Neural Signatures of Spatial Statistical Learning: Characterizing the Extraction of Structure from Complex Visual Scenes

Behavioral evidence has shown that humans automatically develop internal representations adapted to the temporal and spatial statistics of the environment. Building on prior fMRI studies that have focused on statistical learning of temporal sequences, we investigated the neural substrates and mechanisms underlying statistical learning from scenes with a structured spatial layout. Our goals were twofold: (1) to determine discrete brain regions in which degree of learning (i.e., behavioral performance) was a significant predictor of neural activity during acquisition of spatial regularities and (2) to examine how connectivity between this set of areas and the rest of the brain changed over the course of learning. Univariate activity analyses indicated a diffuse set of dorsal striatal and occipitoparietal activations correlated with individual differences in participants' ability to acquire the underlying spatial structure of the scenes. In addition, bilateral medial-temporal activation was linked to participants' behavioral performance, suggesting that spatial statistical learning recruits additional resources from the limbic system. Connectivity analyses examined, across the time course of learning, psychophysiological interactions with peak regions defined by the initial univariate analysis. Generally, we find that task-based connectivity with these regions was significantly greater in early relative to later periods of learning. Moreover, in certain cases, decreased task-based connectivity between time points was predicted by overall posttest performance. Results suggest a narrowing mechanism whereby the brain, confronted with a novel structured environment, initially boosts overall functional integration and then reduces interregional coupling over time.

[1]  J. DiCarlo,et al.  Unsupervised Natural Visual Experience Rapidly Reshapes Size-Invariant Object Representation in Inferior Temporal Cortex , 2010, Neuron.

[2]  Scott A. Guerin,et al.  Both memory and attention systems contribute to visual search for targets cued by implicitly learned context , 2013, Vision Research.

[3]  Chandan J. Vaidya,et al.  Atypical modulation of distant functional connectivity by cognitive state in children with Autism Spectrum Disorders , 2013, Front. Hum. Neurosci..

[4]  Stefan Pollmann,et al.  Early implicit contextual change detection in anterior prefrontal cortex , 2009, Brain Research.

[5]  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 .

[6]  Habib Benali,et al.  Dynamics of motor-related functional integration during motor sequence learning , 2010, NeuroImage.

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

[8]  Marcia K. Johnson,et al.  Implicit Perceptual Anticipation Triggered by Statistical Learning , 2010, The Journal of Neuroscience.

[9]  Karl J. Friston,et al.  Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution , 2003, NeuroImage.

[10]  Richard N. Aslin,et al.  Right Hemisphere Dominance in Visual Statistical Learning , 2011, Journal of Cognitive Neuroscience.

[11]  Danielle S Bassett,et al.  Learning-induced autonomy of sensorimotor systems , 2014, Nature Neuroscience.

[12]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[13]  R. Vogels,et al.  Spatial sensitivity of macaque inferior temporal neurons , 2000, The Journal of comparative neurology.

[14]  Stefan Pollmann,et al.  Dorsal and ventral working memory-related brain areas support distinct processes in contextual cueing , 2013, NeuroImage.

[15]  Barbara Landau,et al.  The Necessity of the Medial Temporal Lobe for Statistical Learning , 2014, Journal of Cognitive Neuroscience.

[16]  M. N. Rajah,et al.  Interactions of prefrontal cortex in relation to awareness in sensory learning. , 1999, Science.

[17]  R. Aslin,et al.  Statistical learning of higher-order temporal structure from visual shape sequences. , 2002, Journal of experimental psychology. Learning, memory, and cognition.

[18]  R. Aslin,et al.  Encoding multielement scenes: statistical learning of visual feature hierarchies. , 2005, Journal of experimental psychology. General.

[19]  Russell A. Epstein,et al.  Neuropsychological evidence for a topographical learning mechanism in parahippocampal cortex , 2001, Cognitive neuropsychology.

[20]  William L. Gross,et al.  Hippocampal differentiation without recognition: an fMRI analysis of the contextual cueing task. , 2007, Learning & memory.

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

[22]  Thomas Serre,et al.  Object decoding with attention in inferior temporal cortex , 2011, Proceedings of the National Academy of Sciences.

[23]  Kyle R. Almryde,et al.  The nature of the language input affects brain activation during learning from a natural language , 2015, Journal of Neurolinguistics.

[24]  O. Sporns,et al.  Network neuroscience , 2017, Nature Neuroscience.

[25]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[26]  Jean-Louis Millot,et al.  Enhancement of spatial learning by predator odor in mice: Involvement of amygdala and hippocampus , 2010, Neurobiology of Learning and Memory.

[27]  Ping Li,et al.  Neural changes underlying successful second language word learning: An fMRI study , 2015, Journal of Neurolinguistics.

[28]  J. D. McGaugh,et al.  Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[29]  A. Damasio,et al.  Role of the Amygdala in Decision‐Making , 2003, Annals of the New York Academy of Sciences.

[30]  Shane T. Mueller,et al.  A note on ROC analysis and non-parametric estimate of sensitivity , 2005 .

[31]  Yasushi Miyashita,et al.  Consolidation of Visual Associative Long-Term Memory in the Temporal Cortex of Primates , 1998, Neurobiology of Learning and Memory.

[32]  Lynne M Reder,et al.  Procedural learning and associative memory mechanisms contribute to contextual cueing: Evidence from fMRI and eye-tracking. , 2012, Learning & memory.

[33]  J. Mazziotta,et al.  Cracking the Language Code: Neural Mechanisms Underlying Speech Parsing , 2006, The Journal of Neuroscience.

[34]  M. Chun,et al.  Contextual Cueing: Implicit Learning and Memory of Visual Context Guides Spatial Attention , 1998, Cognitive Psychology.

[35]  M. D’Esposito,et al.  The parahippocampus subserves topographical learning in man , 1996, NeuroImage.

[36]  Kazuo Okanoya,et al.  On-line Assessment of Statistical Learning by Event-related Potentials , 2008, Journal of Cognitive Neuroscience.

[37]  Gal Richter-Levin,et al.  Amygdala-hippocampus dynamic interaction in relation to memory , 2000, Molecular Neurobiology.

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

[39]  Uri Hasson,et al.  Multiple sensitivity profiles to diversity and transition structure in non-stationary input , 2012, NeuroImage.

[40]  Richard N Aslin,et al.  Statistical learning of new visual feature combinations by infants , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Freja Gheysen,et al.  Hippocampal contribution to early and later stages of implicit motor sequence learning , 2010, Experimental Brain Research.

[42]  Y. Miyashita Inferior temporal cortex: where visual perception meets memory. , 1993, Annual review of neuroscience.

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

[44]  K J Friston,et al.  The predictive value of changes in effective connectivity for human learning. , 1999, Science.

[45]  Matthew Flatt,et al.  PsyScope: An interactive graphic system for designing and controlling experiments in the psychology laboratory using Macintosh computers , 1993 .

[46]  Keith J. Worsley,et al.  Statistical analysis of activation images , 2001 .

[47]  Richard N. Aslin,et al.  Sampling over Nonuniform Distributions: A Neural Efficiency Account of the Primacy Effect in Statistical Learning , 2016, Journal of Cognitive Neuroscience.

[48]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[49]  Scott P. Johnson,et al.  Visual statistical learning in infancy: evidence for a domain general learning mechanism , 2002, Cognition.

[50]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[51]  Richard N. Aslin,et al.  The neural correlates of statistical learning in a word segmentation task: An fMRI study , 2013, Brain and Language.

[52]  A. Kelly,et al.  Human functional neuroimaging of brain changes associated with practice. , 2005, Cerebral cortex.

[53]  Go Uchida,et al.  Object Representation in Inferior Temporal Cortex Is Organized Hierarchically in a Mosaic-Like Structure , 2013, The Journal of Neuroscience.

[54]  Lee M. Miller,et al.  Functional connectivity of cortical networks involved in bimanual motor sequence learning. , 2006, Cerebral cortex.

[55]  E. Phelps Emotion and cognition: insights from studies of the human amygdala. , 2006, Annual review of psychology.

[56]  R. Aslin,et al.  PSYCHOLOGICAL SCIENCE Research Article UNSUPERVISED STATISTICAL LEARNING OF HIGHER-ORDER SPATIAL STRUCTURES FROM VISUAL SCENES , 2022 .

[57]  Timothy E. J. Behrens,et al.  Tools of the trade: psychophysiological interactions and functional connectivity. , 2012, Social cognitive and affective neuroscience.

[58]  Josep Marco-Pallarés,et al.  Time course and functional neuroanatomy of speech segmentation in adults , 2009, NeuroImage.

[59]  K. Okanoya,et al.  Statistical segmentation of tone sequences activates the left inferior frontal cortex: A near-infrared spectroscopy study , 2008, Neuropsychologia.

[60]  Marco Baroni,et al.  Processing of speech and non-speech sounds in the supratemporal plane: Auditory input preference does not predict sensitivity to statistical structure , 2013, NeuroImage.

[61]  Uri Hasson,et al.  Neural systems mediating recognition of changes in statistical regularities , 2012, NeuroImage.