Neural bases of autobiographical support for episodic recollection of faces

Incidental retrieval of autobiographical knowledge can provide rich contextual support for episodic recollection of a recent event. We examined the neural bases of these two processes by performing fMRI scanning during a recognition memory test for faces that were unfamiliar, famous, or personally known. The presence of pre‐experimental knowledge of a face was incidental to the task, but nonetheless resulted in improved performance. Two distinct networks of activation were associated with correct recollection of a face's prior presentation (recollection hits vs. correct rejections) on one hand, and with pre‐experimental knowledge about it (famous or personally known vs. unfamiliar faces) on the other. The former included mid/posterior cingulate cortex, precuneus, and ventral striatum. The latter included bilateral hippocampus, retrosplenial, and ventromedial prefrontal cortices. Anterior and medial thalamic activations showed an interaction between both effects, driven by increased activation for recollection of unfamiliar faces. When recollecting the presentation of a famous or personally known face, hippocampal activation increased with participants' ratings of how well they felt they knew the person shown. Ventromedial prefrontal cortex showed significantly greater activation for personally known than famous faces. Our results indicate a dissociation between the involvement of retrosplenial vs. mid/posterior cingulate and precuneus in memory tasks. They also indicate that, during recognition memory experiments, the hippocampus supports incidental retrieval of pre‐experimental knowledge about the stimuli presented. This type of knowledge likely underlies the additional recollection found for prior presentation of well known stimuli compared with novel ones and may link hippocampal activation at encoding to subsequent memory performance more generally. © 2009 Wiley‐Liss, Inc.

[1]  I. Daum,et al.  Associations evoked during memory encoding recruit the context‐network , 2009, Hippocampus.

[2]  Larry Cahill The amygdala and emotional memory , 2000 .

[3]  Benjamin J. Shannon,et al.  Parietal lobe contributions to episodic memory retrieval , 2005, Trends in Cognitive Sciences.

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

[5]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[7]  Richard S. J. Frackowiak,et al.  The Mind's Eye—Precuneus Activation in Memory-Related Imagery , 1995, NeuroImage.

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

[9]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[10]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[11]  C D Frith,et al.  The functional roles of prefrontal cortex in episodic memory. II. Retrieval. , 1998, Brain : a journal of neurology.

[12]  J. S. Snowden,et al.  Semantic dementia: Autobiographical contribution to preservation of meaning , 1995 .

[13]  M. Conway Sensory-perceptual episodic memory and its context: autobiographical memory. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[14]  Jason P. Mitchell,et al.  Dissociable Medial Prefrontal Contributions to Judgments of Similar and Dissimilar Others , 2006, Neuron.

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

[16]  Karl J. Friston,et al.  Conjunction revisited , 2005, NeuroImage.

[17]  Morris Moscovitch,et al.  Recollective qualities modulate hippocampal activation during autobiographical memory retrieval , 2004, Hippocampus.

[18]  B. Levine,et al.  The functional neuroanatomy of autobiographical memory: A meta-analysis , 2006, Neuropsychologia.

[19]  H. Lanfermann,et al.  Engagement of Lateral and Medial Prefrontal Areas in the Ecphory of Sad and Happy Autobiographical Memories , 2003, Cortex.

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

[21]  E. Tulving,et al.  Episodic memory and the self in a case of isolated retrograde amnesia. , 1998, Brain : a journal of neurology.

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

[23]  N. Burgess,et al.  The hippocampus is required for short‐term topographical memory in humans , 2007, Hippocampus.

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

[25]  M Moscovitch,et al.  Hippocampal complex and retrieval of recent and very remote autobiographical memories: Evidence from functional magnetic resonance imaging in neurologically intact people , 2001, Hippocampus.

[26]  J. Gardiner,et al.  Recollective experience in word and nonword recognition , 1990, Memory & cognition.

[27]  Neal J. Cohen,et al.  The Long and the Short of It: Relational Memory Impairments in Amnesia, Even at Short Lags , 2006, The Journal of Neuroscience.

[28]  Matthew Brett,et al.  The neural basis of autobiographical and semantic memory: New evidence from three PET studies , 2003, Cognitive, affective & behavioral neuroscience.

[29]  E. Phelps Human emotion and memory: interactions of the amygdala and hippocampal complex , 2004, Current Opinion in Neurobiology.

[30]  Andy C. H. Lee,et al.  Specialization in the medial temporal lobe for processing of objects and scenes , 2005, Hippocampus.

[31]  Neil Burgess,et al.  Anterior prefrontal involvement in episodic retrieval reflects contextual interference , 2005, NeuroImage.

[32]  M. W. Brown,et al.  Episodic memory, amnesia, and the hippocampal–anterior thalamic axis , 1999, Behavioral and Brain Sciences.

[33]  R. Dolan,et al.  Beta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[34]  E. Maguire The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. , 2001, Scandinavian journal of psychology.

[35]  M. Moscovitch,et al.  The contribution of autobiographical significance to semantic memory , 2003, Memory & cognition.

[36]  E. Maguire,et al.  A Temporoparietal and Prefrontal Network for Retrieving the Spatial Context of Lifelike Events , 2001, NeuroImage.

[37]  Margot J. Taylor,et al.  Neural correlates of personally familiar faces: Parents, partner and own faces , 2009, Human brain mapping.

[38]  G. Winocur,et al.  In Search of the Self: A Positron Emission Tomography Study , 1999 .

[39]  James L. McGaugh,et al.  Mechanisms of emotional arousal and lasting declarative memory , 1998, Trends in Neurosciences.

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

[41]  D. Schacter,et al.  Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval , 1999, Hippocampus.

[42]  M H Buonocore,et al.  Hippocampal, parahippocampal and occipital-temporal contributions to associative and item recognition memory: an fMRI study , 2001, Neuroreport.

[43]  R. Henson,et al.  Neural activity associated with episodic memory for emotional context , 2001, Neuropsychologia.

[44]  Brian Levine,et al.  The Functional Neuroanatomy of Episodic and Semantic Autobiographical Remembering: A Prospective Functional MRI Study , 2004, Journal of Cognitive Neuroscience.

[45]  T. Shallice,et al.  The functional roles of prefrontal cortex in episodic memory. I. Encoding. , 1998, Brain : a journal of neurology.

[46]  E Tulving,et al.  Neuroanatomical correlates of retrieval in episodic memory: auditory sentence recognition. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[47]  E. Tulving Memory and consciousness. , 1985 .

[48]  N. Burgess,et al.  The Hippocampus Supports Recognition Memory for Familiar Words but Not Unfamiliar Faces , 2008, Current Biology.

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

[50]  R. Henson,et al.  Electrophysiological and haemodynamic correlates of face perception, recognition and priming. , 2003, Cerebral cortex.

[51]  E. Maguire,et al.  Patterns of hippocampal‐cortical interaction dissociate temporal lobe memory subsystems , 2000, Hippocampus.

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

[53]  Carlo Caltagirone,et al.  Recognition memory for single items and for associations in amnesic patients , 2004, Neuropsychologia.

[54]  C. N. Macrae,et al.  Finding the Self? An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[55]  J. Gurd,et al.  Remote memory and lexical retrieval in a case of frontal Pick's disease. , 1994, Archives of neurology.

[56]  S. Becker,et al.  Remembering the past and imagining the future: a neural model of spatial memory and imagery. , 2007, Psychological review.

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

[58]  Richard N. A. Henson,et al.  Recognition memory for faces and scenes in amnesia: Dissociable roles of medial temporal lobe structures , 2007, Neuropsychologia.

[59]  M. Mishkin,et al.  The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. , 2001, Brain : a journal of neurology.

[60]  Raymond J. Dolan,et al.  Familiarity enhances invariance of face representations in human ventral visual cortex: fMRI evidence , 2005, NeuroImage.

[61]  Kevin S. LaBar,et al.  Co-activation of the amygdala, hippocampus and inferior frontal gyrus during autobiographical memory retrieval , 2005, Neuropsychologia.

[62]  Peter Fransson,et al.  Access to the Published Version May Require Journal Subscription. Published with Permission From: Elsevier Fmri Activity in the Medial Temporal Lobe during Famous Face Processing , 2022 .

[63]  E. Tulving,et al.  Episodic and declarative memory: Role of the hippocampus , 1998, Hippocampus.

[64]  Gereon R Fink,et al.  Differential remoteness and emotional tone modulate the neural correlates of autobiographical memory. , 2003, Brain : a journal of neurology.

[65]  Pascale Piolino,et al.  Hippocampal activation for autobiographical memories over the entire lifetime in healthy aged subjects: an fMRI study. , 2007, Cerebral cortex.

[66]  R L Klatzky,et al.  Recognizing familiar and unfamiliar faces , 1984, Memory & cognition.

[67]  Asaf Gilboa,et al.  Autobiographical and episodic memory—one and the same? Evidence from prefrontal activation in neuroimaging studies , 2004, Neuropsychologia.

[68]  J. Hodges,et al.  Differentiating the roles of the hippocampal complex and the neocortex in long-term memory storage: evidence from the study of semantic dementia and Alzheimer's disease. , 1997, Neuropsychology.

[69]  Scott T. Grafton,et al.  Amygdala activity related to enhanced memory for pleasant and aversive stimuli , 1999, Nature Neuroscience.

[70]  Hiroshi Fukuda,et al.  Cortical mechanisms of person representation: Recognition of famous and personally familiar names , 2006, NeuroImage.

[71]  A. Thiel,et al.  Right amygdalar and temporofrontal activation during autobiographic, but not during fictitious memory retrieval. , 2000, Behavioural neurology.

[72]  Ellen Leibenluft,et al.  Social and emotional attachment in the neural representation of faces , 2004, NeuroImage.

[73]  M. Conway,et al.  The construction of autobiographical memories in the self-memory system. , 2000, Psychological review.

[74]  Suparna Rajaram,et al.  Distinguishing states of awareness from confidence during retrieval: Evidence from amnesia , 2002, Cognitive, affective & behavioral neuroscience.

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

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

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

[78]  D. Hassabis,et al.  Using Imagination to Understand the Neural Basis of Episodic Memory , 2007, The Journal of Neuroscience.

[79]  T. B. Rogers,et al.  Self-reference and the encoding of personal information. , 1977, Journal of personality and social psychology.

[80]  G. Winocur,et al.  Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory , 2005, Journal of anatomy.

[81]  R. Cabeza,et al.  Functional neuroimaging of autobiographical memory , 2007, Trends in Cognitive Sciences.

[82]  H. Eichenbaum,et al.  Memory, amnesia, and the hippocampal system , 1993 .

[83]  Tim Shallice,et al.  Recollection and familiarity in dense hippocampal amnesia: A case study , 2006, Neuropsychologia.

[84]  John A. King,et al.  Memory for events and their spatial context: models and experiments. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[85]  G. Winocur,et al.  Remembering our past: functional neuroanatomy of recollection of recent and very remote personal events. , 2004, Cerebral cortex.

[86]  Neil Burgess,et al.  Parallel memory systems for talking about location and age in precuneus, caudate and Broca's region , 2006, NeuroImage.

[87]  Joseph E LeDoux Emotion Circuits in the Brain , 2000 .

[88]  Tim Shallice,et al.  Fractionation of memory in medial temporal lobe amnesia , 2007, Neuropsychologia.

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

[90]  Frank Haist,et al.  Consolidation of human memory over decades revealed by functional magnetic resonance imaging , 2001, Nature Neuroscience.

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

[92]  Perrine Ruby,et al.  A relation between rest and the self in the brain? , 2003, Brain Research Reviews.

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

[94]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

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

[96]  D. Rubin,et al.  Brain Activity during Episodic Retrieval of Autobiographical and Laboratory Events: An fMRI Study using a Novel Photo Paradigm , 2004, Journal of Cognitive Neuroscience.

[97]  Neil Burgess,et al.  Impaired memory for scenes but not faces in developmental hippocampal amnesia: A case study , 2008, Neuropsychologia.