Neuroanatomical Dissociation of Encoding Processes Related to Priming and Explicit Memory

Priming is a facilitation of cognitive processing with stimulus repetition that can occur without explicit memory. Whereas the functional neuroanatomy of perceptual priming at retrieval is established, encoding processes that initiate priming and explicit memory have not yet been anatomically separated, and we investigated them using event-related functional magnetic resonance imaging. Activations predicting later explicit memory occurred in the bilateral medial temporal lobe (MTL) and left prefrontal cortex (PFC). Activity predicting later priming did not occur in these areas, but rather in the bilateral extrastriate cortex, left fusiform gyrus, and bilateral inferior PFC, areas linked with stimulus identification. Surprisingly, these regions showed response reductions. Our results demonstrate that priming and explicit memory have distinct functional neuroanatomies at encoding, with MTL activations being specific for explicit memory, and suggest that priming is initiated by sharpness of neural responding in stimulus identification areas, consistent with recent electrophysiological evidence regarding priming-related neural oscillations at encoding. We tentatively suggest that this sharpened responding at encoding may set the stage for increased neural processing efficiency at retrieval, with these different neural mechanisms both leading to observed priming-related hemodynamic decreases, and argue that neural measurements at encoding, and not just at retrieval, will be critical in resolving the debate about the neural mechanisms of learning that underlie priming.

[1]  J. Gabrieli,et al.  Word-Identification Priming for Ignored and Attended Words , 1998, Consciousness and Cognition.

[2]  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.

[3]  D. Schacter,et al.  Implicit and explicit memory for new associations in normal and amnesic subjects. , 1985, Journal of experimental psychology. Learning, memory, and cognition.

[4]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[5]  N. Kanwisher,et al.  Neuroimaging of cognitive functions in human parietal cortex , 2001, Current Opinion in Neurobiology.

[6]  Cindy Lustig,et al.  Preserved Neural Correlates of Priming in Old Age and Dementia , 2004, Neuron.

[7]  R L Buckner,et al.  Cognitive neuroscience of episodic memory encoding. , 2000, Acta psychologica.

[8]  Alex Martin,et al.  Properties and mechanisms of perceptual priming , 1998, Current Opinion in Neurobiology.

[9]  J D Gabrieli,et al.  The role of selective attention in perceptual and affective priming. , 2000, The American journal of psychology.

[10]  Andrew P. Yonelinas,et al.  Separating conscious and unconscious influences of memory: measuring recollection , 1993 .

[11]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[12]  Peter Graf,et al.  Implicit Memory : New Directions in Cognition, Development, and Neuropsychology , 1993 .

[13]  F. Craik,et al.  The Oxford handbook of memory , 2006 .

[14]  M. Stone,et al.  Attention and conceptual priming : Limits on the effects of divided attention in the category-exemplar production task , 1999 .

[15]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

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

[17]  R. Henson,et al.  Neural response suppression, haemodynamic repetition effects, and behavioural priming , 2003, Neuropsychologia.

[18]  John M. Gardiner,et al.  Retrieval volition and memorial awareness in stem completion: An empirical analysis , 1995, Psychological research.

[19]  M. Behrmann,et al.  Parietal cortex and attention , 2004, Current Opinion in Neurobiology.

[20]  J M Gardiner,et al.  Involuntary conscious memory and the method of opposition. , 1994, Memory.

[21]  D. Schacter Implicit memory: History and current status. , 1987 .

[22]  R. Habib,et al.  Activation of midbrain structures by associative novelty and the formation of explicit memory in humans. , 2004, Learning & memory.

[23]  R. Henson Neuroimaging studies of priming , 2003, Progress in Neurobiology.

[24]  H. Heinze,et al.  Perceptual Priming Versus Explicit Memory: Dissociable Neural Correlates at Encoding , 2002, Journal of Cognitive Neuroscience.

[25]  Lynn Nadel,et al.  Encyclopedia of Cognitive Science , 2003 .

[26]  Hans-Jochen Heinze,et al.  Redefining implicit and explicit memory: the functional neuroanatomy of priming, remembering, and control of retrieval. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[27]  John M. Gardiner,et al.  Cross-modality priming in stem completion reflects conscious memory, but not voluntary memory , 1996, Psychonomic bulletin & review.

[28]  Karl J. Friston,et al.  Human Brain Function , 1997 .

[29]  G Mandler,et al.  The information that amnesic patients do not forget. , 1984, Journal of experimental psychology. Learning, memory, and cognition.

[30]  R. Henson,et al.  State-related and item-related neural correlates of successful memory encoding , 2002, Nature Neuroscience.

[31]  R. Desimone,et al.  Neural mechanisms for visual memory and their role in attention. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Robert A. Bjork,et al.  Measures of Memory , 1988 .

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

[34]  Robert A. Bjork,et al.  Memory, Long-Term , 2006 .

[35]  E Tulving,et al.  Priming and human memory systems. , 1990, Science.

[36]  Emrah Düzel,et al.  Early, partly anticipatory, neural oscillations during identification set the stage for priming , 2005, NeuroImage.

[37]  Jeffrey S. Bowers,et al.  Rethinking Implicit Memory , 2002 .

[38]  Moshe Bar,et al.  The rise and fall of priming: how visual exposure shapes cortical representations of objects. , 2005, Cerebral cortex.

[39]  P. König,et al.  Top-down processing mediated by interareal synchronization. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Alan Richardson-Klavehn,et al.  Level of processing and the process-dissociation procedure: Elusiveness of null effects on estimates of automatic retrieval , 2002, Memory.

[41]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[42]  T. Shallice,et al.  Recollection and Familiarity in Recognition Memory: An Event-Related Functional Magnetic Resonance Imaging Study , 1999, The Journal of Neuroscience.

[43]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[44]  John M. Gardiner,et al.  Conjoint Dissociations Reveal Involuntary “Perceptual” Priming from Generating at Study , 1999, Consciousness and Cognition.

[45]  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.

[46]  J. Hall,et al.  Learning as a function of word-frequency. , 1954, The American journal of psychology.

[47]  L. Jacoby Remembering the data: analyzing interactive processes in reading , 1983 .

[48]  Daniel L. Schacter,et al.  On the Relations among Priming, Conscious Recollection, and Intentional Retrieval: Evidence from Neuroimaging Research , 1998, Neurobiology of Learning and Memory.

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

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

[51]  L. Jacoby Perceptual enhancement: persistent effects of an experience. , 1983, Journal of experimental psychology. Learning, memory, and cognition.

[52]  J M Gardiner,et al.  Depth-of-processing effects on priming in stem completion: tests of the voluntary-contamination, conceptual-processing, and lexical-processing hypotheses. , 1998, Journal of experimental psychology. Learning, memory, and cognition.

[53]  O Josephs,et al.  Event-related functional magnetic resonance imaging: modelling, inference and optimization. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[54]  R. Bjork,et al.  Intention and awareness in perceptual identification priming , 1994, Memory & cognition.

[55]  D. Schacter,et al.  Memory systems of 1999 , 2000 .