in the Frontal Lobe Encode the Value of Multiple Decision Variables , 2009, Journal of Cognitive Neuroscience.

[59]  Y. Niv Reinforcement learning in the brain , 2009 .

[60]  M. Rushworth,et al.  General Mechanisms for Making Decisions? This Review Comes from a Themed Issue on Cognitive Neuroscience Edited the Representation of Value and Reward Expectations in Frontal Cortex Reward Prediction Errors and Learning Rates Other Types of Prediction Error , 2022 .

[61]  C. Schroeder,et al.  Low-frequency neuronal oscillations as instruments of sensory selection , 2009, Trends in Neurosciences.

[62]  David Cucurell,et al.  Human oscillatory activity associated to reward processing in a gambling task , 2008, Neuropsychologia.

[63]  Colin Camerer,et al.  Explicit neural signals reflecting reward uncertainty , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[64]  Colin Camerer,et al.  A framework for studying the neurobiology of value-based decision making , 2008, Nature Reviews Neuroscience.

[65]  S. Quartz,et al.  Human Insula Activation Reflects Risk Prediction Errors As Well As Risk , 2008, The Journal of Neuroscience.

[66]  P. Glimcher,et al.  The neural correlates of subjective value during intertemporal choice , 2007, Nature Neuroscience.

[67]  I. Fried,et al.  Coupling between Neuronal Firing Rate, Gamma LFP, and BOLD fMRI Is Related to Interneuronal Correlations , 2007, Current Biology.

[68]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[69]  R. Kravitz,et al.  Depression , 2007, Annals of Internal Medicine.

[70]  Michael X. Cohen,et al.  Reward expectation modulates feedback-related negativity and EEG spectra , 2007, NeuroImage.

[71]  J. O'Doherty,et al.  Reward Value Coding Distinct From Risk Attitude-Related Uncertainty Coding in Human Reward Systems , 2006, Journal of neurophysiology.

[72]  J. Sampson selection , 2006, Algorithm Design with Haskell.

[73]  C. Padoa-Schioppa,et al.  Neurons in the orbitofrontal cortex encode economic value , 2006, Nature.

[74]  A. Lozano,et al.  Deep Brain Stimulation for Treatment-Resistant Depression , 2005, Neuron.

[75]  Samuel M. McClure,et al.  Separate Neural Systems Value Immediate and Delayed Monetary Rewards , 2004, Science.

[76]  Guglielmo Foffani,et al.  PSTH-based classification of sensory stimuli using ensembles of single neurons , 2004, Journal of Neuroscience Methods.

[77]  R. Cordaux,et al.  Humans , 2004, Current Biology.

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

[79]  Mike Fitzpatrick Choice , 2004, The Lancet.

[80]  J. Wallis,et al.  Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task , 2003, The European journal of neuroscience.

[81]  J. Oller,et al.  Consensus and controversy , 1984 .

[82]  Y. Pesin CHARACTERISTIC LYAPUNOV EXPONENTS AND SMOOTH ERGODIC THEORY , 1977 .

[83]  Edward J. Mock,et al.  Financial Decision Making , 1968 .

[84]  Peter Secretan Learning , 1965, Mental Health.

[85]  G. E. Smith The Human Brain , 1924, Nature.

[86]  F. Wandosell,et al.  Cortex , 2021, Encyclopedic Dictionary of Archaeology.

[87]  Mario Prost System , 2019, Concepts for International Law.

[88]  J. Lygeros,et al.  Decision Making I , 2014 .

[89]  S. Ravat,et al.  Refractory epilepsy. , 2010, Journal of the Indian Medical Association.

[90]  Sushant Sachdeva,et al.  Dimension Reduction , 2008, Encyclopedia of GIS.

[91]  Arne D. Ekstrom,et al.  Human hippocampal theta activity during virtual navigation , 2005, Hippocampus.

[92]  Karl J. Friston,et al.  Functional MRI , 1997 .

[93]  J. Voke,et al.  The visual cortex. , 1983, Nursing mirror.

[94]  R. Haber,et al.  Visual Perception , 2018, Encyclopedia of Database Systems.