Scene Construction in Amnesia: An fMRI Study

In recent years, there has been substantial interest in how the human hippocampus not only supports recollection of past experiences, but also the construction of fictitious and future events, and the leverage this might offer for understanding the operating mechanisms of the hippocampus. Evidence that patients with bilateral hippocampal damage and amnesia cannot construct novel or future scenes/events has been influential in driving this line of research forward. There are, however, some patients with hippocampal damage and amnesia who retain the ability to construct novel scenes. This dissociation may indicate that the hippocampus is not required for scene construction, or alternatively, there could be residual function in remnant hippocampal tissue sufficient to support the basic construction of scenes. Resolving this controversy is central to current theoretical debates about the hippocampus. To investigate, we used fMRI and a scene construction task to test patient P01, who has dense amnesia, ∼50% bilateral hippocampal volume loss, and intact scene construction. We found that scene construction in P01 was associated with increased activity in a set of brain areas, including medial temporal, retrosplenial, and posterior parietal cortices, that overlapped considerably with the regions engaged in control participants performing the same task. Most notably, the remnant of P01's right hippocampus exhibited increased activity during scene construction. This suggests that the intact scene construction observed in some hippocampal-damaged amnesic patients may be supported by residual function in their lesioned hippocampus, in accordance with theoretical frameworks that ascribe a vital role to the hippocampus in scene construction.

[1]  E. Maguire,et al.  Attenuated Boundary Extension Produces a Paradoxical Memory Advantage in Amnesic Patients , 2012, Current Biology.

[2]  Eleanor A. Maguire,et al.  Patient HC with developmental amnesia can construct future scenarios , 2011, Neuropsychologia.

[3]  D. Schacter,et al.  Hippocampal contributions to the episodic simulation of specific and general future events , 2011, Hippocampus.

[4]  M. Corballis,et al.  A role for the hippocampus in encoding simulations of future events , 2011, Proceedings of the National Academy of Sciences.

[5]  Mieke Verfaellie,et al.  Medial Temporal Lobe Damage Causes Deficits in Episodic Memory and Episodic Future Thinking Not Attributable to Deficits in Narrative Construction , 2011, The Journal of Neuroscience.

[6]  E. Maguire,et al.  The effect of hippocampal damage in children on recalling the past and imagining new experiences , 2011, Neuropsychologia.

[7]  Demis Hassabis,et al.  Role of the hippocampus in imagination and future thinking , 2011, Proceedings of the National Academy of Sciences.

[8]  Edward B. O'Neil,et al.  Preserved hippocampal novelty responses following anterior temporal‐lobe resection that impairs familiarity but spares recollection , 2010, Hippocampus.

[9]  Kristin N. Mauldin,et al.  Role of the hippocampus in remembering the past and imagining the future , 2010, Proceedings of the National Academy of Sciences.

[10]  Demis Hassabis,et al.  Imagining fictitious and future experiences: Evidence from developmental amnesia , 2010, Neuropsychologia.

[11]  Orna Aizenstein,et al.  Bilateral hippocampal lesion and a selective impairment of the ability for mental time travel , 2010, Neurocase.

[12]  D. Hassabis,et al.  Autobiographical memory in semantic dementia: A longitudinal fMRI study , 2010, Neuropsychologia.

[13]  Boris Suchan,et al.  Foreseeing the future: Occurrence probability of imagined future events modulates hippocampal activation , 2009, Hippocampus.

[14]  G. Winocur,et al.  Amnesia as an impairment of detail generation and binding: Evidence from personal, fictional, and semantic narratives in K.C. , 2009, Neuropsychologia.

[15]  D. Schacter,et al.  On the nature of medial temporal lobe contributions to the constructive simulation of future events , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[16]  Demis Hassabis,et al.  The construction system of the brain , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[17]  R. Nathan Spreng,et al.  The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis , 2009, Journal of Cognitive Neuroscience.

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

[19]  G. Winocur,et al.  Memory for familiar environments learned in the remote past: fMRI studies of healthy people and an amnesic person with extensive bilateral hippocampal lesions , 2007, Hippocampus.

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

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

[22]  D. Schacter,et al.  The cognitive neuroscience of constructive memory: remembering the past and imagining the future , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[23]  Alana T. Wong,et al.  Remembering the past and imagining the future: Common and distinct neural substrates during event construction and elaboration , 2007, Neuropsychologia.

[24]  R. Buckner,et al.  Opinion TRENDS in Cognitive Sciences Vol.11 No.2 Self-projection and the brain , 2022 .

[25]  D. Hassabis,et al.  Patients with hippocampal amnesia cannot imagine new experiences , 2007, Proceedings of the National Academy of Sciences.

[26]  K. Szpunar,et al.  Neural substrates of envisioning the future , 2007, Proceedings of the National Academy of Sciences.

[27]  Karl J. Friston,et al.  Design and analysis of fMRI studies with neurologically impaired patients , 2006, Journal of magnetic resonance imaging : JMRI.

[28]  Andrew P. Yonelinas,et al.  Sparing of the familiarity component of recognition memory in a patient with hippocampal pathology , 2005, Neuropsychologia.

[29]  Larry R Squire,et al.  Quantifying medial temporal lobe damage in memory‐impaired patients † , 2005, Hippocampus.

[30]  Masatoshi Itoh,et al.  Thinking of the future and past: the roles of the frontal pole and the medial temporal lobes , 2003, NeuroImage.

[31]  P. McKenna,et al.  Preserved Semantic Learning in an Amnesic Patient , 2002, Cortex.

[32]  P. Garthwaite,et al.  Investigation of the single case in neuropsychology: confidence limits on the abnormality of test scores and test score differences , 2002, Neuropsychologia.

[33]  J. Kihlstrom,et al.  THE EFFECTS OF EPISODIC MEMORY LOSS ON AN AMNESIC PATIENT ’ S ABILITY TO REMEMBER THE PAST AND IMAGINE THE FUTURE , 2003 .

[34]  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.

[35]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[38]  D. C. Howell,et al.  Comparing an Individual's Test Score Against Norms Derived from Small Samples , 1998 .

[39]  M. Moser,et al.  Functional differentiation in the hippocampus , 1998, Hippocampus.

[40]  Daniel L. Schacter,et al.  Priming of semantic autobiographical knowledge: A case study of retrograde amnesia , 1988, Brain and Cognition.

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

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