Implicit Perceptual Anticipation Triggered by Statistical Learning

Our environments are highly regular in terms of when and where objects appear relative to each other. Statistical learning allows us to extract and represent these regularities, but how this knowledge is used by the brain during ongoing perception is unclear. We used rapid event-related fMRI to measure hemodynamic responses to individual visual images in a continuous stream that contained sequential contingencies. Sixteen human observers encountered these statistical regularities while performing an unrelated cognitive task, and were unaware of their existence. Nevertheless, the right anterior hippocampus showed greater hemodynamic responses to predictive stimuli, providing evidence for implicit anticipation as a consequence of unsupervised statistical learning. Hippocampal anticipation based on predictive stimuli correlated with subsequent processing of the predicted stimuli in occipital and parietal cortex, and anticipation in additional brain regions correlated with facilitated object recognition as reflected in behavioral priming. Additional analyses suggested that implicit perceptual anticipation does not contribute to explicit familiarity, but can result in predictive potentiation of category-selective ventral visual cortex. Overall, these findings show that future-oriented processing can arise incidentally during the perception of statistical regularities.

[1]  F. W. Irwin Purposive Behavior in Animals and Men , 1932, The Psychological Clinic.

[2]  D Marr,et al.  Simple memory: a theory for archicortex. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[3]  J. Grier,et al.  Nonparametric indexes for sensitivity and bias: computing formulas. , 1971, Psychological bulletin.

[4]  Marcia K. Johnson A multiple-entry, modular memory system , 1983 .

[5]  L R Squire,et al.  Paired-associate learning and priming effects in amnesia: a neuropsychological study. , 1984, Journal of experimental psychology. General.

[6]  P. A. Kolers,et al.  Procedures of mind. , 1984 .

[7]  M. Lévesque Perception , 1986, The Yale Journal of Biology and Medicine.

[8]  R. F. Thompson,et al.  Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. , 1986, Behavioral neuroscience.

[9]  M. Nissen,et al.  Attentional requirements of learning: Evidence from performance measures , 1987, Cognitive Psychology.

[10]  D. Aaronson,et al.  Extensions of Grier's computational formulas for A' and B'' to below-chance performance. , 1987, Psychological bulletin.

[11]  Y. Miyashita Neuronal correlate of visual associative long-term memory in the primate temporal cortex , 1988, Nature.

[12]  Y. Miyashita,et al.  Neural organization for the long-term memory of paired associates , 1991, Nature.

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

[14]  J. Hodges Memory, Amnesia and the Hippocampal System , 1995 .

[15]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[16]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[17]  R N Aslin,et al.  Statistical Learning by 8-Month-Old Infants , 1996, Science.

[18]  T. Allison,et al.  Face-Specific Processing in the Human Fusiform Gyrus , 1997, Journal of Cognitive Neuroscience.

[19]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[20]  Karl J. Friston,et al.  Characterizing Stimulus–Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments , 1998, NeuroImage.

[21]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[22]  E. Newport,et al.  Computation of Conditional Probability Statistics by 8-Month-Old Infants , 1998 .

[23]  M. D’Esposito,et al.  An Area within Human Ventral Cortex Sensitive to “Building” Stimuli Evidence and Implications , 1998, Neuron.

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

[25]  M. Chun,et al.  Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage , 1999, Nature Neuroscience.

[26]  T. Shallice,et al.  Recollection and Familiarity in Recognition Memory: An Event-Related Functional Magnetic Resonance Imaging Study , 1999, The Journal of Neuroscience.

[27]  R. Desimone,et al.  Responses of Macaque Perirhinal Neurons during and after Visual Stimulus Association Learning , 1999, The Journal of Neuroscience.

[28]  A. Dickinson,et al.  Neuronal coding of prediction errors. , 2000, Annual review of neuroscience.

[29]  R. Buckner,et al.  Neural Correlates of Episodic Retrieval Success , 2000, NeuroImage.

[30]  Marcia K. Johnson,et al.  fMRI evidence of age-related hippocampal dysfunction in feature binding in working memory. , 2000, Brain research. Cognitive brain research.

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

[32]  M. Chun,et al.  Temporal contextual cuing of visual attention. , 2001, Journal of experimental psychology. Learning, memory, and cognition.

[33]  R. Aslin,et al.  Statistical learning in a serial reaction time task: access to separable statistical cues by individual learners. , 2001, Journal of experimental psychology. General.

[34]  Eero P. Simoncelli,et al.  Natural image statistics and neural representation. , 2001, Annual review of neuroscience.

[35]  L. Squire,et al.  Perceptual learning, awareness, and the hippocampus , 2001, Hippocampus.

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

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

[38]  C. Büchel,et al.  The Role of Medial Temporal Lobe Structures in Implicit Learning An Event-Related fMRI Study , 2002, Neuron.

[39]  L. Davachi,et al.  Hippocampal contributions to episodic encoding: insights from relational and item-based learning. , 2002, Journal of neurophysiology.

[40]  Katharina Henke,et al.  Nonconscious formation and reactivation of semantic associations by way of the medial temporal lobe , 2003, Neuropsychologia.

[41]  C. Stern,et al.  An fMRI Study of the Role of the Medial Temporal Lobe in Implicit and Explicit Sequence Learning , 2003, Neuron.

[42]  R. O’Reilly,et al.  Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. , 2003, Psychological review.

[43]  M. Shapiro,et al.  Prospective and Retrospective Memory Coding in the Hippocampus , 2003, Neuron.

[44]  L. Chelazzi,et al.  Associative knowledge controls deployment of visual selective attention , 2003, Nature Neuroscience.

[45]  S. M. Daselaar,et al.  When less means more: deactivations during encoding that predict subsequent memory , 2004, NeuroImage.

[46]  M. Behrmann,et al.  Role of attention and perceptual grouping in visual statistical learning. , 2004, Psychological science.

[47]  Marc W Howard,et al.  The temporal context model in spatial navigation and relational learning: toward a common explanation of medial temporal lobe function across domains. , 2005, Psychological review.

[48]  Christian Büchel,et al.  Unconscious Detection of Implicit Expectancies , 2005, Journal of Cognitive Neuroscience.

[49]  Karl J. Friston,et al.  A theory of cortical responses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[50]  Raymond J. Dolan,et al.  Information theory, novelty and hippocampal responses: unpredicted or unpredictable? , 2005, Neural Networks.

[51]  B. Scholl,et al.  The Automaticity of Visual Statistical Learning Statistical Learning , 2005 .

[52]  Jeffrey C. Cooper,et al.  Functional magnetic resonance imaging of reward prediction , 2005, Current opinion in neurology.

[53]  J. Lisman,et al.  Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer , 2005, Trends in Neurosciences.

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

[55]  Paul J Reber,et al.  Priming effects in the fusiform gyrus: changes in neural activity beyond the second presentation. , 2005, Cerebral cortex.

[56]  Rainer Goebel,et al.  Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single‐subject to cortically aligned group general linear model analysis and self‐organizing group independent component analysis , 2006, Human brain mapping.

[57]  E. Halgren,et al.  Top-down facilitation of visual recognition. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[58]  P. Perruchet,et al.  Implicit learning and statistical learning: one phenomenon, two approaches , 2006, Trends in Cognitive Sciences.

[59]  A. Nobre,et al.  Orienting Attention Based on Long-Term Memory Experience , 2006, Neuron.

[60]  Karl J. Friston,et al.  Encoding uncertainty in the hippocampus , 2006, Neural Networks.

[61]  M. Chun,et al.  Linking Implicit and Explicit Memory: Common Encoding Factors and Shared Representations , 2006, Neuron.

[62]  Jennifer A. Mangels,et al.  Predictive Codes for Forthcoming Perception in the Frontal Cortex , 2006, Science.

[63]  W. Schultz Behavioral theories and the neurophysiology of reward. , 2006, Annual review of psychology.

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

[65]  Daniel L Schacter,et al.  Evidence for a specific role of the anterior hippocampal region in successful associative encoding , 2007, Hippocampus.

[66]  D. Kumaran,et al.  Which computational mechanisms operate in the hippocampus during novelty detection? , 2007, Hippocampus.

[67]  D. Hassabis,et al.  Patients with hippocampal amnesia cannot imagine new experiences , 2007, Proceedings of the National Academy of Sciences.

[68]  Marcia K. Johnson,et al.  A brief thought can modulate activity in extrastriate visual areas: Top-down effects of refreshing just-seen visual stimuli , 2007, NeuroImage.

[69]  M. Bar,et al.  The parahippocampal cortex mediates spatial and nonspatial associations. , 2007, Cerebral cortex.

[70]  Adam Johnson,et al.  Neural Ensembles in CA3 Transiently Encode Paths Forward of the Animal at a Decision Point , 2007, The Journal of Neuroscience.

[71]  M. Bar The proactive brain: using analogies and associations to generate predictions , 2007, Trends in Cognitive Sciences.

[72]  R. Buckner,et al.  Opinion TRENDS in Cognitive Sciences Vol.11 No.2 Self-projection and the brain , 2022 .

[73]  Alana T. Wong,et al.  Remembering the past and imagining the future: Common and distinct neural substrates during event construction and elaboration , 2007, Neuropsychologia.

[74]  Jim M. Monti,et al.  Neural repetition suppression reflects fulfilled perceptual expectations , 2008, Nature Neuroscience.

[75]  Richard N Aslin,et al.  Bayesian learning of visual chunks by human observers , 2008, Proceedings of the National Academy of Sciences.

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

[77]  C. Summerfield,et al.  A Neural Representation of Prior Information during Perceptual Inference , 2008, Neuron.

[78]  J. Desmond,et al.  Neural substrates underlying human delay and trace eyeblink conditioning , 2008, Proceedings of the National Academy of Sciences.

[79]  M. Moscovitch,et al.  The parietal cortex and episodic memory: an attentional account , 2008, Nature Reviews Neuroscience.

[80]  B. Scholl,et al.  Multidimensional Visual Statistical Learning Visual Statistical Learning , 2005 .

[81]  Timothy F. Brady,et al.  PSYCHOLOGICAL SCIENCE Research Article Statistical Learning Using Real-World Scenes Extracting Categorical Regularities Without Conscious Intent , 2022 .

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

[83]  R. Nathan Spreng,et al.  The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis , 2009, Journal of Cognitive Neuroscience.

[84]  B. Scholl,et al.  Flexible visual statistical learning: transfer across space and time. , 2009, Journal of experimental psychology. Human perception and performance.

[85]  Kazuo Okanoya,et al.  Visual statistical learning of shape sequences: An ERP study , 2009, Neuroscience Research.

[86]  Karl J. Friston,et al.  A Dual Role for Prediction Error in Associative Learning , 2008, Cerebral cortex.

[87]  Emily J. Ward,et al.  How reliable are visual context effects in the parahippocampal place area? , 2010, Cerebral cortex.

[88]  Karl J. Friston,et al.  Behavioral / Systems / Cognitive Striatal Prediction Error Modulates Cortical Coupling , 2010 .