The neural correlates of recollection: Hippocampal activation declines as episodic memory fades

Memories for certain events tend to linger in rich, vivid detail, and retrieval of these memories includes a sense of re‐experiencing the details of the event. Most events, however, are not retained in any detailed way for more than a few days. According to one theory, the hippocampus plays a specific role in supporting episodic retrieval, that is, the re‐experiencing of an event as part of one's personal past. This theory predicts that as episodic memories fade over time and are reduced to feelings of familiarity, activity in the hippocampus should no longer be associated with retrieval. We used high‐resolution functional imaging to explore neural activity in medial temporal lobe subregions while participants performed a recognition task at both a short (10‐min) and long (1‐week) study‐test delay. For each recognized item, subjects made “Remember/Know” judgments, allowing us to distinguish between items that were consistently episodic across the two tests and items that were initially episodic, but later became merely familiar. Our results demonstrate that activity in the subiculum is specifically associated with episodic recollection. Overall, recollected items were associated with higher activity in the subiculum than other items. For transiently recollected items, there was a decrease in subicular activity across the 1‐week delay as memory faded from recollection to familiarity, whereas consistently recollected items were associated with enhanced subicular activity at both delays. These results provide evidence of a link between subicular activation and recollective experience. © 2008 Wiley‐Liss, Inc.

[1]  E. Rolls,et al.  Computational analysis of the role of the hippocampus in memory , 1994, Hippocampus.

[2]  B. Knowlton,et al.  A Dissociation of Encoding and Retrieval Processes in the Human Hippocampus , 2005, The Journal of Neuroscience.

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

[4]  Myra A. Fernandes,et al.  Neural correlates of recollection and familiarity: A review of neuroimaging and patient data , 2007, Neuropsychologia.

[5]  Peter E. Wais,et al.  The Hippocampus Supports both the Recollection and the Familiarity Components of Recognition Memory , 2006, Neuron.

[6]  Robert T. Knight,et al.  Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity , 2002, Nature Neuroscience.

[7]  Morris Moscovitch,et al.  Hippocampal contributions to recollection in retrograde and anterograde amnesia , 2006, Hippocampus.

[8]  M. Rugg,et al.  Separating the Brain Regions Involved in Recollection and Familiarity in Recognition Memory , 2005, The Journal of Neuroscience.

[9]  M. Moser,et al.  Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus , 2007, Science.

[10]  L R Squire,et al.  Remembering and knowing: two different expressions of declarative memory. , 1995, Journal of experimental psychology. Learning, memory, and cognition.

[11]  G. Paxinos,et al.  THE HUMAN NERVOUS SYSTEM , 1975 .

[12]  Craig E. L. Stark,et al.  When zero is not zero: The problem of ambiguous baseline conditions in fMRI , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[14]  Nicole M Dudukovic,et al.  Remember-Know judgments and retrieval of contextual details. , 2006, Acta psychologica.

[15]  H. Duvernoy,et al.  The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI , 1997 .

[16]  Stephen A. Engel,et al.  Application of Cortical Unfolding Techniques to Functional MRI of the Human Hippocampal Region , 2000, NeuroImage.

[17]  E. Tulving Memory and consciousness. , 1985 .

[18]  David G. Amaral,et al.  21 – Hippocampal Formation , 1990 .

[19]  M. W. Brown,et al.  Episodic memory, amnesia, and the hippocampal–anterior thalamic axis , 1999, Behavioral and Brain Sciences.

[20]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[21]  Thomas E. Nichols,et al.  Optimization of experimental design in fMRI: a general framework using a genetic algorithm , 2003, NeuroImage.

[22]  R. Cabeza,et al.  Triple dissociation in the medial temporal lobes: recollection, familiarity, and novelty. , 2006, Journal of neurophysiology.

[23]  D. Montaldi,et al.  The neural system that mediates familiarity memory , 2006, Hippocampus.

[24]  D. Amaral,et al.  The Hippocampal Formation , 2009 .

[25]  A. Wagner,et al.  Domain-general and domain-sensitive prefrontal mechanisms for recollecting events and detecting novelty. , 2005, Cerebral cortex.

[26]  D. W. In memory of ... , 1963, Science.

[27]  Roberto Cabeza,et al.  Role of parietal regions in episodic memory retrieval: The dual attentional processes hypothesis , 2008, Neuropsychologia.

[28]  Barbara J Knowlton,et al.  The effect of testing procedure on remember-know judgments , 2002, Psychonomic bulletin & review.

[29]  R. Clark,et al.  Recognition memory and the medial temporal lobe: a new perspective , 2007, Nature Reviews Neuroscience.

[30]  L. Squire,et al.  Recall and recognition are equally impaired in patients with selective hippocampal damage , 2004, Cognitive, affective & behavioral neuroscience.

[31]  Rachel A. Diana,et al.  Imaging recollection and familiarity in the medial temporal lobe: a three-component model , 2007, Trends in Cognitive Sciences.

[32]  J. G. Snodgrass,et al.  A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. , 1980, Journal of experimental psychology. Human learning and memory.

[33]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[34]  John T. Wixted,et al.  Remember/Know Judgments Probe Degrees of Recollection , 2008, Journal of Cognitive Neuroscience.

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

[36]  Boris Suchan,et al.  Hippocampal involvement in recollection but not familiarity across time: A prospective study , 2008, Hippocampus.

[37]  N. Roberts,et al.  Item recognition is less impaired than recall and associative recognition in a patient with selective hippocampal damage , 2005, Hippocampus.

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