Neural Correlates of Memory for Items and for Associations: An Event-related Functional Magnetic Resonance Imaging Study

Although results from cognitive psychology, neuropsychology, and behavioral neuroscience clearly suggest that item and associative information in memory rely on partly different brain regions, little is known concerning the differences and similarities that exist between these two types of information as a function of memory stage (i.e., encoding and retrieval). We used event-related functional magnetic resonance imaging to assess neural correlates of item and associative encoding and retrieval of simple images in 18 healthy subjects. During encoding, subjects memorized items and pairs. During retrieval, subjects made item recognition judgments (old vs. new) and associative recognition judgments (intact vs. rearranged). Relative to baseline, item and associative trials activated bilateral medial temporal and prefrontal regions during both encoding and retrieval. Direct contrasts were then performed between item and associative trials for each memory stage. During encoding, greater prefrontal, hippocampal, and parietal activation was observed for associations, but no significant activation was observed for items at the selected threshold. During recognition, greater activation was observed for associative trials in the left dorsolateral prefrontal cortex and superior parietal lobules bilaterally, whereas item recognition trials showed greater activation of bilateral frontal regions, bilateral anterior medial temporal areas, and the right temporo-parietal junction. Post hoc analyses suggested that the anterior medial temporal activation observed during item recognition was driven mainly by new items, confirming a role for this structure in novelty detection. These results suggest that although some structures such as the medial temporal and prefrontal cortex play a general role in memory, the pattern of activation in these regions can be modulated by the type of information (items or associations) interacting with memory stages.

[1]  Anthony Randal McIntosh,et al.  Towards a network theory of cognition , 2000, Neural Networks.

[2]  J A Maldjian,et al.  Functional activation of the left amygdala and hippocampus during associative encoding , 2000, Neuroreport.

[3]  Martin Lepage,et al.  Differential contribution of left and right prefrontal cortex to associative cued-recall memory: a parametric PET study , 2004, Neuroscience Research.

[4]  Edward T. Bullmore,et al.  Prolonged Reaction Time to a Verbal Working Memory Task Predicts Increased Power of Posterior Parietal Cortical Activation , 2000, NeuroImage.

[5]  Daniel L Schacter,et al.  Encoding activity in anterior medial temporal lobe supports subsequent associative recognition , 2004, NeuroImage.

[6]  Marcia K. Johnson,et al.  fMRI investigations of left and right PFC contributions to episodic remembering , 2000, Psychobiology.

[7]  P W Burgess,et al.  Confabulation and the control of recollection. , 1996, Memory.

[8]  N. Alpert,et al.  Conscious recollection and the human hippocampal formation: evidence from positron emission tomography. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Matthew Menear,et al.  Associative interference does not affect recognition memory in schizophrenia , 2005, Schizophrenia Research.

[10]  Stephan Lewandowsky,et al.  Recognition Memory for Item and Associative Information: A Comparison of Forgetting Rates , 1991 .

[11]  A. Yonelinas Recognition memory ROCs for item and associative information: The contribution of recollection and familiarity , 1997, Memory & cognition.

[12]  H. Eichenbaum,et al.  Memory, amnesia, and the hippocampal system , 1993 .

[13]  B. Knowlton,et al.  Remembering episodes: a selective role for the hippocampus during retrieval , 2000, Nature Neuroscience.

[14]  Lila Davachi,et al.  When Keeping in Mind Supports Later Bringing to Mind: Neural Markers of Phonological Rehearsal Predict Subsequent Remembering , 2001, Journal of Cognitive Neuroscience.

[15]  R. Dolan,et al.  Functional segregation within the human hippocampus , 1999, Molecular Psychiatry.

[16]  Marcia K. Johnson,et al.  Confabulation, Memory Deficits, and Frontal Dysfunction , 1997, Brain and Cognition.

[17]  H. Eichenbaum,et al.  Two functional components of the hippocampal memory system , 1994, Behavioral and Brain Sciences.

[18]  M. Denis,et al.  Functional Anatomy of Spatial Mental Imagery Generated from Verbal Instructions , 1996, The Journal of Neuroscience.

[19]  Martin Lepage,et al.  Dorsolateral prefrontal cortex involvement in memory post-retrieval monitoring revealed in both item and associative recognition tests , 2005, NeuroImage.

[20]  Arthur P. Shimamura,et al.  Source memory impairment in patients with frontal lobe lesions , 1989, Neuropsychologia.

[21]  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.

[22]  Eliot Hazeltine,et al.  Dissociable Contributions of Prefrontal and Parietal Cortices to Response Selection , 2002, NeuroImage.

[23]  R. Dolan,et al.  Differential activation of the prefrontal cortex in successful and unsuccessful memory retrieval. , 1996, Brain : a journal of neurology.

[24]  M. Brodeur,et al.  Prefrontal cortex contribution to associative recognition memory in humans: an event-related functional magnetic resonance imaging study , 2003, Neuroscience Letters.

[25]  H. Spiers,et al.  Prefrontal and medial temporal lobe interactions in long-term memory , 2003, Nature Reviews 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]  John R. Anderson,et al.  Competition and representation during memory retrieval: Roles of the prefrontal cortex and the posterior parietal cortex , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Alan A. Wilson,et al.  Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[29]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[30]  Andrew R. Mayes,et al.  What are the functional deficits produced by hippocampal and perirhinal cortex lesions? , 1999, Behavioral and Brain Sciences.

[31]  D J Wyper,et al.  Associative encoding of pictures activates the medial temporal lobes , 1998, Human brain mapping.

[32]  M H Buonocore,et al.  Hippocampal, parahippocampal and occipital-temporal contributions to associative and item recognition memory: an fMRI study , 2001, Neuroreport.

[33]  B. Murdock A Theory for the Storage and Retrieval of Item and Associative Information. , 1982 .

[34]  William E. Hockley,et al.  Item versus associative information: Further comparisons of forgetting rates. , 1992 .

[35]  Karl J. Friston,et al.  Segregating the functions of human hippocampus. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[36]  L. Squire,et al.  Functional Magnetic Resonance Imaging (fMRI) Activity in the Hippocampal Region during Recognition Memory , 2000, The Journal of Neuroscience.

[37]  Michael D. Rugg,et al.  The Role of the Prefrontal Cortex in Recognition Memory and Memory for Source: An fMRI Study , 1999, NeuroImage.

[38]  Daniel L. Schacter,et al.  Retrieval of Relational Information: A Role for the Left Inferior Prefrontal Cortex , 2002, NeuroImage.

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

[40]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

[41]  T. Shallice,et al.  Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. , 1999, Brain : a journal of neurology.

[42]  Donna Rose Addis,et al.  Prefrontal and hippocampal contributions to the generation and binding of semantic associations during successful encoding , 2006, NeuroImage.

[43]  M. Humphreys,et al.  Relational information and the context effect in recognition memory , 1976, Memory & cognition.

[44]  Larry R Squire,et al.  Recognition Memory for Single Items and for Associations Is Similarly Impaired following Damage to the Hippocampal Region & L E a R N I N G M E M O R Y , 2022 .

[45]  Daniel G. Bobrow,et al.  Descriptions: An intermediate stage in memory retrieval , 1979, Cognitive Psychology.

[46]  M. Mishkin,et al.  Differential effects of early hippocampal pathology on episodic and semantic memory. , 1997, Science.

[47]  C D Frith,et al.  Brain activity during memory retrieval. The influence of imagery and semantic cueing. , 1996, Brain : a journal of neurology.

[48]  Stefan Köhler,et al.  Differential contributions of the parahippocampal place area and the anterior hippocampus to human memory for scenes , 2002, Hippocampus.

[49]  M. Humphreys Item and relational information: A case for context independent retrieval , 1978 .

[50]  R. Cabeza,et al.  Lateralization of Prefrontal Activity during Episodic Memory Retrieval: Evidence for the Production-Monitoring Hypothesis , 2003, Journal of Cognitive Neuroscience.

[51]  E. Tulving,et al.  Novelty assessment in the brain and long-term memory encoding , 1995, Psychonomic bulletin & review.

[52]  Marcia K. Johnson,et al.  The role of prefrontal cortex during tests of episodic memory , 1998, Trends in Cognitive Sciences.

[53]  Hans-Jochen Heinze,et al.  Human Hippocampal and Parahippocampal Activity during Visual Associative Recognition Memory for Spatial and Nonspatial Stimulus Configurations , 2003, The Journal of Neuroscience.

[54]  A. Mecklinger,et al.  Intra- and Inter-Item Associations Doubly Dissociate the Electrophysiological Correlates of Familiarity and Recollection , 2006, Neuron.

[55]  T. Shallice,et al.  Confidence in Recognition Memory for Words: Dissociating Right Prefrontal Roles in Episodic Retrieval , 2000, Journal of Cognitive Neuroscience.

[56]  J. Desmond,et al.  Making memories: brain activity that predicts how well visual experience will be remembered. , 1998, Science.

[57]  B. Weber,et al.  Human hippocampus establishes associations in memory , 1997, Hippocampus.

[58]  Richard S. J. Frackowiak,et al.  Functional anatomy of a common semantic system for words and pictures , 1996, Nature.

[59]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[60]  M. Egan,et al.  Complexity of prefrontal cortical dysfunction in schizophrenia: more than up or down. , 2003, The American journal of psychiatry.

[61]  A R McIntosh,et al.  The neural correlates of intentional learning of verbal materials: a PET study in humans. , 1996, Brain research. Cognitive brain research.

[62]  H. Eichenbaum,et al.  On the Binding of Associations in Memory: Clues From Studies on the Role of the Hippocampal Region in Paired-Associate Learning , 1995 .

[63]  O. Krastoshevsky,et al.  Hippocampal Contributions to Episodic Encoding : Insights From Relational and Item-Based Learning , 2002 .

[64]  Matthew Menear,et al.  Associative Memory Encoding and Recognition in Schizophrenia: An Event-Related fMRI Study , 2006, Biological Psychiatry.

[65]  Alexandra J. Golby,et al.  The brain basis for episodic memory: Insights from functional MRI, intracranial EEG, and patients with epilepsy , 2006, Epilepsy & Behavior.

[66]  Rugg,et al.  Episodic memory retrieval: an (event-related) functional neuroimaging perspective , 2002 .

[67]  Lars Nyberg,et al.  Brain Regions Differentially Involved in Remembering What and When: a PET Study , 1997, Neuron.

[68]  Toshio Iijima,et al.  Medial temporal lobe activation during context‐dependent relational processes in episodic retrieval: An fMRI study , 2002 .

[69]  Michael Petrides,et al.  6 – Mapping Prefrontal Cortical Systems for the Control of Cognition , 2000 .

[70]  Marcia K. Johnson,et al.  Left prefrontal activation during episodic remembering: an event‐related fMRI study , 1998, Neuroreport.

[71]  Richard S. J. Frackowiak,et al.  Neural Correlates of Memory Retrieval during Recognition Memory and Cued Recall , 1998, NeuroImage.

[72]  Malcolm W. Brown,et al.  Recognition memory: What are the roles of the perirhinal cortex and hippocampus? , 2001, Nature Reviews Neuroscience.

[73]  Karl Magnus Petersson,et al.  Instruction-specific brain activations during episodic encoding a generalized level of processing effect , 2003, NeuroImage.

[74]  N. Hunkin,et al.  Memory for single items, word pairs, and temporal order of different kinds in a patient with selective hippocampal lesions , 2001, Cognitive neuropsychology.

[75]  Alan C. Evans,et al.  BrainWeb: Online Interface to a 3D MRI Simulated Brain Database , 1997 .

[76]  R. Ratcliff,et al.  Time course of item and associative information: implications for global memory models. , 1989, Journal of experimental psychology. Learning, memory, and cognition.

[77]  H G Wieser,et al.  Human hippocampus associates information in memory. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[78]  Alan C. Evans,et al.  A General Statistical Analysis for fMRI Data , 2000, NeuroImage.

[79]  Alan C. Evans,et al.  A general statistical analysis for fMRI data , 2000, NeuroImage.

[80]  S. E. Petersen,et al.  Response from Kelley, Buckner and Petersen , 1998, Trends in Cognitive Sciences.

[81]  R. Henson,et al.  A familiarity signal in human anterior medial temporal cortex? , 2003, Hippocampus.

[82]  D. Schnyer,et al.  A critical role for the anterior hippocampus in relational memory: Evidence from an fMRI study comparing associative and item recognition , 2004, Hippocampus.

[83]  A. Yonelinas The Nature of Recollection and Familiarity: A Review of 30 Years of Research , 2002 .

[84]  Richard S. J. Frackowiak,et al.  Brain regions associated with acquisition and retrieval of verbal episodic memory , 1994, Nature.

[85]  L. Squire,et al.  Simple and associative recognition memory in the hippocampal region. , 2001, Learning & memory.

[86]  M. Rugg,et al.  Retrieval processing and episodic memory , 2000, Trends in Cognitive Sciences.

[87]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[88]  Katharina Henke,et al.  Active hippocampus during nonconscious memories , 2003, Consciousness and Cognition.