The neural basis of autobiographical memory deficits in transient epileptic amnesia

Transient epileptic amnesia (TEA) is a recently recognized form of temporal lobe epilepsy which is often associated with persistent interictal impairment of autobiographical memory. We used fMRI to investigate the neural basis of this deficit. Eleven patients with TEA, who had no significant deficits on standard tests of anterograde memory, and 17 age and IQ matched healthy controls retrieved memories from across the lifespan. Both groups engaged the autobiographical memory network, but activation in patients was less extensive than in controls. Direct comparison revealed hypoactivation of regions in the right hemisphere. Specifically, patients showed reduced activation of the posterior parahippocampal gyrus (pPHG), especially for mid-life and recent memories, with decreased engagement of the right temporoparietal junction and the cerebellum. In addition, we found reduced effective connectivity in patients between the right pPHG and the right middle temporal gyrus. Our results are consistent with other evidence that TEA is a syndrome of medial temporal lobe epilepsy and indicate that it affects the function and connectivity of regions within the autobiographical memory network.

[1]  N. Muhlert,et al.  Novel forms of forgetting in temporal lobe epilepsy , 2013, Epilepsy & Behavior.

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

[3]  Morris Moscovitch,et al.  The nature and time‐course of medial temporal lobe contributions to semantic retrieval: An fMRI study on verbal fluency , 2012, Hippocampus.

[4]  J R Hodges,et al.  Transient epileptic amnesia: regional brain atrophy and its relationship to memory deficits. , 2009, Brain : a journal of neurology.

[5]  J. Hodges,et al.  Focal retrograde amnesia: Extending the clinical syndrome of transient epileptic amnesia , 2010, Journal of Clinical Neuroscience.

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

[7]  J. Panksepp,et al.  The flow of anoetic to noetic and autonoetic consciousness: A vision of unknowing (anoetic) and knowing (noetic) consciousness in the remembrance of things past and imagined futures , 2009, Consciousness and Cognition.

[8]  Demis Hassabis,et al.  Differential engagement of brain regions within a ‘core’ network during scene construction , 2010, Neuropsychologia.

[9]  C. Butler,et al.  Transient epileptic amnesia. , 2010, Current opinion in neurology.

[10]  J. Hodges,et al.  The syndrome of transient epileptic amnesia , 2007, Annals of neurology.

[11]  N. Kapur,et al.  Epilepsy and Memory , 2012 .

[12]  M. Saling,et al.  Verbal memory in mesial temporal lobe epilepsy: beyond material specificity. , 2009, Brain : a journal of neurology.

[13]  F. L. D. Silva,et al.  Kindling of the hippocampus induces spatial memory deficits in the rat , 1986, Neuroscience Letters.

[14]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[15]  A. Zeman,et al.  Transient epileptic amnesia: déjà vu heralding recovery of lost memories , 2010, Journal of Neurology, Neurosurgery & Psychiatry.

[16]  G. Winocur,et al.  Aging and autobiographical memory: dissociating episodic from semantic retrieval. , 2002, Psychology and aging.

[17]  A. Zeman,et al.  A case of transient epileptic amnesia with radiological localization , 2008, Nature Clinical Practice Neurology.

[18]  N. Roberts,et al.  Voxel‐based morphometry of temporal lobe epilepsy: An introduction and review of the literature , 2008, Epilepsia.

[19]  Bruce Hermann,et al.  The impact of epilepsy from the patient’s perspective I. Descriptions and subjective perceptions , 2000, Epilepsy Research.

[20]  J. Desmond,et al.  Neuroimaging studies of the cerebellum: language, learning and memory , 1998, Trends in Cognitive Sciences.

[21]  Morris Moscovitch,et al.  Determinants of autobiographical memory in patients with unilateral temporal lobe epilepsy or excisions , 2009, Neuropsychologia.

[22]  R. Corcoran,et al.  Memory failure in epilepsy: retrospective reports and prospective recordings , 1992, Seizure.

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

[24]  M. H. Mendes,et al.  Transient epileptic amnesia: an under-diagnosed phenomenon? Three more cases , 2002, Seizure.

[25]  L. Squire,et al.  The neuroscience of remote memory , 2007, Current Opinion in Neurobiology.

[26]  F. Manes,et al.  Focal autobiographical amnesia in association with transient epileptic amnesia. , 2001, Brain : a journal of neurology.

[27]  Karl J. Friston,et al.  Combining Spatial Extent and Peak Intensity to Test for Activations in Functional Imaging , 1997, NeuroImage.

[28]  E A Maguire,et al.  Neuroimaging studies of autobiographical event memory. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  B. Steinhoff,et al.  Remote Memory in Temporal Lobe Epilepsy , 2006, Epilepsia.

[30]  Laurie Miller,et al.  Effects of Temporal Lobe Lesions on Retrograde Memory: A Critical Review , 2008, Neuropsychology Review.

[31]  N. Muhlert,et al.  Accelerated forgetting of real-life events in Transient Epileptic Amnesia , 2010, Neuropsychologia.

[32]  A. Zeman,et al.  Recent insights into the impairment of memory in epilepsy: transient epileptic amnesia, accelerated long-term forgetting and remote memory impairment. , 2008, Brain : a journal of neurology.

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

[34]  Abdelmalek Benattayallah,et al.  An fMRI study of long-term everyday memory using SenseCam , 2011, Memory.

[35]  Rachel A. Diana,et al.  Imaging recollection and familiarity in the medial temporal lobe: a three-component model , 2007, Trends in Cognitive Sciences.

[36]  A D Baddeley,et al.  The autobiographical memory interview: a new assessment of autobiographical and personal semantic memory in amnesic patients. , 1989, Journal of clinical and experimental neuropsychology.

[37]  Karl J. Friston,et al.  Scanning patients with tasks they can perform , 1999, Human brain mapping.

[38]  M. Mesulam,et al.  Accelerated Forgetting in Association with Temporal Lobe Epilepsy and Paraneoplastic Encephalitis , 1997, Brain and Cognition.

[39]  E. H. Burrows,et al.  Focal retrograde amnesia following bilateral temporal lobe pathology. A neuropsychological and magnetic resonance study. , 1992, Brain : a journal of neurology.

[40]  P. Osterrieth Le test de copie d'une figure complexe , 1944 .

[41]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

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

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

[44]  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.

[45]  R. Gallassi Epileptic Amnesic Syndrome: An Update and Further Considerations , 2006, Epilepsia.

[46]  Pascale Piolino,et al.  Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings , 2009, Neuropsychologia.

[47]  D. Hassabis,et al.  Deconstructing episodic memory with construction , 2007, Trends in Cognitive Sciences.

[48]  M Baulac,et al.  Autobiographical memory after temporal lobe resection: neuropsychological and MRI volumetric findings. , 2007, Brain : a journal of neurology.

[49]  Klaas E. Stephan,et al.  Dynamic causal modelling: A critical review of the biophysical and statistical foundations , 2011, NeuroImage.

[50]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[51]  Indre V. Viskontas,et al.  Remote Episodic Memory Deficits in Patients with Unilateral Temporal Lobe Epilepsy and Excisions , 2000, The Journal of Neuroscience.

[52]  Martin A. Conway,et al.  Using SenseCam with an amnesic patient: Accessing inaccessible everyday memories , 2011, Memory.

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

[54]  Eric Guedj,et al.  Long-term consolidation of declarative memory: insight from temporal lobe epilepsy. , 2011, Brain : a journal of neurology.

[55]  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.

[56]  M. Moscovitch,et al.  The immediacy of recollection: The use of the historical present in narratives of autobiographical episodes by patients with unilateral temporal lobe epilepsy , 2011, Neuropsychologia.

[57]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

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

[59]  E. Lugaresi,et al.  Epilepsy Presenting as Memory Disturbances , 1988, Epilepsia.

[60]  M. E. Corcoran,et al.  Kindling of hippocampal field CA1 impairs spatial learning and retention in the Morris water maze , 1996, Behavioural Brain Research.

[61]  Jean-Baptiste Poline,et al.  Analysis of a large fMRI cohort: Statistical and methodological issues for group analyses , 2007, NeuroImage.

[62]  J. Gardiner Episodic memory and autonoetic consciousness: a first-person approach. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[63]  N. Muhlert,et al.  Remote memory deficits in transient epileptic amnesia. , 2010, Brain : a journal of neurology.

[64]  Gregory P. Lee,et al.  Impaired Long-Term Retention Despite Normal Verbal Learning in Patients With Temporal Lobe Dysfunction , 1991 .

[65]  Morris Moscovitch,et al.  The contribution of autobiographical significance to semantic memory: evidence from Alzheimer’s disease, semantic dementia, and amnesia , 2004, Neuropsychologia.

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

[67]  Arthur MacNeill Horton,et al.  Wechsler Memory Scale III , 1999 .

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

[69]  Brian Everitt,et al.  A systematic review and quantitative appraisal of fMRI studies of verbal fluency: Role of the left inferior frontal gyrus , 2006, Human brain mapping.

[70]  Transient epileptic amnesia: a description of the clinical and neuropsychological features in 10 cases and a review of the literature , 2000 .

[71]  Morris Moscovitch,et al.  Consequences of hippocampal damage across the autobiographical memory network in left temporal lobe epilepsy. , 2007, Brain : a journal of neurology.

[72]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[73]  Morris Moscovitch,et al.  Characterizing spatial and temporal features of autobiographical memory retrieval networks: a partial least squares approach , 2004, NeuroImage.

[74]  Cheryl L. Grady,et al.  Common and Unique Neural Activations in Autobiographical, Episodic, and Semantic Retrieval , 2007, Journal of Cognitive Neuroscience.

[75]  N. Muhlert,et al.  The neural correlates of everyday recognition memory , 2011, Brain and Cognition.

[76]  Karl J. Friston,et al.  Nonlinear Responses in fMRI: The Balloon Model, Volterra Kernels, and Other Hemodynamics , 2000, NeuroImage.

[77]  L. Barsalou The content and organization of autobiographical memories , 1988 .

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

[79]  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.

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

[81]  Hans J. Markowitsch,et al.  Memory, autonoetic consciousness, and the self , 2011, Consciousness and Cognition.

[82]  Hellmuth Obrig,et al.  Focal Retrograde Amnesia: Voxel-Based Morphometry Findings in a Case without MRI Lesions , 2011, PloS one.

[83]  Craig E. L. Stark,et al.  When zero is not zero: The problem of ambiguous baseline conditions in fMRI , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[84]  A. Mechelli,et al.  Functional integration between the posterior hippocampus and prefrontal cortex is impaired in both first episode schizophrenia and the at risk mental state. , 2009, Brain : a journal of neurology.