Retrieval of Associative Information Congruent with Prior Knowledge Is Related to Increased Medial Prefrontal Activity and Connectivity

We remember information that is congruent instead of incongruent with prior knowledge better, but the underlying neural mechanisms related to this enhancement are still relatively unknown. Recently, this memory enhancement due to a prior schema has been suggested to be based on rapid neocortical assimilation of new information, related to optimized encoding and consolidation processes. The medial prefrontal cortex (mPFC) is thought to be important in mediating this process, but its role in retrieval of schema-consistent information is still unclear. In this study, we regarded multisensory congruency with prior knowledge as a schema and used this factor to probe retrieval of consolidated memories either consistent or inconsistent with prior knowledge. We conducted a visuotactile learning paradigm in which participants studied visual motifs randomly associated with word–fabric combinations that were either congruent or incongruent with common knowledge. The next day, participants were scanned using functional magnetic resonance imaging while their memory was tested. Congruent associations were remembered better than incongruent ones. This behavioral finding was parallelized by stronger retrieval-related activity in and connectivity between medial prefrontal and left somatosensory cortex. Moreover, we found a positive across-subject correlation between the connectivity enhancement and the behavioral congruency effect. These results show that successful retrieval of congruent compared to incongruent visuotactile associations is related to enhanced processing in an mPFC–somatosensory network, and support the hypothesis that new information that fits a preexisting schema is more rapidly assimilated in neocortical networks, a process that may be mediated, at least in part, by the mPFC.

[1]  D. Marr A theory for cerebral neocortex , 1970, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[2]  Marcia K. Johnson,et al.  Contextual prerequisites for understanding: Some investigations of comprehension and recall , 1972 .

[3]  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.

[4]  Rolf A. Zwaan,et al.  Situation models in language comprehension and memory. , 1998, Psychological bulletin.

[5]  E. Maguire,et al.  The functional neuroanatomy of comprehension and memory: the importance of prior knowledge. , 1999, Brain : a journal of neurology.

[6]  Ann L. Brown,et al.  How people learn: Brain, mind, experience, and school. , 1999 .

[7]  E. Tulving,et al.  Reactivation of encoding-related brain activity during memory retrieval. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[8]  H Burton,et al.  Attending to and Remembering Tactile Stimuli: A Review of Brain Imaging Data and Single-Neuron Responses , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[9]  S. Petersen,et al.  Memory's echo: vivid remembering reactivates sensory-specific cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[10]  E A Maguire,et al.  Neuroimaging studies of autobiographical event memory. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[11]  R. Buckner,et al.  THE COGNITIVE NEUROSCIENCE OF REMEMBERING , 2001 .

[12]  Mathew E. Diamond,et al.  The Cortical Distribution of Sensory Memories , 2001, Neuron.

[13]  R. Henson,et al.  Frontal lobes and human memory: insights from functional neuroimaging. , 2001, Brain : a journal of neurology.

[14]  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.

[15]  Kenichi Ohki,et al.  Neural Correlates for Feeling-of-Knowing An fMRI Parametric Analysis , 2002, Neuron.

[16]  R. Mar The neuropsychology of narrative: story comprehension, story production and their interrelation , 2004, Neuropsychologia.

[17]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[18]  Yasushi Miyashita,et al.  Cognitive Memory: Cellular and Network Machineries and Their Top-Down Control , 2004, Science.

[19]  A. Amedi,et al.  Functional imaging of human crossmodal identification and object recognition , 2005, Experimental Brain Research.

[20]  B. McNaughton,et al.  Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[21]  G. Winocur,et al.  The cognitive neuroscience of remote episodic, semantic and spatial memory , 2006, Current Opinion in Neurobiology.

[22]  A. Giraud,et al.  Implicit Multisensory Associations Influence Voice Recognition , 2006, PLoS biology.

[23]  Bruno Bontempi,et al.  Fast track to the medial prefrontal cortex. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Norio Matsuki,et al.  Systems Consolidation Requires Postlearning Activation of NMDA Receptors in the Medial Prefrontal Cortex in Trace Eyeblink Conditioning , 2006, The Journal of Neuroscience.

[25]  M. Ernst Learning to integrate arbitrary signals from vision and touch. , 2007, Journal of vision.

[26]  Edward Awh,et al.  Spatial attention, preview, and popout: which factors influence critical spacing in crowded displays? , 2007, Journal of vision.

[27]  Nathaniel Lasry,et al.  The effect of multiple internal representations on context-rich instruction , 2006, physics/0605148.

[28]  K. Petersson,et al.  Memory trace stabilization leads to large-scale changes in the retrieval network: a functional MRI study on associative memory. , 2007, Learning & memory.

[29]  J. Born,et al.  Maintaining memories by reactivation , 2007, Current Opinion in Neurobiology.

[30]  Dorothy Tse,et al.  References and Notes Supporting Online Material Materials and Methods Figs. S1 to S5 Tables S1 to S3 Electron Impact (ei) Mass Spectra Chemical Ionization (ci) Mass Spectra References Schemas and Memory Consolidation Research Articles Research Articles Research Articles Research Articles , 2022 .

[31]  Aaron R. Seitz,et al.  Benefits of multisensory learning , 2008, Trends in Cognitive Sciences.

[32]  Aaron R. Seitz,et al.  Benefits of Stimulus Congruency for Multisensory Facilitation of Visual Learning , 2008, PloS one.

[33]  B. McNaughton,et al.  Spontaneous Changes of Neocortical Code for Associative Memory During Consolidation , 2008, Science.

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

[35]  Anders Björkman,et al.  Optimizing the mapping of finger areas in primary somatosensory cortex using functional MRI. , 2008, Magnetic resonance imaging.

[36]  J. Driver,et al.  Multisensory Interplay Reveals Crossmodal Influences on ‘Sensory-Specific’ Brain Regions, Neural Responses, and Judgments , 2008, Neuron.

[37]  Shlomit Yuval-Greenberg,et al.  The dog’s meow: asymmetrical interaction in cross-modal object recognition , 2009, Experimental Brain Research.

[38]  D. Hassabis,et al.  Tracking the Emergence of Conceptual Knowledge during Human Decision Making , 2009, Neuron.

[39]  D. Goldreich,et al.  Diminutive Digits Discern Delicate Details: Fingertip Size and the Sex Difference in Tactile Spatial Acuity , 2009, The Journal of Neuroscience.

[40]  Irene P. Kan,et al.  Contribution of Prior Semantic Knowledge to New Episodic Learning in Amnesia , 2009, Journal of Cognitive Neuroscience.

[41]  Charles Spence,et al.  The cognitive and neural correlates of tactile memory. , 2009, Psychological bulletin.

[42]  M. Khamassi,et al.  Replay of rule-learning related neural patterns in the prefrontal cortex during sleep , 2009, Nature Neuroscience.

[43]  Guillén Fernández,et al.  Shift from Hippocampal to Neocortical Centered Retrieval Network with Consolidation , 2009, The Journal of Neuroscience.

[44]  Bruce L. McNaughton,et al.  Spontaneous changes of neocortical code for associative memory during consolidation , 2008, Neuroscience Research.

[45]  Edouard Gentaz,et al.  Learning of Arbitrary Association between Visual and Auditory Novel Stimuli in Adults: The “Bond Effect” of Haptic Exploration , 2009, PloS one.

[46]  J. C. Gray,et al.  Event congruency enhances episodic memory encoding through semantic elaboration and relational binding. , 2009, Cerebral cortex.

[47]  Nicole A. Yoskowitz,et al.  Towards effective evaluation and reform in medical education: a cognitive and learning sciences perspective , 2009, Advances in health sciences education : theory and practice.

[48]  Morris Moscovitch,et al.  Ventromedial Prefrontal Cortex Lesions Produce Early Functional Alterations during Remote Memory Retrieval , 2009, The Journal of Neuroscience.

[49]  J. Born,et al.  The memory function of sleep , 2010, Nature Reviews Neuroscience.

[50]  Mehdi Khamassi,et al.  Coherent Theta Oscillations and Reorganization of Spike Timing in the Hippocampal- Prefrontal Network upon Learning , 2010, Neuron.

[51]  R. Morris,et al.  Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. , 2010, Annual review of psychology.

[52]  Guillén Fernández,et al.  Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans , 2010, Proceedings of the National Academy of Sciences.