Medial temporal lobe BOLD activity at rest predicts individual differences in memory ability in healthy young adults

Human beings differ in their ability to form and retrieve lasting long-term memories. To explore the source of these individual differences, we used functional magnetic resonance imaging to measure blood-oxygen-level-dependent (BOLD) activity in healthy young adults (n = 50) during periods of resting fixation that were interleaved with periods of simple cognitive tasks. We report that medial temporal lobe BOLD activity during periods of rest predicts individual differences in memory ability. Specifically, individuals who exhibited greater magnitudes of task-induced deactivations in medial temporal lobe BOLD signal (as compared to periods of rest) demonstrated superior memory during offline testing. This relationship was independent of differences in general cognitive function and persisted across different control tasks (i.e., number judgment versus checkerboard detection) and experimental designs (i.e., blocked versus event-related). These results offer a neurophysiological basis for the variability in mnemonic ability that is present amongst healthy young adults and may help to guide strategies aimed at early detection and intervention of neurological and mnemonic impairment.

[1]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[2]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

[3]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

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

[5]  Philip McGuire,et al.  Brain activity during stimulus independent thought. , 1996 .

[6]  C. Frith,et al.  Performance-related activity in medial rostral prefrontal cortex (area 10) during low-demand tasks. , 2006, Journal of experimental psychology. Human perception and performance.

[7]  W. M. van der Flier,et al.  Volumetric MRI predicts rate of cognitive decline related to AD and cerebrovascular disease , 2003, Neurology.

[8]  C. Van Petten,et al.  Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: review and meta-analysis. , 2004, Neuropsychologia.

[9]  R. Stickgold.  Sleep-dependent memory consolidation , 2005, Nature.

[10]  A. Convit,et al.  Hippocampal formation glucose metabolism and volume losses in MCI and AD , 2001, Neurobiology of Aging.

[11]  M. Wilson,et al.  Temporally Structured Replay of Awake Hippocampal Ensemble Activity during Rapid Eye Movement Sleep , 2001, Neuron.

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

[13]  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.

[14]  Hanna Damasio,et al.  Correlations between Regional Brain Volumes and Memory Performance in Anoxia , 2006, Journal of clinical and experimental neuropsychology.

[15]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[16]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[17]  R. Buckner,et al.  Functional-Anatomic Correlates of Individual Differences in Memory , 2006, Neuron.

[18]  David J. Foster,et al.  Reverse replay of behavioural sequences in hippocampal place cells during the awake state , 2006, Nature.

[19]  Timothy D. Wilson,et al.  Prospection: Experiencing the Future , 2007, Science.

[20]  Scott T. Grafton,et al.  Wandering Minds: The Default Network and Stimulus-Independent Thought , 2007, Science.

[21]  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.

[22]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[23]  M. Rugg,et al.  Brain activity before an event predicts later recollection , 2006, Nature Neuroscience.

[24]  Ed X. Wu,et al.  Imaging Physiologic Dysfunction of Individual Hippocampal Subregions in Humans and Genetically Modified Mice , 2000, Neuron.

[25]  M. Mintun,et al.  Brain work and brain imaging. , 2006, Annual review of neuroscience.

[26]  G. Buzsáki,et al.  Forward and reverse hippocampal place-cell sequences during ripples , 2007, Nature Neuroscience.

[27]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[28]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[29]  F. Craik,et al.  The role of rehearsal in short-term memory , 1973 .

[30]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[31]  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.

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

[33]  L. Squire.  Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[34]  Albert K. Lee,et al.  Memory of Sequential Experience in the Hippocampus during Slow Wave Sleep , 2002, Neuron.

[35]  C. Degueldre,et al.  Offline Persistence of Memory-Related Cerebral Activity during Active Wakefulness , 2006, PLoS biology.

[36]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[37]  E. Maguire,et al.  Routes to remembering: the brains behind superior memory , 2003, Nature Neuroscience.

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

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

[40]  M. Greicius,et al.  Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI , 2004, Proc. Natl. Acad. Sci. USA.

[41]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[42]  I. Fried,et al.  Coupling Between Neuronal Firing, Field Potentials, and fMRI in Human Auditory Cortex , 2005, Science.

[43]  N. Stanhope,et al.  Structural MRI volumetric analysis in patients with organic amnesia, 2: correlations with anterograde memory and executive tests in 40 patients , 2001, Journal of neurology, neurosurgery, and psychiatry.

[44]  J. Yesavage,et al.  Structural MRI correlates of recognition memory in Alzheimer's disease , 1998, Journal of the International Neuropsychological Society.

[45]  Henry Schmitz,et al.  Congenital Hemolytic Anemias , 1942 .

[46]  R. Buckner,et al.  Self-projection and the brain , 2007, Trends in Cognitive Sciences.

[47]  Benjamin J. Shannon,et al.  Coherent spontaneous activity identifies a hippocampal-parietal memory network. , 2006, Journal of neurophysiology.

[48]  J. Hodges.  Memory, Amnesia and the Hippocampal System , 1995 .

[49]  J. Binder,et al.  A Parametric Manipulation of Factors Affecting Task-induced Deactivation in Functional Neuroimaging , 2003, Journal of Cognitive Neuroscience.

[50]  B. Mazoyer,et al.  Cortical networks for working memory and executive functions sustain the conscious resting state in man , 2001, Brain Research Bulletin.

[51]  Yaakov Stern,et al.  Imaging hippocampal function across the human life span: Is memory decline normal or not? , 2002, Annals of neurology.