Behavioural and Magnetoencephalographic Evidence for the Interaction Between Semantic and Episodic Memory in Healthy Elderly Subjects

The relationship between episodic and semantic memory systems has long been debated. Some authors argue that episodic memory is contingent on semantic memory (Tulving 1984), while others postulate that both systems are independent since they can be selectively damaged (Squire 1987). The interaction between these memory systems is particularly important in the elderly, since the dissociation of episodic and semantic memory defects characterize different aging-related pathologies. Here, we investigated the interaction between semantic knowledge and episodic memory processes associated with faces in elderly subjects using an experimental paradigm where the semantic encoding of famous and unknown faces was compared to their episodic recognition. Results showed that the level of semantic awareness of items affected the recognition of those items in the episodic memory task. Event-related magnetic fields confirmed this interaction between episodic and semantic memory: ERFs related to the old/new effect during the episodic task were markedly different for famous and unknown faces. The old/new effect for famous faces involved sustained activities maximal over right temporal sensors, showing a spatio-temporal pattern partly similar to that found for famous versus unknown faces during the semantic task. By contrast, an old/new effect for unknown faces was observed on left parieto-occipital sensors. These findings suggest that the episodic memory for famous faces activated the retrieval of stored semantic information, whereas it was based on items’ perceptual features for unknown faces. Overall, our results show that semantic information interfered markedly with episodic memory processes and suggested that the neural substrates of these two memory systems overlap.

[1]  G. Barba,et al.  The influence of semantic encoding on recognition memory in Alzheimer's disease , 1996, Neuropsychologia.

[2]  P Walla,et al.  Early occipito-parietal activity in a word recognition task: an EEG and MEG study , 1999, Clinical Neurophysiology.

[3]  Marta Kutas,et al.  Neural Dynamics Associated with Semantic and Episodic Memory for Faces: Evidence from Multiple Frequency Bands , 2010, Journal of Cognitive Neuroscience.

[4]  M. Rugg,et al.  Event-related potentials and recognition memory , 2007, Trends in Cognitive Sciences.

[5]  L. Chaby,et al.  [Processing facial identity and emotional expression in normal aging and neurodegenerative diseases]. , 2009, Psychologie & neuropsychiatrie du vieillissement.

[6]  G. Denes,et al.  Semantic and episodic memory in aphasia , 1996, Neuropsychologia.

[7]  Mark C. W. van Rossum,et al.  Investigating the functional interaction between semantic and episodic memory: Convergent behavioral and electrophysiological evidence for the role of familiarity , 2007, NeuroImage.

[8]  J. Hodges,et al.  Semantic dementia: a unique clinicopathological syndrome , 2007, The Lancet Neurology.

[9]  S. Pappatà,et al.  Cortical Networks Implicated in Semantic and Episodic Memory: Common or Unique? , 1998, Cortex.

[10]  D. Friedman Event-related brain potential investigations of memory and aging , 2000, Biological Psychology.

[11]  Anders M. Dale,et al.  N400-like Magnetoencephalography Responses Modulated by Semantic Context, Word Frequency, and Lexical Class in Sentences , 2002, NeuroImage.

[12]  Soledad Ballesteros,et al.  The effect of age on word-stem cued recall: A behavioral and electrophysiological study , 2009, Brain Research.

[13]  F. Craik,et al.  Depth of processing and the retention of words , 1975 .

[14]  J. Fell,et al.  A magnetoencephalographic study of brain activity related to recognition memory in healthy young human subjects , 2000, Neuroscience Letters.

[15]  Marie-Claire Goldblum,et al.  The influence of semantic and perceptual encoding on recognition memory in Alzheimer’s disease , 1998, Neuropsychologia.

[16]  E. Tulving Elements of episodic memory , 1983 .

[17]  Tim Curran,et al.  Picture Superiority Doubly Dissociates the ERP Correlates of Recollection and Familiarity , 2011, Journal of Cognitive Neuroscience.

[18]  D Friedman,et al.  Event‐related potential (ERP) studies of memory encoding and retrieval: A selective review , 2000, Microscopy research and technique.

[19]  F. Craik,et al.  Levels of Pro-cessing: A Framework for Memory Research , 1975 .

[20]  E. L. Wilding,et al.  Erratum: An event-related potential study of recognition memory with and without retrieval of source. (Brain (1996) 119 (889-905) , 1996 .

[21]  E. Denkova,et al.  Neural correlates of remembering/knowing famous people: An event-related fMRI study , 2006, Neuropsychologia.

[22]  E. Tulving How many memory systems are there , 1985 .

[23]  M. Eimer Event-related brain potentials distinguish processing stages involved in face perception and recognition , 2000, Clinical Neurophysiology.

[24]  M. Rugg,et al.  Recognition memory for new associations: electrophysiological evidence for the role of recollection , 1998, Neuropsychologia.

[25]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[26]  Endel Tulving,et al.  Multiple Learning and Memory Systems , 1984 .

[27]  David I. Donaldson,et al.  Examining the neural basis of episodic memory: ERP evidence that faces are recollected differently from names , 2009, Neuropsychologia.

[28]  P. Walla,et al.  Depth of word processing in Alzheimer patients and normal controls: a magnetoencephalographic (MEG) study , 2005, Journal of Neural Transmission.

[29]  B. Dubois,et al.  Confabulation in Alzheimer's disease: poor encoding and retrieval of over-learned information. , 2009, Brain : a journal of neurology.

[30]  M. Kutas,et al.  Reading between the lines: Event-related brain potentials during natural sentence processing , 1980, Brain and Language.

[31]  L. Chaby,et al.  La reconnaissance des visages et de leurs expressions faciales au cours du vieillissement normal et dans les pathologies neurodégénératives , 2009 .

[32]  Edward T. Bullmore,et al.  The hippocampal region is involved in successful recognition of both remote and recent famous faces , 2004, NeuroImage.

[33]  Vinod Menon,et al.  Relating semantic and episodic memory systems. , 2002, Brain research. Cognitive brain research.

[34]  Sönke Johannes,et al.  Event-related brain potentials to unfamiliar faces in explicit and implicit memory tasks , 1997, Neuroscience Research.

[35]  D. Schacter,et al.  Cortical activity reductions during repetition priming can result from rapid response learning , 2004, Nature.

[36]  L. Deouell,et al.  STRUCTURAL ENCODING AND IDENTIFICATION IN FACE PROCESSING: ERP EVIDENCE FOR SEPARATE MECHANISMS , 2000, Cognitive neuropsychology.

[37]  C. C. Wood,et al.  Event-related potentials, lexical decision and semantic priming. , 1985, Electroencephalography and clinical neurophysiology.

[38]  Stefan Knecht,et al.  New Names for Known Things: On the Association of Novel Word Forms with Existing Semantic Information , 2010, Journal of Cognitive Neuroscience.

[39]  Mark S. Seidenberg,et al.  Neural Systems Underlying the Recognition of Familiar and Newly Learned Faces , 2000, The Journal of Neuroscience.

[40]  M. Erb,et al.  Mild cognitive impairment (MCI) and actual retrieval performance affect cerebral activation in the elderly , 2007, Neurobiology of Aging.

[41]  Marcia Grabowecky,et al.  Electrophysiological Correlates of Recollecting Faces of Known and Unknown Individuals , 2000, NeuroImage.

[42]  B Renault,et al.  Differential processing of part-to-whole and part-to-part face priming: an ERP study. , 1999, Neuroreport.

[43]  M. Rugg,et al.  An event-related potential study of recognition memory with and without retrieval of source. , 1996, Brain : a journal of neurology.

[44]  Sven Joubert,et al.  The cognitive and neural expression of semantic memory impairment in mild cognitive impairment and early Alzheimer's disease , 2010, Neuropsychologia.

[45]  B Renault,et al.  Event-related potentials to structural familiar face incongruity processing. , 1999, Psychophysiology.

[46]  Stephan G. Boehm,et al.  Do I Know You? Insights into Memory for Faces from Brain Potentials , 2006, Clinical EEG and neuroscience.

[47]  N. Cohen Neuropsychological evidence for a distinction between procedural and declarative knowledge in human memory and amnesia , 1981 .

[48]  R Kakigi,et al.  [Event-related brain potentials]. , 1997, Nihon rinsho. Japanese journal of clinical medicine.

[49]  E. Tulving,et al.  On the Measurement of Priming: What is the Correct Baseline? , 1995 .

[50]  L. Squire CHAPTER 7 – Memory and the Brain* , 1986 .

[51]  D. Neary,et al.  Knowledge of famous faces and names in semantic dementia. , 2004, Brain : a journal of neurology.

[52]  Astrid M. Schloerscheidt,et al.  The impact of change in stimulus format on the electrophysiological indices of recognition , 2004, Neuropsychologia.

[53]  W. Sommer,et al.  Differential localization of brain systems subserving memory for names and faces in normal subjects with event-related potentials. , 1997, Electroencephalography and clinical neurophysiology.

[54]  Bernhard P. Staresina,et al.  Magnetoencephalographic correlates of different levels in subjective recognition memory , 2005, NeuroImage.

[55]  L. Squire,et al.  Human memory and amnesia , 1984 .

[56]  Werner Sommer,et al.  Effects of previous experience and associated knowledge on retrieval processes of faces: An ERP investigation of newly learned faces , 2010, Brain Research.

[57]  Wilfried Lang,et al.  Left Temporal and Temporoparietal Brain Activity Depends on Depth of Word Encoding: A Magnetoencephalographic Study in Healthy Young Subjects , 2001, NeuroImage.

[58]  Michael D. Rugg,et al.  Event-Related Potentials and Recognition Memory for Low- and High-Frequency Words , 1992, Journal of Cognitive Neuroscience.

[59]  D Friedman,et al.  Item and source memory: differential age effects revealed by event‐related potentials , 1997, Neuroreport.

[60]  R Salmelin,et al.  Information processing in the human brain: magnetoencephalographic approach. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[61]  T. Curran,et al.  Semantic and perceptual effects on recognition memory: Evidence from ERP , 2009, Brain Research.

[62]  J R Hodges,et al.  Episodic memory: insights from semantic dementia. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[63]  Robert C. Knowlton,et al.  Dynamic Brain Activation Patterns for Face Recognition: A Magnetoencephalography Study , 2005, Brain Topography.