Relational and non‐relational memory – electrophysiological correlates of novelty detection, repetition detection and subsequent memory

The dissociability of novelty detection in relational (RM) and non‐relational memory (NRM) is currently under debate. To further address the time courses and underlying brain correlates of novelty detection, event‐related potentials (ERPs) were analysed for encoding and retrieval on three memory tasks in healthy subjects. Spatial and non‐spatial RM as well as NRM were assessed separately. The ERPs related to RM and NRM were dissociable for hits and correct rejections in an early and late time window. An early old/new effect was observed for NRM. A late old/new effect replicated the frequently reported recollection‐associated old/new effect in terms of direction and amplitudes. Four different novelty types (spatial relational, non‐spatial relational, horizontal non‐relational and inverted non‐relational) were examined. The P3a related to novelty detection differed in horizontal vs. inverted distractors in NRM, but not in spatial vs. non‐spatial RM. ERPs for repetition detection (hits during retrieval) and also for subsequent hits (encoding phase) differed between RM and NRM. These findings are discussed in relation to potential brain correlates in RM and NRM during encoding and retrieval.

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

[2]  D. Schacter,et al.  Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming. , 2000, Brain : a journal of neurology.

[3]  Klaus Lehnertz,et al.  Human temporal lobe potentials in verbal learning and memory processes , 1997, Neuropsychologia.

[4]  Irene Daum,et al.  Involvement of the human thalamus in relational and non‐relational memory , 2008, The European journal of neuroscience.

[5]  T. Nakada,et al.  A Review of EEG and Blood Flow Data , 1998, Reviews in the neurosciences.

[6]  J. Rohrbaugh,et al.  Electrocortical signs of levels of processing: perceptual analysis and recognition memory. , 1980, Psychophysiology.

[7]  I. Daum,et al.  Course of relational and non-relational recognition memory across the adult lifespan. , 2008, Learning & memory.

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

[9]  K. Hugdahl,et al.  Sex differences in visuo-spatial processing: An fMRI study of mental rotation , 2006, Neuropsychologia.

[10]  Michael D. Rugg,et al.  Dissociation of the neural correlates of implicit and explicit memory , 1998, Nature.

[11]  Michael D. Rugg,et al.  Content dependence of the electrophysiological correlates of recollection , 2008, NeuroImage.

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

[13]  H. Eichenbaum,et al.  The Hippocampus, Memory, and Place Cells Is It Spatial Memory or a Memory Space? , 1999, Neuron.

[14]  J. G. Snodgrass,et al.  Pragmatics of measuring recognition memory: applications to dementia and amnesia. , 1988, Journal of experimental psychology. General.

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

[16]  N. Squires,et al.  Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. , 1975, Electroencephalography and clinical neurophysiology.

[17]  Robert M. Siwiec,et al.  Neural Correlates of Successful Encoding Identified Using Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[18]  R. Desimone,et al.  The representation of stimulus familiarity in anterior inferior temporal cortex. , 1993, Journal of neurophysiology.

[19]  P. P. Rickham.  HUMAN EXPERIMENTATION. CODE OF ETHICS OF THE WORLD MEDICAL ASSOCIATION. DECLARATION OF HELSINKI. , 1964, British medical journal.

[20]  Jeffrey D. Johnson,et al.  The relationship between the right frontal old/new ERP effect and post-retrieval monitoring: Specific or non-specific? , 2008, Neuropsychologia.

[21]  R. Passingham.  The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[22]  Lee Ryan,et al.  Hippocampal activation during episodic and semantic memory retrieval: Comparing category production and category cued recall , 2008, Neuropsychologia.

[23]  C Ranganath,et al.  Brain waves following remembered faces index conscious recollection. , 1999, Brain research. Cognitive brain research.

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

[25]  Giuseppe Sartori,et al.  Predicting outcomes of decisions in the brain , 2008, Behavioural Brain Research.

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

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

[28]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[29]  R. Knight.  Decreased response to novel stimuli after prefrontal lesions in man. , 1984, Electroencephalography and clinical neurophysiology.

[30]  Hiroki R. Hayama,et al.  Electrophysiological dissociation of the neural correlates of recollection and familiarity , 2006, Brain Research.

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

[32]  T W Picton,et al.  Attention and successful episodic encoding: an event-related potential study. , 2001, Brain research. Cognitive brain research.

[33]  Ken A Paller,et al.  The neural basis of the butcher-on-the-bus phenomenon: when a face seems familiar but is not remembered , 2004, NeuroImage.

[34]  Robert T. Knight,et al.  Intact Recollection Memory in High-performing Older Adults: ERP and Behavioral Evidence , 2006, Journal of Cognitive Neuroscience.

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

[36]  H Eichenbaum,et al.  Memory for items and memory for relations in the procedural/declarative memory framework. , 1997, Memory.

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

[38]  J. Polich.  Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[39]  D Friedman,et al.  Effects of aging on the novelty P3 during attend and ignore oddball tasks. , 1998, Psychophysiology.

[40]  K. Zilles,et al.  The neural correlates of person familiarity. A functional magnetic resonance imaging study with clinical implications. , 2001, Brain : a journal of neurology.

[41]  Christian Bellebaum,et al.  Time course of cross-hemispheric spatial updating in the human parietal cortex , 2006, Behavioural Brain Research.

[42]  D. Schacter,et al.  The neural origins of specific and general memory: the role of the fusiform cortex , 2005, Neuropsychologia.

[43]  J. O’Keefe.  Do hippocampal pyramidal cells signal non‐spatial as well as spatial information? , 1999, Hippocampus.

[44]  L. Squire.  Declarative and Nondeclarative Memory: Multiple Brain Systems Supporting Learning and Memory , 1992, Journal of Cognitive Neuroscience.

[45]  Ravi S. Menon,et al.  Novelty responses to relational and non‐relational information in the hippocampus and the parahippocampal region: A comparison based on event‐related fMRI , 2005, Hippocampus.

[46]  Richard S. J. Frackowiak,et al.  Knowing where and getting there: a human navigation network. , 1998, Science.

[47]  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.

[48]  Nicole M. Dudukovic,et al.  Goal-dependent modulation of declarative memory: Neural correlates of temporal recency decisions and novelty detection , 2007, Neuropsychologia.

[49]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[50]  G. Rainer,et al.  Cognitive neuroscience: Neural mechanisms for detecting and remembering novel events , 2003, Nature Reviews Neuroscience.

[51]  S. Ueno,et al.  Distinct neural correlates underlying two- and three-dimensional mental rotations using three-dimensional objects , 2007, Brain Research.

[52]  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.

[53]  B. Rossion,et al.  Revisiting Snodgrass and Vanderwart's Object Pictorial Set: The Role of Surface Detail in Basic-Level Object Recognition , 2004, Perception.

[54]  R. Knight,et al.  Dissociable neural correlates for familiarity and recollection during the encoding and retrieval of pictures. , 2004, Brain research. Cognitive brain research.

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

[56]  E A Maguire,et al.  Hippocampal Amnesia , 2001, Neurocase.

[57]  E. Maguire,et al.  The Human Hippocampus and Spatial and Episodic Memory , 2002, Neuron.

[58]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[59]  A. Lawson,et al.  Distinct neural mechanisms for repetition effects of visual objects , 2007, Neuroscience.

[60]  G. Vingerhoets,et al.  Regional Brain Activity during Different Paradigms of Mental Rotation in Healthy Volunteers: A Positron Emission Tomography Study , 2001, NeuroImage.

[61]  Rickham Pp.  Human Experimentation: Code of Ethics of the World Medical Association (Declaration of Helsinki). , 1964, Canadian Medical Association journal.

[62]  Ava J. Senkfor,et al.  Memory for drawings in locations: spatial source memory and event-related potentials. , 2000, Psychophysiology.

[63]  D. Lehmann,et al.  Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[65]  H. Eichenbaum.  Hippocampus Cognitive Processes and Neural Representations that Underlie Declarative Memory , 2004, Neuron.

[66]  Demis Hassabis,et al.  Impaired spatial and non-spatial configural learning in patients with hippocampal pathology , 2007, Neuropsychologia.

[67]  T. Curran.  Brain potentials of recollection and familiarity , 2000, Memory & cognition.

[68]  Maija Pihlajamäki,et al.  Visual presentation of novel objects and new spatial arrangements of objects differentially activates the medial temporal lobe subareas in humans , 2004, The European journal of neuroscience.

[69]  T. Curran.  Effects of attention and confidence on the hypothesized ERP correlates of recollection and familiarity , 2004, Neuropsychologia.

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

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

[72]  T. Curran,et al.  Using ERPs to dissociate recollection from familiarity in picture recognition. , 2003, Brain research. Cognitive brain research.

[73]  Sabrina M. Tom,et al.  Dissociable correlates of recollection and familiarity within the medial temporal lobes , 2004, Neuropsychologia.

[74]  D. Friedman,et al.  The novelty P3: an event-related brain potential (ERP) sign of the brain's evaluation of novelty , 2001, Neuroscience & Biobehavioral Reviews.