Changing temporal context in human temporal lobe promotes memory of distinct episodes

Memories of experiences that occur around the same time are linked together by a shared temporal context, represented by shared patterns of neural activity. However, shared temporal context may be problematic for selective retrieval of specific memories. Here, we examine intracranial EEG (iEEG) in the human temporal lobe as participants perform a verbal paired associates memory task that requires the encoding of distinct word pairs in memory. We find that the rate of change in patterns of low frequency (3–12 Hz) power distributed across the temporal lobe is significantly related to memory performance. We also find that exogenous electrical stimulation affects how quickly these neural representations of temporal context change with time, which directly affects the ability to successfully form memories for distinct items. Our results indicate that the ability to retrieve distinct episodic memories is related to how quickly neural representations of temporal context change over time during encoding.Memories formed around the same time are linked together by a shared temporal context. Here, the authors show that the ability to selectively retrieve distinct episodic memories formed close together in time is related to how quickly neural representations of temporal context change over time during encoding.

[1]  Marc W Howard,et al.  Human Episodic Memory Retrieval Is Accompanied by a Neural Contiguity Effect , 2018, The Journal of Neuroscience.

[2]  Sean M. Polyn,et al.  A context maintenance and retrieval model of organizational processes in free recall. , 2009, Psychological review.

[3]  Bradley C. Lega,et al.  Closed-loop stimulation of temporal cortex rescues functional networks and improves memory , 2018, Nature Communications.

[4]  Jeremy R. Manning,et al.  Oscillatory patterns in temporal lobe reveal context reinstatement during memory search , 2011, Proceedings of the National Academy of Sciences.

[5]  B. Staresina,et al.  Medial Temporal Theta/Alpha Power Enhancement Precedes Successful Memory Encoding: Evidence Based on Intracranial EEG , 2011, The Journal of Neuroscience.

[6]  Marc W Howard,et al.  The temporal context model in spatial navigation and relational learning: toward a common explanation of medial temporal lobe function across domains. , 2005, Psychological review.

[7]  Michael J. Jutras,et al.  Direct Brain Stimulation Modulates Encoding States and Memory Performance in Humans , 2017, Current Biology.

[8]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[9]  Orin C. Davis,et al.  Temporal associative processes revealed by intrusions in paired-associate recall , 2008, Psychonomic bulletin & review.

[10]  Per B Sederberg,et al.  The temporal contiguity effect predicts episodic memory performance. , 2010, Memory & cognition.

[11]  Joseph R. Madsen,et al.  Individualized localization and cortical surface-based registration of intracranial electrodes , 2012, NeuroImage.

[12]  K. Zaghloul,et al.  Reinstatement of distributed cortical oscillations occurs with precise spatiotemporal dynamics during successful memory retrieval , 2014, Proceedings of the National Academy of Sciences.

[13]  Sang Ah Lee,et al.  Direct Electrical Stimulation of the Human Entorhinal Region and Hippocampus Impairs Memory , 2016, Neuron.

[14]  Li Lu,et al.  Integrating time from experience in the lateral entorhinal cortex , 2018, Nature.

[15]  C. Stark,et al.  Pattern Separation in the Human Hippocampal CA3 and Dentate Gyrus , 2008, Science.

[16]  Marc W Howard,et al.  The Same Hippocampal CA1 Population Simultaneously Codes Temporal Information over Multiple Timescales , 2018, Current Biology.

[17]  Itzhak Fried,et al.  Theta-burst microstimulation in the human entorhinal area improves memory specificity , 2017, eLife.

[18]  Brian B. Avants,et al.  Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain , 2008, Medical Image Anal..

[19]  H. Eichenbaum,et al.  Hippocampal “Time Cells” Bridge the Gap in Memory for Discontiguous Events , 2011, Neuron.

[20]  Marc W. Howard,et al.  A distributed representation of temporal context , 2002 .

[21]  Dong Song,et al.  Developing a hippocampal neural prosthetic to facilitate human memory encoding and recall , 2018, Journal of neural engineering.

[22]  John J. Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities , 1999 .

[23]  Rafi U. Haque,et al.  Cortical Low-Frequency Power and Progressive Phase Synchrony Precede Successful Memory Encoding , 2015, The Journal of Neuroscience.

[24]  Kareem A. Zaghloul,et al.  Principled Approaches to Direct Brain Stimulation for Cognitive Enhancement , 2017, Front. Neurosci..

[25]  M. Kahana Associative retrieval processes in free recall , 1996, Memory & cognition.

[26]  Rajesh C. Rao,et al.  Memory enhancement and deep-brain stimulation of the entorhinal area. , 2012 .

[27]  Arne D. Ekstrom,et al.  Specific responses of human hippocampal neurons are associated with better memory , 2015, Proceedings of the National Academy of Sciences.

[28]  Sang Ah Lee,et al.  Electrical Stimulation in Hippocampus and Entorhinal Cortex Impairs Spatial and Temporal Memory , 2018, The Journal of Neuroscience.

[29]  E. Düzel,et al.  Medial temporal theta state before an event predicts episodic encoding success in humans , 2009, Proceedings of the National Academy of Sciences.

[30]  Vishnu Sreekumar,et al.  Signal Complexity of Human Intracranial EEG Tracks Successful Associative-Memory Formation across Individuals , 2018, The Journal of Neuroscience.

[31]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

[32]  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.

[33]  W. Estes Statistical theory of spontaneous recovery and regression. , 1955, Psychological review.

[34]  D Marr,et al.  Simple memory: a theory for archicortex. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[35]  M. Moser,et al.  Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus , 2007, Science.

[36]  Christian F. Doeller,et al.  Mnemonic convergence in the human hippocampus , 2016, Nature Communications.

[37]  Hans-Jochen Heinze,et al.  Richness in Functional Connectivity Depends on the Neuronal Integrity within the Posterior Cingulate Cortex , 2017, Front. Neurosci..

[38]  J. Fermaglich Electric Fields of the Brain: The Neurophysics of EEG , 1982 .