Common pathway in the medial temporal lobe for storage and recovery of words as revealed by event‐related functional MRI

Lesion studies have provided compelling evidence that episodic memory is dependent on the integrity of the medial temporal lobe (MTL). This role of the MTL in episodic memory has been supported by several neuroimaging studies during both episodic encoding and retrieval. After two meta‐analyses of positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) studies, we investigated a possible dissociation within the MTL memory system in relation to encoding and retrieval processes. Based on previous reports that specifically related the function of the MTL in episodic memory to successful encoding and actual recovery of information, we applied event‐related fMRI to compare successful encoding of words (ES) directly with successful recognition of those same words (RS). Our results did not indicate a clear dissociation between encoding and retrieval activations in the MTL. Instead, a region in the left MTL, covering the parahippocampal cortex and hippocampal formation, which was activated during ES almost completely overlapped with the area that was activated during RS. An additional region in the left anterior MTL, including the entorhinal cortex, was found to be activated exclusively during ES. Research has indicated that a large percentage of cells in this region are particularly sensitive to the relative novelty of stimuli. Our results, therefore, suggest that the parahippocampal/hippocampal region is involved in the formation and subsequent reactivation of memory traces, whereas the activity observed in the entorhinal cortex may reflect elementary memory processes related to novelty detection. © 2003 Wiley‐Liss, Inc.

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

[2]  H. Eichenbaum,et al.  The Neurophysiology of Memory , 2000, Annals of the New York Academy of Sciences.

[3]  D. Gaffan,et al.  Perirhinal Cortex Ablation Impairs Visual Object Identification , 1998, The Journal of Neuroscience.

[4]  F. Barkhof,et al.  Anterior Medial Temporal Lobe Activation during Attempted Retrieval of Encoded Visuospatial Scenes: An Event-Related fMRI Study , 2001, NeuroImage.

[5]  M. W. Brown,et al.  Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe , 1998, Neuropharmacology.

[6]  Anthony Randal McIntosh,et al.  Transperceptual Encoding and Retrieval Processes in Memory: A PET Study of Visual and Haptic Objects , 2001, NeuroImage.

[7]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[8]  S. Petersen,et al.  Hemispheric Specialization in Human Dorsal Frontal Cortex and Medial Temporal Lobe for Verbal and Nonverbal Memory Encoding , 1998, Neuron.

[9]  O Josephs,et al.  Dissociable Human Perirhinal, Hippocampal, and Parahippocampal Roles during Verbal Encoding , 2002, The Journal of Neuroscience.

[10]  D. Gaffan,et al.  Impairment of visual object-discrimination learning after perirhinal cortex ablation. , 1997 .

[11]  I. Riches,et al.  The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gyrus and inferior temporal cortex of the primate , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[13]  J. T. Erichsen,et al.  Fos Imaging Reveals Differential Patterns of Hippocampal and Parahippocampal Subfield Activation in Rats in Response to Different Spatial Memory Tests , 2000, The Journal of Neuroscience.

[14]  Andrew J Saykin,et al.  Memory deficits before and after temporal lobectomy: Effect of laterality and age of onset , 1989, Brain and Cognition.

[15]  Randy L. Buckner,et al.  Encoding Processes during Retrieval Tasks , 2001, Journal of Cognitive Neuroscience.

[16]  M. Witter,et al.  Anatomical Organization of the Parahippocampal‐Hippocampal Network , 2000, Annals of the New York Academy of Sciences.

[17]  F. H. Lopes da Silva,et al.  Cortico‐hippocampal communication by way of parallel parahippocampal‐subicular pathways , 2000, Hippocampus.

[18]  E. Tulving,et al.  Hippocampal PET activations of memory encoding and retrieval: The HIPER model , 1998, Hippocampus.

[19]  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.

[20]  E. Rolls,et al.  View‐responsive neurons in the primate hippocampal complex , 1995, Hippocampus.

[21]  S. C. Strother,et al.  The Quantitative Evaluation of Functional Neuroimaging Experiments: Mutual Information Learning Curves , 2002, NeuroImage.

[22]  K Lehnertz,et al.  Real-time tracking of memory formation in the human rhinal cortex and hippocampus. , 1999, Science.

[23]  R. Gur,et al.  Neuropsychological Changes after Anterior Temporal Lobectomy Acute Effects on Memory, Language, and Music , 1992 .

[24]  M Erb,et al.  Differential activation in parahippocampal and prefrontal cortex during word and face encoding tasks , 2001, Neuroreport.

[25]  A R McIntosh,et al.  Episodic encoding and recognition of pictures and words: role of the human medial temporal lobes. , 2000, Acta psychologica.

[26]  T. Shallice,et al.  Long-term retrograde amnesia… the crucial role of the hippocampus , 2001, Neuropsychologia.

[27]  L R Squire,et al.  Profound Amnesia After Damage to the Medial Temporal Lobe: A Neuroanatomical and Neuropsychological Profile of Patient E. P. , 2000, The Journal of Neuroscience.

[28]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[29]  A. Dale,et al.  Selective averaging of rapidly presented individual trials using fMRI , 1997, Human brain mapping.

[30]  R. Buckner,et al.  Human Brain Mapping 6:373–377(1998) � Event-Related fMRI and the Hemodynamic Response , 2022 .

[31]  G H Glover,et al.  Separate neural bases of two fundamental memory processes in the human medial temporal lobe. , 1997, Science.

[32]  D. Schacter,et al.  Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval , 1999, Hippocampus.

[33]  J. Desmond,et al.  Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. , 2001, Brain : a journal of neurology.

[34]  L M Saksida,et al.  The Parahippocampal Region and Object Identification , 2000, Annals of the New York Academy of Sciences.

[35]  D L Schacter,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Medial Blockintemporal Blockinlobe Blockinactivation Blockinduring Blockinepisodic Encoding Blockinand Blockinretrieval: Blockina Blockinpet Blockinstudy , 2022 .

[36]  Dick J. Veltman,et al.  Parahippocampal Activation during Successful Recognition of Words: A Self-Paced Event-Related fMRI Study , 2001, NeuroImage.

[37]  J. R. Baker,et al.  The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[38]  F Barkhof,et al.  Visual association encoding activates the medial temporal lobe: A functional magnetic resonance imaging study , 1997, Hippocampus.

[39]  S. Houle,et al.  Activation of medial temporal structures during episodic memory retrieval , 1996, Nature.

[40]  B. Milner,et al.  Disorders of learning and memory after temporal lobe lesions in man. , 1972, Clinical neurosurgery.

[41]  R. Dolan,et al.  Encoding and retrieval in human medial temporal lobes: An empirical investigation using functional magnetic resonance imaging (fMRI) , 1999, Hippocampus.

[42]  S E Petersen,et al.  Direct comparison of episodic encoding and retrieval of words: an event-related fMRI study. , 1999, Memory.

[43]  Karl J. Friston,et al.  Event‐related f MRI , 1997, Human brain mapping.

[44]  Randy L. Buckner,et al.  Set-and Code-Specific Activation in the Frontal Cortex: An fMRI Study of Encoding and Retrieval of Faces and Words , 1999, Journal of Cognitive Neuroscience.

[45]  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.