Executive Control during Episodic Retrieval Multiple Prefrontal Processes Subserve Source Memory

During recognition, one may sense items as familiar (item memory) and additionally recollect specific contextual details of the earlier encounters (source memory). Cognitive theory suggests that, unlike item memory, source memory requires controlled cue specification and monitoring processes. Functional imaging suggests that such processes may depend on left prefrontal cortex (PFC). However, the nature and possible anatomical segregation of these processes remains unknown. Using functional magnetic resonance imaging, we isolated distinct response patterns in left PFC during source memory consistent with semantic analysis/cue specification (anterior ventrolateral), recollective monitoring (posterior dorsolateral and frontopolar), and phonological maintenance/rehearsal (posterior ventrolateral). Importantly, cue specification and recollective monitoring responses were not seen during item memory and were unaffected by retrieval success, demonstrating that the mere attempt to recollect episodic detail engages multiple control processes with different left PFC substrates.

[1]  P W Burgess,et al.  Confabulation and the control of recollection. , 1996, Memory.

[2]  P. Suppes,et al.  Contemporary Developments in Mathematical Psychology , 1976 .

[3]  J. B. Demb,et al.  Functional Magnetic Resonance Imaging of Semantic Memory Processes in the Frontal Lobes , 1996 .

[4]  L. Squire,et al.  Cognitive impairment following frontal lobe damage and its relevance to human amnesia. , 1989 .

[5]  Richard S. J. Frackowiak,et al.  Brain regions associated with acquisition and retrieval of verbal episodic memory , 1994, Nature.

[6]  Richard C. Atkinson,et al.  Search and decision processes in recognition memory. , 1974 .

[7]  D. Schacter,et al.  Task-specific repetition priming in left inferior prefrontal cortex. , 2000, Cerebral cortex.

[8]  Daniel L. Schacter,et al.  Retrieval without Recollection: An Experimental Analysis of Source Amnesia , 1984 .

[9]  A P Shimamura,et al.  Cognitive impairment following frontal lobe damage and its relevance to human amnesia. , 1989, Behavioral neuroscience.

[10]  W P Banks,et al.  Recognition and Source Memory as Multivariate Decision Processes , 2000, Psychological science.

[11]  Jason P. Mitchell,et al.  The Seven Sins of Memory , 2003, Annals of the New York Academy of Sciences.

[12]  Arthur P. Shimamura,et al.  What is the role of frontal lobe damage in memory disorders , 1991 .

[13]  N Burgess,et al.  Recoding, storage, rehearsal and grouping in verbal short-term memory: an fMRI study , 2000, Neuropsychologia.

[14]  M. Buonocore,et al.  Remembering familiar people: the posterior cingulate cortex and autobiographical memory retrieval , 2001, Neuroscience.

[15]  Edward E. Smith,et al.  Dissociation of Storage and Rehearsal in Verbal Working Memory: Evidence From Positron Emission Tomography , 1996 .

[16]  A. Yonelinas Receiver-operating characteristics in recognition memory: evidence for a dual-process model. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

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

[18]  G. Mandler Recognizing: The judgment of previous occurrence. , 1980 .

[19]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[20]  David J. Turk,et al.  A positron emission tomography (PET) study of autobiographical memory retrieval. , 1999, Memory.

[21]  Daniel G. Bobrow,et al.  Descriptions: An intermediate stage in memory retrieval , 1979, Cognitive Psychology.

[22]  E. Balint Memory and consciousness. , 1987, The International journal of psycho-analysis.

[23]  Jemett L. Desmond,et al.  Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  Morris Moscovitch,et al.  Strategic retrieval and the frontal lobes: Evidence from confabulation and amnesia , 1997, Neuropsychologia.

[25]  Richard M. Shiffrin,et al.  Cuing effects and associative information in recognition memory , 1992, Memory & cognition.

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

[27]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[28]  Michael D. Rugg,et al.  The Role of the Prefrontal Cortex in Recognition Memory and Memory for Source: An fMRI Study , 1999, NeuroImage.

[29]  A. Dale,et al.  Functional–Anatomic Study of Episodic Retrieval II. Selective Averaging of Event-Related fMRI Trials to Test the Retrieval Success Hypothesis , 1998, NeuroImage.

[30]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[31]  R. Buckner,et al.  Dissociation of human prefrontal cortical areas across different speech production tasks and gender groups. , 1995, Journal of neurophysiology.

[32]  E. Maguire,et al.  Differential modulation of a common memory retrieval network revealed by positron emission tomography , 1999, Hippocampus.

[33]  E K Warrington,et al.  Selective impairment of memory and visual perception in splenial tumours. , 1991, Brain : a journal of neurology.

[34]  P F Liddle,et al.  The role of the left prefrontal cortex in verbal processing: semantic processing or willed action? , 1994, Neuroreport.

[35]  F. Miezin,et al.  Functional anatomical studies of explicit and implicit memory retrieval tasks , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  R. Buckner,et al.  Neural Correlates of Episodic Retrieval Success , 2000, NeuroImage.

[37]  Andrew P Yonelinas,et al.  Novelty effects on recollection and familiarity in recognition memory , 2003, Memory & cognition.

[38]  E Valenstein,et al.  Retrosplenial amnesia. , 1987, Brain : a journal of neurology.

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

[40]  Lila Davachi,et al.  When Keeping in Mind Supports Later Bringing to Mind: Neural Markers of Phonological Rehearsal Predict Subsequent Remembering , 2001, Journal of Cognitive Neuroscience.

[41]  Marcia K. Johnson,et al.  Source monitoring. , 1993, Psychological bulletin.

[42]  Arthur P. Shimamura,et al.  Source memory impairment in patients with frontal lobe lesions , 1989, Neuropsychologia.

[43]  J D Gabrieli,et al.  Dissociations between familiarity processes in explicit recognition and implicit perceptual memory. , 1997, Journal of experimental psychology. Learning, memory, and cognition.

[44]  A P Yonelinas,et al.  The contribution of recollection and familiarity to recognition and source-memory judgments: a formal dual-process model and an analysis of receiver operating characteristics. , 1999, Journal of experimental psychology. Learning, memory, and cognition.

[45]  Marcia K. Johnson,et al.  Left prefrontal activation during episodic remembering: an event‐related fMRI study , 1998, Neuroreport.

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

[47]  Trying versus Succeeding Event-Related Designs Dissociate Memory Processes , 1999, Neuron.

[48]  G. Fink,et al.  Cerebral Representation of One’s Own Past: Neural Networks Involved in Autobiographical Memory , 1996, The Journal of Neuroscience.

[49]  D. Schacter,et al.  The cognitive neuroscience of constructive memory. , 1998, Annual review of psychology.

[50]  L. Jacoby A process dissociation framework: Separating automatic from intentional uses of memory , 1991 .

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

[52]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

[53]  Arthur P. Shimamura,et al.  Memory and metamemory: Comparisons between patients with frontal lobe lesions and amnesic patients , 1989, Psychobiology.

[54]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[55]  A. Stone,et al.  The Seven Sins of Memory: How the Mind Forgets and Remembers , 2001 .

[56]  A. Benton,et al.  Frontal Lobe Function and Dysfunction , 1991 .

[57]  J. Taylor,et al.  Episodic retrieval activates the precuneus irrespective of the imagery content of word pair associates. A PET study. , 1999, Brain : a journal of neurology.

[58]  Daniel L. Schacter,et al.  The Seven Sins of Memory: How the Mind Forgets and Remembers , 2001 .

[59]  A P Yonelinas,et al.  Predicting individual false alarm rates and signal detection theory: A role for remembering , 2000, Memory & cognition.

[60]  T. Shallice,et al.  Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. , 1999, Brain : a journal of neurology.