Retrieval from Episodic Memory: Neural Mechanisms of Interference Resolution

Selectively retrieving a target memory among related memories requires some degree of inhibitory control over interfering and competing memories, a process assumed to be supported by inhibitory mechanisms. Evidence from behavioral studies suggests that such inhibitory control can lead to subsequent forgetting of the interfering information, a finding called retrieval-induced forgetting [Anderson, M. C., Bjork, R. A., & Bjork, E. L. Remembering can cause forgetting: Retrieval dynamics in long-term memory. Journal of Experimental Psychology: Learning, Memory & Cognition, 20, 1063–1087, 1994]. In the present functional magnetic resonance imaging study, we investigated the neural processes underlying retrieval-induced forgetting and, in particular, examined the extent to which these processes are retrieval (i.e., selection) specific. Participants actively retrieved a subset of previously studied material (selection condition), or were re-exposed to the same material for relearning (nonselection condition). Replicating prior behavioral work, selective retrieval caused significant forgetting of the nonretrieved items on a delayed recall test, relative to the re-exposure condition. Selective retrieval was associated with increased BOLD responses in the posterior temporal and parietal association cortices, in the bilateral hippocampus, and in the dorsolateral prefrontal cortex. Medial and lateral prefrontal areas showed a strong negative linear relationship between selection-related neural activity and subsequent forgetting of competitors. These findings suggest reduced demands on inhibitory control processes when interference is successfully resolved during early selective retrieval from episodic memory.

[1]  David Badre,et al.  Left ventrolateral prefrontal cortex and the cognitive control of memory , 2007, Neuropsychologia.

[2]  M Herrmann,et al.  Control of semantic interference in episodic memory retrieval is associated with an anterior cingulate‐prefrontal activation pattern , 2001, Human brain mapping.

[3]  Michael C. Anderson Rethinking interference theory: Executive control and the mechanisms of forgetting. , 2003 .

[4]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[5]  Bernhard Pastötter,et al.  Retrieval inhibition in autobiographical memory , 2010 .

[6]  Lubna Ahmed,et al.  Transfer appropriate forgetting: The cue-dependent nature of retrieval-induced forgetting. , 2004 .

[7]  R. Cabeza,et al.  Neural bases of learning and memory: functional neuroimaging evidence , 2000, Current opinion in neurology.

[8]  K. Bäuml The list-strength effect: Strength-dependent competition or suppression? , 1997, Psychonomic bulletin & review.

[9]  Michael C. Anderson,et al.  On the status of inhibitory mechanisms in cognition: memory retrieval as a model case. , 1995, Psychological review.

[10]  R. J. Dolan,et al.  Functional Magnetic Resonance Imaging of Proactive Interference during Spoken Cued Recall , 2002, NeuroImage.

[11]  Brenda Milner,et al.  Strategic search and retrieval inhibition: The role of the frontal lobes , 1993, Neuropsychologia.

[12]  R. Henson,et al.  Frontal lobes and human memory: insights from functional neuroimaging. , 2001, Brain : a journal of neurology.

[13]  Karl-Heinz Bäuml,et al.  Semantic Generation Can Cause Episodic Forgetting , 2002, Psychological science.

[14]  U Noppeney,et al.  The neural areas that control the retrieval and selection of semantics , 2004, Neuropsychologia.

[15]  J. K. Chan,et al.  When does Retrieval Induce Forgetting and When does it Induce Facilitation? Implications for Retrieval Inhibition, Testing Effect, and Text Processing , 2009 .

[16]  M. Rugg,et al.  Retrieval processing and episodic memory , 2000, Trends in Cognitive Sciences.

[17]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[18]  Brice A. Kuhl,et al.  Neural Systems Underlying the Suppression of Unwanted Memories , 2004, Science.

[19]  John R. Anderson,et al.  Competition and representation during memory retrieval: Roles of the prefrontal cortex and the posterior parietal cortex , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Axel Mecklinger,et al.  When remembering causes forgetting: electrophysiological correlates of retrieval-induced forgetting. , 2007, Cerebral cortex.

[21]  K. Bäuml,et al.  Retrieval-induced forgetting in young children , 2010, Psychonomic bulletin & review.

[22]  J. Desmond,et al.  Prefrontal regions involved in keeping information in and out of mind. , 2001, Brain : a journal of neurology.

[23]  Harm Veling,et al.  Remembering can cause inhibition: retrieval-induced inhibition as cue independent process. , 2004, Journal of experimental psychology. Learning, memory, and cognition.

[24]  L. Nyberg,et al.  Common fronto-parietal activity in attention, memory, and consciousness: Shared demands on integration? , 2005, Consciousness and Cognition.

[25]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[26]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

[27]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[28]  R. Zacks,et al.  Is retrieval-induced forgetting an inhibitory process? , 2001, The American journal of psychology.

[29]  R. Buckner,et al.  Functional Dissociation among Components of Remembering: Control, Perceived Oldness, and Content , 2003, The Journal of Neuroscience.

[30]  J. Kissler,et al.  Does remembering cause forgetting in chronically stressed people? A study of Ugandan civil war refugees with and without PTSD , 2010 .

[31]  Emiliano Macaluso,et al.  Neural correlates of episodic retrieval: An fMRI study of the part-list cueing effect , 2010, NeuroImage.

[32]  H. Garavan,et al.  Dissociable Executive Functions in the Dynamic Control of Behavior: Inhibition, Error Detection, and Correction , 2002, NeuroImage.

[33]  K. Bäuml,et al.  Theta oscillations predict the detrimental effects of memory retrieval , 2010, Cognitive, affective & behavioral neuroscience.

[34]  Cameron S. Carter,et al.  Separating semantic conflict and response conflict in the Stroop task: A functional MRI study , 2005, NeuroImage.

[35]  Jan Derrfuss,et al.  Cognitive control in the posterior frontolateral cortex: evidence from common activations in task coordination, interference control, and working memory , 2004, NeuroImage.

[36]  Michael C. Anderson,et al.  Inhibitory processes and the control of memory retrieval , 2002, Trends in Cognitive Sciences.

[37]  M. Conway,et al.  Disruption of Inhibitory Control of Memory Following Lesions to the Frontal and Temporal Lobes , 2003, Cortex.

[38]  Elizabeth W. Dunn,et al.  Forgetting by remembering: Stereotype inhibition through rehearsal of alternative aspects of identity , 2003 .

[39]  A P Shimamura,et al.  Retrieval-induced forgetting in episodic memory. , 1999, Journal of experimental psychology. Learning, memory, and cognition.

[40]  Michael C. Anderson,et al.  Inhibiting Your Native Language , 2007, Psychological science.

[41]  W. Montague,et al.  Category norms of verbal items in 56 categories A replication and extension of the Connecticut category norms , 1969 .

[42]  Michael C. Anderson,et al.  Retrieval-induced forgetting: Evidence for a recall-specific mechanism , 2000, Psychonomic bulletin & review.

[43]  K. Bäuml,et al.  Deutschsprachige Normen für Vertreter von 48 Kategorien. , 1995 .

[44]  A. Wagner,et al.  Prefrontal and hippocampal contributions to visual associative recognition: Interactions between cognitive control and episodic retrieval , 2004, Brain and Cognition.

[45]  R. Poldrack,et al.  Dissociable Controlled Retrieval and Generalized Selection Mechanisms in Ventrolateral Prefrontal Cortex , 2005, Neuron.

[46]  Michael C. Anderson,et al.  The Role of Inhibitory Control in Forgetting Semantic Knowledge , 2004, Psychological science.

[47]  Eliot Hazeltine,et al.  Dissociable Contributions of Prefrontal and Parietal Cortices to Response Selection , 2002, NeuroImage.

[48]  D. Schacter,et al.  Functional–Anatomic Study of Episodic Retrieval Using fMRI I. Retrieval Effort versus Retrieval Success , 1998, NeuroImage.

[49]  Karl-Heinz T. Bäuml,et al.  Strong items get suppressed, weak items do not: The role of item strength in output interference , 1998 .

[50]  N. Raz Aging of the brain and its impact on cognitive performance: Integration of structural and functional findings. , 2000 .

[51]  Rugg,et al.  Episodic memory retrieval: an (event-related) functional neuroimaging perspective , 2002 .

[52]  R. McCarley,et al.  Retrieval-induced forgetting in schizophrenia , 2005, Schizophrenia Research.

[53]  Dewey Rundus,et al.  Negative effects of using list items as recall cues , 1973 .

[54]  Hugh Garavan,et al.  Practice‐related functional activation changes in a working memory task , 2000, Microscopy research and technique.

[55]  Michael C. Anderson,et al.  Remembering can cause forgetting: retrieval dynamics in long-term memory. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

[56]  M. Rugg,et al.  Human recognition memory: a cognitive neuroscience perspective , 2003, Trends in Cognitive Sciences.

[57]  J. Raaijmakers,et al.  A model for interference and forgetting , 1988 .

[58]  Anthony D Wagner,et al.  Executive Control during Episodic Retrieval Multiple Prefrontal Processes Subserve Source Memory , 2002, Neuron.

[59]  Alan C. Evans,et al.  BrainWeb: Online Interface to a 3D MRI Simulated Brain Database , 1997 .

[60]  B. J. Casey,et al.  Imaging the developing brain: what have we learned about cognitive development? , 2005, Trends in Cognitive Sciences.

[61]  C. N. Macrae,et al.  Gone but Not Forgotten: The Transient Nature of Retrieval-Induced Forgetting , 2001, Psychological science.

[62]  Simon Hanslmayr,et al.  Binding and inhibition in episodic memory—Cognitive, emotional, and neural processes , 2010, Neuroscience & Biobehavioral Reviews.

[63]  G. Lohmann,et al.  Color-Word Matching Stroop Task: Separating Interference and Response Conflict , 2001, NeuroImage.

[64]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[65]  Brice A. Kuhl,et al.  Decreased demands on cognitive control reveal the neural processing benefits of forgetting , 2007, Nature Neuroscience.

[66]  K. Bäuml,et al.  Retrieval-induced forgetting and part-list cuing in associatively structured lists , 2003, Memory & cognition.

[67]  J. Wixted,et al.  Recall Latency Following Pure- and Mixed-Strength Lists: A Direct Test of the Relative Strength Model of Free Recall , 1997 .

[68]  K. Bäuml,et al.  Part-list cuing as instructed retrieval inhibition , 2004, Memory & cognition.

[69]  Irene P. Kan,et al.  Effects of Repetition and Competition on Activity in Left Prefrontal Cortex during Word Generation , 1999, Neuron.

[70]  Benjamin C. Storm,et al.  Is retrieval success a necessary condition for retrieval-induced forgetting? , 2006, Psychonomic bulletin & review.

[71]  J. Kissler,et al.  ERP dynamics underlying successful directed forgetting of neutral but not negative pictures. , 2011, Social cognitive and affective neuroscience.

[72]  Karl-Heinz Bäuml,et al.  Retrieval-induced forgetting in item recognition: evidence for a reduction in general memory strength. , 2007, Journal of experimental psychology. Learning, memory, and cognition.

[73]  E. Tulving,et al.  Availability versus accessibility of information in memory for words , 1966 .

[74]  A. Shimamura Neuropsychological perspectives on memory and cognitive decline in normal human aging , 1994 .

[75]  Malcolm D. MacLeod,et al.  Retrieval‐induced forgetting in eyewitness memory: forgetting as a consequence of remembering , 2002 .

[76]  R. Henson,et al.  The neural basis of episodic memory: evidence from functional neuroimaging. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.