Multimodal imaging of brain connectivity reveals predictors of individual decision strategy in statistical learning

Successful human behaviour depends on the brain’s ability to extract meaningful structure from information streams and make predictions about future events. Individuals can differ markedly in the decision strategies they use to learn the environment’s statistics, yet we have little idea why. Here, we investigate whether the brain networks involved in learning temporal sequences without explicit reward differ depending on the decision strategy that individuals adopt. We demonstrate that individuals alter their decision strategy in response to changes in temporal statistics and engage dissociable circuits: extracting the exact sequence statistics relates to plasticity in motor corticostriatal circuits, while selecting the most probable outcomes relates to plasticity in visual, motivational and executive corticostriatal circuits. Combining graph metrics of functional and structural connectivity, we provide evidence that learning-dependent changes in these circuits predict individual decision strategy. Our findings propose brain plasticity mechanisms that mediate individual ability for interpreting the structure of variable environments.Combining behavioural modelling with functional and structural brain connectivity, Karlaftis et al. show that individuals learn the structure of variable environments by employing alternate decision strategies that engage distinct brain networks.

[1]  B. Biswal,et al.  Functional connectivity of human striatum: a resting state FMRI study. , 2008, Cerebral cortex.

[2]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[3]  Donald Eugene. Farrar,et al.  Multicollinearity in Regression Analysis; the Problem Revisited , 2011 .

[4]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[5]  Chandan J. Vaidya,et al.  Caudate Resting Connectivity Predicts Implicit Probabilistic Sequence Learning , 2013, Brain Connect..

[6]  John Suckling,et al.  A wavelet method for modeling and despiking motion artifacts from resting-state fMRI time series , 2014, NeuroImage.

[7]  Antonello Baldassarre,et al.  Visual Learning Induces Changes in Resting-State fMRI Multivariate Pattern of Information , 2015, The Journal of Neuroscience.

[8]  Vince D. Calhoun,et al.  Impact of autocorrelation on functional connectivity , 2014, NeuroImage.

[9]  Stefan Skare,et al.  How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging , 2003, NeuroImage.

[10]  Carol A. Seger,et al.  The Involvement of Corticostriatal Loops in Learning Across Tasks, Species, and Methodologies , 2009 .

[11]  Wynne W. Chin,et al.  Socio-cognitive profiles for visual learning in young and older adults , 2015, Front. Aging Neurosci..

[12]  Heidi Johansen-Berg,et al.  Using diffusion imaging to study human connectional anatomy. , 2009, Annual review of neuroscience.

[13]  Peter B. Jones,et al.  373. Adolescence is Associated with Genomically Patterned Consolidation of the Hubs of the Human Brain Connectome , 2016, Biological Psychiatry.

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

[15]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[16]  G. Glover,et al.  Functional neuroanatomy of visuo‐spatial working memory in turner syndrome , 2001, Human brain mapping.

[17]  Zikuan Chen,et al.  Effect of Spatial Smoothing on Task fMRI ICA and Functional Connectivity , 2018, Front. Neurosci..

[18]  Leslie G. Ungerleider,et al.  The neural systems that mediate human perceptual decision making , 2008, Nature Reviews Neuroscience.

[19]  Archana Venkataraman,et al.  Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. , 2010, Journal of neurophysiology.

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

[21]  I. Erev,et al.  On adaptation, maximization, and reinforcement learning among cognitive strategies. , 2005, Psychological review.

[22]  Ben R. Newell,et al.  Of matchers and maximizers: How competition shapes choice under risk and uncertainty , 2015, Cognitive Psychology.

[23]  M. Corbetta,et al.  The Dynamical Balance of the Brain at Rest , 2011, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[24]  Dino J. Levy,et al.  The root of all value: a neural common currency for choice , 2012, Current Opinion in Neurobiology.

[25]  Y. Benjamini,et al.  False Discovery Rate–Adjusted Multiple Confidence Intervals for Selected Parameters , 2005 .

[26]  P. Tiňo,et al.  Learning Predictive Statistics: Strategies and Brain Mechanisms , 2017, The Journal of Neuroscience.

[27]  B. Balleine,et al.  Human and Rodent Homologies in Action Control: Corticostriatal Determinants of Goal-Directed and Habitual Action , 2010, Neuropsychopharmacology.

[28]  A. de Rugy,et al.  Different mechanisms contributing to savings and anterograde interference are impaired in Parkinson's disease , 2013, Front. Hum. Neurosci..

[29]  Karl J. Friston,et al.  A critique of functional localisers , 2006, NeuroImage.

[30]  Alexander Leemans,et al.  The B‐matrix must be rotated when correcting for subject motion in DTI data , 2009, Magnetic resonance in medicine.

[31]  W. Fias,et al.  The Neural Basis of Implicit Perceptual Sequence Learning , 2011, Front. Hum. Neurosci..

[32]  Alan C. Evans,et al.  Enhanced structural connectivity within a brain sub-network supporting working memory and engagement processes after cognitive training , 2017, Neurobiology of Learning and Memory.

[33]  M. Corbetta,et al.  Individual variability in functional connectivity predicts performance of a perceptual task , 2012, Proceedings of the National Academy of Sciences.

[34]  Leonard M. Freeman,et al.  A set of measures of centrality based upon betweenness , 1977 .

[35]  R. Cools,et al.  Human Choice Strategy Varies with Anatomical Projections from Ventromedial Prefrontal Cortex to Medial Striatum. , 2016, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  P. Matthews,et al.  Normalized Accurate Measurement of Longitudinal Brain Change , 2001, Journal of computer assisted tomography.

[37]  H. Johansen-Berg,et al.  White Matter Plasticity in the Adult Brain , 2017, Neuron.

[38]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[39]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[40]  E. Bullmore,et al.  Hierarchical Organization of Human Cortical Networks in Health and Schizophrenia , 2008, The Journal of Neuroscience.

[41]  A. Mackey,et al.  Intensive Reasoning Training Alters Patterns of Brain Connectivity at Rest , 2013, The Journal of Neuroscience.

[42]  Timothy Edward John Behrens,et al.  Characterization and propagation of uncertainty in diffusion‐weighted MR imaging , 2003, Magnetic resonance in medicine.

[43]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[44]  N. Swindale,et al.  Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans , 2004, Annals of neurology.

[45]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[46]  Mara Cercignani,et al.  Twenty‐five pitfalls in the analysis of diffusion MRI data , 2010, NMR in biomedicine.

[47]  Morten H. Christiansen,et al.  Towards a theory of individual differences in statistical learning , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[48]  Y. Stern,et al.  Unilateral disruptions in the default network with aging in native space , 2013, Brain and behavior.

[49]  Chris I. Baker,et al.  Teaching an adult brain new tricks: A critical review of evidence for training-dependent structural plasticity in humans , 2013, NeuroImage.

[50]  Jean-Loup Guillaume,et al.  Fast unfolding of communities in large networks , 2008, 0803.0476.

[51]  Daniel C. McNamee,et al.  Characterizing the Associative Content of Brain Structures Involved in Habitual and Goal-Directed Actions in Humans: A Multivariate fMRI Study , 2015, The Journal of Neuroscience.

[52]  Jessica A. Turner,et al.  Behavioral Interpretations of Intrinsic Connectivity Networks , 2011, Journal of Cognitive Neuroscience.

[53]  R. C. Miall,et al.  Graph network analysis of immediate motor-learning induced changes in resting state BOLD , 2013, Front. Hum. Neurosci..

[54]  Patrick Dupont,et al.  Motor learning-induced changes in functional brain connectivity as revealed by means of graph-theoretical network analysis , 2012, NeuroImage.

[55]  M. Greicius,et al.  Decoding subject-driven cognitive states with whole-brain connectivity patterns. , 2012, Cerebral cortex.

[56]  Kevin Murphy,et al.  Resting-state fMRI confounds and cleanup , 2013, NeuroImage.

[57]  Kevin Murphy,et al.  Towards a consensus regarding global signal regression for resting state functional connectivity MRI , 2017, NeuroImage.

[58]  Peter B. Jones,et al.  Gene transcription profiles associated with inter-modular hubs and connection distance in human functional magnetic resonance imaging networks , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[59]  G. Deco,et al.  Spontaneous Brain Activity Predicts Learning Ability of Foreign Sounds , 2013, The Journal of Neuroscience.

[60]  Victor Alves,et al.  The Impact of Normalization and Segmentation on Resting-State Brain Networks , 2015, Brain Connect..

[61]  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.

[62]  M. V. D. Heuvel,et al.  Exploring the brain network: A review on resting-state fMRI functional connectivity , 2010, European Neuropsychopharmacology.

[63]  S. Hochstein,et al.  The reverse hierarchy theory of visual perceptual learning , 2004, Trends in Cognitive Sciences.

[64]  Luigi Acerbi,et al.  On the Origins of Suboptimality in Human Probabilistic Inference , 2014, PLoS Comput. Biol..

[65]  Anthony Randal McIntosh,et al.  Partial Least Squares (PLS) methods for neuroimaging: A tutorial and review , 2011, NeuroImage.

[66]  Cornelis J. Stam,et al.  Small-world and scale-free organization of voxel-based resting-state functional connectivity in the human brain , 2008, NeuroImage.

[67]  Richard S. J. Frackowiak,et al.  Evidence for Segregated and Integrative Connectivity Patterns in the Human Basal Ganglia , 2008, The Journal of Neuroscience.

[68]  L. Tyler,et al.  Robust Resilience of the Frontotemporal Syntax System to Aging , 2016, The Journal of Neuroscience.

[69]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[70]  Wolfgang M. Pauli,et al.  Regional specialization within the human striatum for diverse psychological functions , 2016, Proceedings of the National Academy of Sciences.

[71]  Marvin M. Chun,et al.  Neural Evidence of Statistical Learning: Efficient Detection of Visual Regularities Without Awareness , 2009, Journal of Cognitive Neuroscience.

[72]  Xenophon Papademetris,et al.  Groupwise whole-brain parcellation from resting-state fMRI data for network node identification , 2013, NeuroImage.

[73]  Timothy Edward John Behrens,et al.  Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging , 2003, Nature Neuroscience.

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

[75]  E. Newport,et al.  Science Current Directions in Psychological Statistical Learning : from Acquiring Specific Items to Forming General Rules on Behalf Of: Association for Psychological Science , 2022 .

[76]  Stamatios N. Sotiropoulos,et al.  An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging , 2016, NeuroImage.

[77]  O. Sporns,et al.  Network hubs in the human brain , 2013, Trends in Cognitive Sciences.

[78]  J. Kruskal On the shortest spanning subtree of a graph and the traveling salesman problem , 1956 .

[79]  Guillaume A. Rousselet,et al.  Robust Correlation Analyses: False Positive and Power Validation Using a New Open Source Matlab Toolbox , 2012, Front. Psychology.

[80]  R J HERRNSTEIN,et al.  Relative and absolute strength of response as a function of frequency of reinforcement. , 1961, Journal of the experimental analysis of behavior.

[81]  Stephen C. Mack,et al.  Rethinking human visual attention: Spatial cueing effects and optimality of decisions by honeybees, monkeys and humans , 2013, Vision Research.

[82]  Vince D. Calhoun,et al.  The effect of preprocessing pipelines in subject classification and detection of abnormal resting state functional network connectivity using group ICA , 2017, NeuroImage.

[83]  Joe Whittaker,et al.  Application of the Parametric Bootstrap to Models that Incorporate a Singular Value Decomposition , 1995 .

[84]  J. Rissanen,et al.  Modeling By Shortest Data Description* , 1978, Autom..

[85]  Zhaoyu Wei,et al.  The plunging cavities formed by the impinged jet after the entry of a sphere into water , 2014, J. Vis..

[86]  D. Shanks,et al.  A Re-examination of Probability Matching and Rational Choice , 2002 .

[87]  Jonathan K. Foster,et al.  Bone mineral density, adiposity, and cognitive functions , 2015, Front. Aging Neurosci..

[88]  P. Rousseeuw Silhouettes: a graphical aid to the interpretation and validation of cluster analysis , 1987 .

[89]  D. Levi,et al.  Perceptual learning in vernier acuity: What is learned? , 1995, Vision Research.

[90]  Peter T. Fox,et al.  Changes occur in resting state network of motor system during 4weeks of motor skill learning , 2011, NeuroImage.

[91]  C. Kelly,et al.  Strengthening Connections: Functional Connectivity and Brain Plasticity , 2014, Neuropsychology Review.

[92]  K. R. Ridderinkhof,et al.  Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning , 2004, Brain and Cognition.

[93]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[94]  Olaf Sporns,et al.  Network attributes for segregation and integration in the human brain , 2013, Current Opinion in Neurobiology.

[95]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[96]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[97]  V. Calhoun,et al.  Functional neural circuits for mental timekeeping , 2007, Human brain mapping.

[98]  Timothy Edward John Behrens,et al.  Diffusion-Weighted Imaging Tractography-Based Parcellation of the Human Lateral Premotor Cortex Identifies Dorsal and Ventral Subregions with Anatomical and Functional Specializations , 2007, The Journal of Neuroscience.

[99]  Anthony Randal McIntosh,et al.  Partial least squares analysis of neuroimaging data: applications and advances , 2004, NeuroImage.

[100]  Yu Zhang,et al.  The Human Brainnetome Atlas: A New Brain Atlas Based on Connectional Architecture , 2016, Cerebral cortex.

[101]  P. Tiňo,et al.  Learning predictive statistics from temporal sequences: Dynamics and strategies , 2017, Journal of vision.

[102]  Jonathan D. Cohen,et al.  Role of prefrontal cortex and the midbrain dopamine system in working memory updating , 2012, Proceedings of the National Academy of Sciences.

[103]  Richard F. Murray,et al.  Posterior Probability Matching and Human Perceptual Decision Making , 2015, PLoS Comput. Biol..

[104]  Bryon A. Mueller,et al.  Altered resting state complexity in schizophrenia , 2012, NeuroImage.

[105]  V Latora,et al.  Efficient behavior of small-world networks. , 2001, Physical review letters.

[106]  T. Robbins Shifting and stopping: fronto-striatal substrates, neurochemical modulation and clinical implications , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[107]  Edwin M. Robertson,et al.  The Resting Human Brain and Motor Learning , 2009, Current Biology.