Dynamics of memory engrams

In this update article, we focus on "memory engrams", which are traces of long-term memory in the brain, and emphasizes that they are not static but dynamic. We first introduce the major findings in neuroscience and psychology reporting that memory engrams are sometimes diffuse and unstable, indicating that they are dynamically modified processes of consolidation and reconsolidation. Second, we introduce and discuss the concepts of cell assembly and engram cell, the former has been investigated by psychological experiments and behavioral electrophysiology and the latter is defined by recent combination of activity-dependent cell labelling with optogenetics to show causal relationships between cell population activity and behavioral changes. Third, we discuss the similarities and differences between the cell assembly and engram cell concepts to reveal the dynamics of memory engrams. We also discuss the advantages and problems of live-cell imaging, which has recently been developed to visualize multineuronal activities. The last section suggests the experimental strategy and background assumptions for future research of memory engrams. The former encourages recording of cell assemblies from different brain regions during memory consolidation-reconsolidation processes, while the latter emphasizes the multipotentiality of neurons and regions that contribute to dynamics of memory engrams in the working brain.

[1]  K. Svoboda,et al.  Photon Upmanship: Why Multiphoton Imaging Is More than a Gimmick , 1997, Neuron.

[2]  Brendon O. Watson,et al.  Spike inference from calcium imaging using sequential Monte Carlo methods. , 2009, Biophysical journal.

[3]  S. Tonegawa,et al.  Memory Engram Cells Have Come of Age , 2015, Neuron.

[4]  J. Arthur Woodward,et al.  Individual differences in verbal memory performance: A test of alternative information-processing models , 1982 .

[5]  K. Deisseroth,et al.  Optogenetic stimulation of a hippocampal engram activates fear memory recall , 2012, Nature.

[6]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[7]  E. John Multipotentiality: A Statistical Theory of Brain Function—Evidence and Implications , 1980 .

[8]  L. Squire Memory and Brain , 1987 .

[9]  G. Buzsáki,et al.  Millisecond Timescale Synchrony among Hippocampal Neurons , 2014, The Journal of Neuroscience.

[10]  Michele Pignatelli,et al.  Engram cells retain memory under retrograde amnesia , 2015, Science.

[11]  Yasser Roudi,et al.  Multi-neuronal activity and functional connectivity in cell assemblies , 2015, Current Opinion in Neurobiology.

[12]  M K Habib,et al.  Dynamics of neuronal firing correlation: modulation of "effective connectivity". , 1989, Journal of neurophysiology.

[13]  Richard F. Thompson,et al.  Localization of a memory trace in the mammalian brain. , 1993, Science.

[14]  Jun Liu,et al.  512-Channel and 13-Region Simultaneous Recordings Coupled with Optogenetic Manipulation in Freely Behaving Mice , 2016, Front. Syst. Neurosci..

[15]  Takashi Kitamura,et al.  The role of engram cells in the systems consolidation of memory , 2018, Nature Reviews Neuroscience.

[16]  Elad Eban,et al.  A cortical–hippocampal–cortical loop of information processing during memory consolidation , 2016, Nature Neuroscience.

[17]  Jeansok J Kim,et al.  Multiple brain-memory systems: the whole does not equal the sum of its parts , 2001, Trends in Neurosciences.

[18]  Christine Grienberger,et al.  Imaging Calcium in Neurons , 2012, Neuron.

[19]  G. Palm,et al.  Cell assemblies, coherence, and corticohippocampal interplay , 1993, Hippocampus.

[20]  Dan D. Stettler,et al.  Driving Opposing Behaviors with Ensembles of Piriform Neurons , 2011, Cell.

[21]  György Buzsáki,et al.  Neural Syntax: Cell Assemblies, Synapsembles, and Readers , 2010, Neuron.

[22]  E R John,et al.  Switchboard versus statistical theories of learning and memory. , 1972, Science.

[23]  Vítor Lopes-dos-Santos,et al.  Detecting cell assemblies in large neuronal populations , 2013, Journal of Neuroscience Methods.

[24]  Y. Sakurai,et al.  Dynamic Synchrony of Firing in the Monkey Prefrontal Cortex during Working-Memory Tasks , 2006, The Journal of Neuroscience.

[25]  Takashi Kitamura,et al.  Engrams and circuits crucial for systems consolidation of a memory , 2017, Science.

[26]  Dheeraj S. Roy,et al.  Memory retrieval by activating engram cells in mouse models of early Alzheimer’s disease , 2016, Nature.

[27]  N. Matsuo,et al.  Irreplaceability of Neuronal Ensembles after Memory Allocation. , 2015, Cell reports.

[28]  Y. Sakurai,et al.  Hippocampal and neocortical cell assemblies encode memory processes for different types of stimuli in the rat , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  K. Lashley Studies of Cerebral Function in Learning. II. The Effects of Long Continued Practice upon Cerebral L , 1921 .

[30]  John B. Carroll,et al.  Individual differences in cognitive abilities. , 1979, Annual review of psychology.

[31]  Yuma Osako,et al.  Multiple Approaches to the Investigation of Cell Assembly in Memory Research—Present and Future , 2018, Front. Syst. Neurosci..

[32]  H. Markowitsch,et al.  Hypotheses on mnemonic information processing by the brain. , 1985, The International journal of neuroscience.

[33]  Pablo E. Jercog,et al.  Neural ensemble dynamics underlying a long-term associative memory , 2017, Nature.

[34]  H. Eichenbaum The Cognitive Neuroscience of Memory , 2002 .

[35]  Kaoru Inokuchi,et al.  Artificial association of pre-stored information to generate a qualitatively new memory. , 2015, Cell reports.

[36]  Li Lu,et al.  Coordination of entorhinal–hippocampal ensemble activity during associative learning , 2014, Nature.

[37]  H. Eichenbaum Barlow versus Hebb: When is it time to abandon the notion of feature detectors and adopt the cell assembly as the unit of cognition? , 2017, Neuroscience Letters.

[38]  Lin Tian,et al.  Functional imaging of hippocampal place cells at cellular resolution during virtual navigation , 2010, Nature Neuroscience.

[39]  E F Loftus,et al.  Creating false memories. , 1997, Scientific American.

[40]  Yoshio Sakurai,et al.  Sub-Millisecond Firing Synchrony of Closely Neighboring Pyramidal Neurons in Hippocampal CA1 of Rats During Delayed Non-Matching to Sample Task , 2009, Front. Neural Circuits.

[41]  K. Svoboda,et al.  Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice , 2008, Nature.

[42]  H. Eichenbaum,et al.  Consolidation and Reconsolidation: Two Lives of Memories? , 2011, Neuron.