Functional brain networks for learning predictive statistics

Joseph Giorgio, Vasilis M Karlaftis, Rui Wang, Yuan Shen, Peter Tino, Andrew Welchman, Zoe Kourtzi, Joseph Giorgio, Vasilis M Karlaftis, Rui Wang, Yuan Shen, Peter Tino, Andrew Welchman, Zoe Kourtzi

Abstract

Making predictions about future events relies on interpreting streams of information that may initially appear incomprehensible. This skill relies on extracting regular patterns in space and time by mere exposure to the environment (i.e., without explicit feedback). Yet, we know little about the functional brain networks that mediate this type of statistical learning. Here, we test whether changes in the processing and connectivity of functional brain networks due to training relate to our ability to learn temporal regularities. By combining behavioral training and functional brain connectivity analysis, we demonstrate that individuals adapt to the environment's statistics as they change over time from simple repetition to probabilistic combinations. Further, we show that individual learning of temporal structures relates to decision strategy. Our fMRI results demonstrate that learning-dependent changes in fMRI activation within and functional connectivity between brain networks relate to individual variability in strategy. In particular, extracting the exact sequence statistics (i.e., matching) relates to changes in brain networks known to be involved in memory and stimulus-response associations, while selecting the most probable outcomes in a given context (i.e., maximizing) relates to changes in frontal and striatal networks. Thus, our findings provide evidence that dissociable brain networks mediate individual ability in learning behaviorally-relevant statistics.

Keywords: Brain plasticity; Functional Network Connectivity; Individual differences; Statistical learning; fMRI.

Copyright © 2017 The Authors. Published by Elsevier Ltd.. All rights reserved.

Figures

Fig. 1
Fig. 1
Trial and sequence design. (a) The trial design: 8–14 symbols were presented sequentially followed by a cue and the test display. (b) Sequence design: Markov models of the two context-length levels. For the zero-order model (level-0): different states (A, B, C, D) are assigned to four symbols with different probabilities. For the first-order model (level-1), diagrams indicate states (circles) and conditional probabilities (solid arrows: high probability; dashed arrows: low probability). Transitional probabilities are shown in a four-by-four (level-1) conditional probability matrix, where rows indicate the context and columns the corresponding target.
Fig. 2
Fig. 2
Behavioral performance. (a) Mean normalized performance index (PI) across participants per level during pre-training (gray bars) and post-training (black bars) test sessions. Error bars indicate standard error of the mean across participants. (b) Strategy index boxplots for level-0 and level-1 indicate individual variability. The upper and lower error bars display the minimum and maximum data values and the central boxes represent the interquartile range (25th to 75th percentiles). The thick line in the central boxes represents the median. (c) Scatterplot of strategy index for level-0 against strategy index for level-1.
Fig. 3
Fig. 3
Spatial maps of ICA task-related components. 15 task-related components are shown organized into known functional groups (Allen et al., 2011). Spatial maps are thresholded at p < .005 (FWER corrected) and displayed in neurological convention (left is left) on the MNI template. The x, y, z coordinates per component denote the location of the sagittal, coronal and axial slices, respectively.
Fig. 4
Fig. 4
ICA components related to matching strategy. Average spatial maps showing significant negative correlation of BOLD change (post minus pre-training) with strategy index for (a) Learning frequency statistics: Precuneus, Sensorimotor and Right Central Executive. (b) Learning context-based statistics: Precuneus and Middle Temporal. Spatial maps are averaged across sessions, thresholded at p < .005 (FWER corrected) and displayed in neurological convention (left is left) on the MNI template. Open circles in the correlation plots denote outliers.
Fig. 5
Fig. 5
ICA components related to maximization strategy. Average spatial maps showing significant positive correlation of BOLD change (post minus pre-training) with strategy index for: (a) Learning frequency statistics: Basal Ganglia. (b) Learning context-based statistics: Left Central Executive. Spatial maps are averaged across sessions, thresholded at p < .005 (FWER corrected) and displayed in neurological convention (left is left) on the MNI template.
Fig. 6
Fig. 6
Functional Network Connectivity (FNC) change related to strategy. Correlation matrix of FNC change (post minus pre-training) with strategy index for: (a) frequency statistics and (b) context-based statistics. Black dots indicate significant positive, while black diamonds significant negative correlations (at 95% bootstrapped confidence intervals) of FNC change with strategy index. ICA components included in this analysis are: Left Central Executive Network (lCEN), Right Central Executive Network (rCEN), Middle Temporal (MT), Precuneus (PRCUN), Basal Ganglia (BG) and Sensorimotor (SM).

References

    1. Acerbi L., Vijayakumar S., Wolpert D.M. On the origins of suboptimality in human probabilistic inference. PLoS Computational Biology. 2014;10
    1. Aizenstein H.J., Stenger A.V., Cochran J., Clark K., Johnson M., Nebes R.D. Regional brain activation during concurrent implicit and explicit sequence learning. Cerebral Cortex. 2004;14:199–208.
    1. Albouy G., Sterpenich V., Balteau E., Vandewalle G., Desseilles M., Dang-Vu T. Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron. 2008;58:261–272.
    1. Alexander G.E., DeLong M.R., Strick P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience. 1986;9:357–381.
    1. Allen E.A., Erhardt E.B., Damaraju E., Gruner W., Segall J.M., Silva R.F. A baseline for the multivariate comparison of resting-state networks. Frontiers in Systems Neuroscience. 2011;5:2.
    1. Antoniou M., Ettlinger M., Wong P.C. Complexity, training paradigm design, and the contribution of memory subsystems to grammar learning. PLoS One. 2016;11
    1. Antzoulatos E.G., Miller E.K. Increases in functional connectivity between prefrontal cortex and striatum during category learning. Neuron. 2014;83:216–225.
    1. Ashby F.G., Maddox W.T. Human category learning. Annual Review of Psychology. 2005;56:149–178.
    1. Aslin R.N., Newport E.L. Statistical learning: From acquiring specific items to forming general rules. Current Directions in Psychological Science. 2012;21:170–176.
    1. Baldassarre A., Lewis C.M., Committeri G., Snyder A.Z., Romani G.L., Corbetta M. Individual variability in functional connectivity predicts performance of a perceptual task. Proceedings of the National Academy of Sciences. 2012;109:3516–3521.
    1. Balleine B.W., O'Doherty J.P. Human and rodent homologies in action control: Corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology. 2010;35:48–69.
    1. Bassett D.S., Wymbs N.F., Porter M.A., Mucha P.J., Carlson J.M., Grafton S.T. Dynamic reconfiguration of human brain networks during learning. Proceedings of the National Academy of Sciences. 2011;108:7641–7646.
    1. van den Bos E., Poletiek F.H. Effects of grammar complexity on artificial grammar learning. Memory & Cognition. 2008;36:1122–1131.
    1. Brainard D.H. The psychophysics toolbox. Spatial Vision. 1997;10:433–436.
    1. Cabeza R., Ciaramelli E., Olson I.R., Moscovitch M. The parietal cortex and episodic memory: An attentional account. Nature Reviews Neuroscience. 2008;9:613–625.
    1. Calhoun V.D., Adali T. Multisubject independent component analysis of fMRI: A decade of intrinsic networks, default mode, and neurodiagnostic discovery. IEEE Reviews in Biomedical Engineering. 2012;5:60–73.
    1. Calhoun V.D., Liu J., Adali T. A review of group ICA for fMRI data and ICA for joint inference of imaging, genetic, and ERP data. NeuroImage. 2009;45:163–172.
    1. Chun M.M. Contextual cueing of visual attention. Trends in Cognitive Sciences. 2000;4:170–178.
    1. Chun M., Jiang Y. Contextual cueing: Implicit learning and memory of visual context guides spatial attention. Cognitive Psychology. 1998;36:28–71.
    1. Cools R., Clark L., Owen A.M., Robbins T.W. Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging. The Journal of Neuroscience. 2002;22:4563–4567.
    1. Cools R., Clark L., Robbins T.W. Differential responses in human striatum and prefrontal cortex to changes in object and rule relevance. Journal of Neuroscience. 2004;24:1129–1135.
    1. Dale R., Duran N.D., Morehead J.R. Prediction during statistical learning, and implications for the implicit/explicit divide. Advances in Cognitive Psychology. 2012;8:196–209.
    1. D'Ardenne K., Eshel N., Luka J., Lenartowicz A., Nystrom L.E., Cohen J.D. Role of prefrontal cortex and the midbrain dopamine system in working memory updating. Proceedings of the National Academy of Sciences. 2012;109:19900–19909.
    1. Eckstein M.P., Mack S.C., Liston D.B., Bogush L., Menzel R., Krauzlis R.J. Rethinking human visual attention: Spatial cueing effects and optimality of decisions by honeybees, monkeys and humans. Vision Research. 2013;85:5–9.
    1. Erev I., Barron G. On adaptation, maximization, and reinforcement learning among cognitive strategies. Psychological Review. 2005;112:912–931.
    1. Fiser J., Aslin R.N. Statistical learning of higher-order temporal structure from visual shape sequences. Journal of Experimental Psychology: Learning, Memory, and Cognition. 2002;28:458–467.
    1. Fiser J., Aslin R.N. Encoding multielement scenes: Statistical learning of visual feature hierarchies. Journal of Experimental Psychology: General. 2005;134:521.
    1. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews Neuroscience. 2007;8:700–711.
    1. Fulvio J.M., Green C.S., Schrater P.R. Task-specific response strategy selection on the basis of recent training experience. PLoS Computational Biology. 2014;10
    1. Gheysen F., Van Opstal F., Roggeman C., Van Waelvelde H., Fias W. The neural basis of implicit perceptual sequence learning. Frontiers in Human Neuroscience. 2011;5
    1. Gluck M.A., Shohamy D., Myers C. How do people solve the “weather prediction” task?: Individual variability in strategies for probabilistic category learning. Learning & Memory. 2002;9:408–418.
    1. Haberecht M.F., Menon V., Warsofsky I.S., White C.D., Dyer-Friedman J., Glover G.H. Functional neuroanatomy of visuo-spatial working memory in turner syndrome. Human Brain Mapping. 2001;14:96–107.
    1. Himberg J., Hyvärinen A., Esposito F. Validating the independent components of neuroimaging time series via clustering and visualization. NeuroImage. 2004;22:1214–1222.
    1. Hsieh L.T., Gruber M.J., Jenkins L.J., Ranganath C. Hippocampal activity patterns carry information about objects in temporal context. Neuron. 2014;81:1165–1178.
    1. Jafri M.J., Pearlson G.D., Stevens M., Calhoun V.D. A method for functional network connectivity among spatially independent resting-state components in schizophrenia. NeuroImage. 2008;39:1666–1681.
    1. Knowlton B.J., Squire L.R., Gluck M.A. Probabilistic classification learning in amnesia. Learning & Memory. 1994;1:106–120.
    1. Lagnado D.A., Newell B.R., Kahan S., Shanks D.R. Insight and strategy in multiple-cue learning. Journal of Experimental Psychology: General. 2006;135:162.
    1. Lawrence A.D., Sahakian B.J., Robbins T.W. Cognitive functions and corticostriatal circuits: Insights from Huntington's disease. Trends in Cognitive Sciences. 1998;2:379–388.
    1. Lee I.A., Preacher K.J. 2013. Calculation for the test of the difference between two dependent correlations with one variable in common.
    1. Lewis C.M., Baldassarre A., Committeri G., Romani G.L., Corbetta M. Learning sculpts the spontaneous activity of the resting human brain. Proceedings of the National Academy of Sciences. 2009;106:17558–17563.
    1. Ma L., Narayana S., Robin D.A., Fox P.T., Xiong J. Changes occur in resting state network of motor system during 4 weeks of motor skill learning. NeuroImage. 2011;58:226–233.
    1. McKeown M.J., Makeig S., Brown G.G., Jung T.P., Kindermann S.S., Bell A.J. Analysis of fMRI data by blind separation into independent spatial components. Human Brain Mapping. 1998;6:160–188.
    1. Monchi O., Petrides M., Petre V., Worsley K., Dagher A. Wisconsin card sorting revisited: Distinct neural circuits participating in different stages of the task identified by event-related functional magnetic resonance imaging. The Journal of Neuroscience. 2001;21:7733–7741.
    1. Muellbacher W., Ziemann U., Wissel J., Dang N., Kofler M., Facchini S. Early consolidation in human primary motor cortex. Nature. 2002;415:640–644.
    1. Murray R.F., Patel K., Yee A. Posterior probability matching and human perceptual decision making. PLoS Computational Biology. 2015;11
    1. Nissen M.J., Bullemer P. Attentional requirements of learning: Evidence from performance measures. Cognitive Psychology. 1987;19:1–32.
    1. Nyberg L., Forkstam C., Petersson K.M., Cabeza R., Ingvar M. Brain imaging of human memory systems: Between-systems similarities and within-system differences. Cognitive Brain Research. 2002;13:281–292.
    1. Pasupathy A., Miller E.K. Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature. 2005;433:873–876.
    1. Pelli D.G. The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision. 1997;10:437–442.
    1. Pernet C.R., Wilcox R., Rousselet G.A. Robust correlation Analyses: False positive and power validation using a new open source Matlab toolbox. Frontiers in Psychology. 2013;3
    1. Perruchet P., Pacton S. Implicit learning and statistical learning: One phenomenon, two approaches. Trends in Cognitive Sciences. 2006;10:233–238.
    1. Rauch S.L., Whalen P.J., Savage C.R., Curran T., Kendrick A., Brown H.D. Striatal recruitment during an implicit sequence learning task as measured by functional magnetic resonance imaging. Human Brain Mapping. 1997;5:124–132.
    1. Reber A.S. Implicit learning of artificial grammars. Journal of Verbal Learning and Verbal Behavior. 1967;6:855–863.
    1. Ridderinkhof K.R., van den Wildenberg W.P., Segalowitz S.J., Carter C.S. Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain and Cognition. 2004;56:129–140.
    1. Rieskamp J., Otto P.E. SSL: A theory of how people learn to select strategies. Journal of Experimental Psychology: General. 2006;135:207–236.
    1. Rissanen J. Modeling by shortest data description. Automatica. 1978;14:465–471.
    1. Robbins T.W. Shifting and stopping: Fronto-striatal substrates, neurochemical modulation and clinical implications. Philosophical Transactions of the Royal Society B: Biological Sciences. 2007;362:917–932.
    1. Rose M., Haider H., Salari N., Buchel C. Functional dissociation of hippocampal mechanism during implicit learning based on the domain of associations. Journal of Neuroscience. 2011;31:13739–13745.
    1. Saffran J.R., Aslin R.N., Newport E.L. Statistical learning by 8-month-old infants. Science. 1996;274:1926–1928.
    1. Saffran J.R., Johnson E.K., Aslin R.N., Newport E.L. Statistical learning of tone sequences by human infants and adults. Cognition. 1999;70:27–52.
    1. Schapiro A.C., Kustner L.V., Turk-Browne N.B. Shaping of object representations in the human medial temporal lobe based on temporal regularities. Current Biology. 2012;22:1622–1627.
    1. Schendan H.E., Searl M.M., Melrose R.J., Stern C.E. An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron. 2003;37:1013–1025.
    1. Schwarb H., Schumacher E. Generalized lessons about sequence learning from the study of the serial reaction time task. Advances in Cognitive Psychology. 2012;8:165–178.
    1. Seger C.A. Implicit learning. Psychological Bulletin. 1994;115:163–196.
    1. Seger C.A., Cincotta C.M. Dynamics of frontal, striatal, and hippocampal systems during rule learning. Cerebral Cortex. 2005;16:1546–1555.
    1. Seger C.A., Poldrack R.A., Prabhakaran V., Zhao M., Glover G.H., Gabrieli J.D. Hemispheric asymmetries and individual differences in visual concept learning as measured by functional MRI. Neuropsychologia. 2000;38:1316–1324.
    1. Shanks D.R., Tunney R.J., McCarthy J.D. A re-examination of probability matching and rational choice. Journal of Behavioral Decision Making. 2002;15:233–250.
    1. Shohamy D., Myers C.E., Kalanithi J., Gluck M.A. Basal ganglia and dopamine contributions to probabilistic category learning. Neuroscience and Biobehavioral Reviews. 2008;32:219–236.
    1. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E. Correspondence of the brain's functional architecture during activation and rest. Proceedings of the National Academy of Sciences of the United States of America. 2009;106:13040–13045.
    1. St. Jacques P.L., Kragel P.A., Rubin D.C. Dynamic neural networks supporting memory retrieval. NeuroImage. 2011;57:608–616.
    1. Stevens M.C., Kiehl K.A., Pearlson G., Calhoun V.D. Functional neural circuits for mental timekeeping. Human Brain Mapping. 2007;28:394–408.
    1. Sun F.T., Miller L.M., Rao A.A., D'esposito M. Functional connectivity of cortical networks involved in bimanual motor sequence learning. Cerebral Cortex. 2007;17:1227–1234.
    1. Taylor J.R., Williams N., Cusack R., Auer T., Shafto M.A., Dixon M. The Cambridge Centre for Ageing and Neuroscience (Cam-CAN) data repository: Structural and functional MRI, MEG, and cognitive data from a cross-sectional adult lifespan sample. NeuroImage. 2015;144:262–269.
    1. Turk-Browne N.B., Junge J., Scholl B.J. The automaticity of visual statistical learning. Journal of Experimental Psychology. General. 2005;134:552–564.
    1. Turk-Browne N.B., Scholl B.J., Johnson M.K., Chun M.M. Implicit perceptual anticipation triggered by statistical learning. The Journal of Neuroscience. 2010;30:11177–11187.
    1. Van Dijk K.R., Hedden T., Venkataraman A., Evans K.C., Lazar S.W., Buckner R.L. Intrinsic functional connectivity as a tool for human connectomics: Theory, properties, and optimization. Journal of Neurophysiology. 2010;103:297–321.
    1. Ventura-Campos N., Sanjuan A., Gonzalez J., Palomar-Garcia M.-A., Rodriguez-Pujadas A., Sebastian-Galles N. Spontaneous brain activity predicts learning ability of Foreign sounds. Journal of Neuroscience. 2013;33:9295–9305.
    1. Veroude K., Norris D.G., Shumskaya E., Gullberg M., Indefrey P. Functional connectivity between brain regions involved in learning words of a new language. Brain and Language. 2010;113:21–27.
    1. Vincent J.L., Kahn I., Snyder A.Z., Raichle M.E., Buckner R.L. Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. Journal of neurophysiology. 2008;100:3328–3342.
    1. Vincent J.L., Snyder A.Z., Fox M.D., Shannon B.J., Andrews J.R., Raichle M.E. Coherent spontaneous activity identifies a hippocampal-parietal memory network. Journal of Neurophysiology. 2006;96:3517–3531.
    1. Wagner A.D., Shannon B.J., Kahn I., Buckner R.L. Parietal lobe contributions to episodic memory retrieval. Trends in Cognitive Sciences. 2005;9:445–453.
    1. Wang, R., Shen, Y., Tino, P., Welchman, A., & Kourtzi, Z. (in press). Learning predictive statistics from temporal sequences: dynamics and strategies. Journal of Vision
    1. Wozny D.R., Beierholm U.R., Shams L. Probability matching as a computational strategy used in perception. PLoS Computational Biology. 2010;6

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