Cortical cell ensemble control of past experience-dependent memory updating

When processing current sensory inputs, animals refer to related past experiences. Current information is then incorporated into the related neural network to update previously stored memories. However, the neuronal mechanism underlying the impact of memories of prior experiences on current learning is not well understood. Here, we found that a cellular ensemble in the posterior parietal cortex (PPC) that is activated during past experience mediates an interaction between past and current information to update memory through a PPC-anterior cingulate cortex circuit in mice. Moreover, optogenetic silencing of the PPC ensemble immediately after retrieval dissociated the interaction without affecting individual memories stored in the hippocampus and amygdala. Thus, a specific subpopulation of PPC cells represents past information and instructs downstream brain regions to update previous memories.

[1]  H. Hirai,et al.  Efficient whole brain transduction by systemic infusion of minimally purified AAV-PHP.eB , 2020, Journal of Neuroscience Methods.

[2]  J. Koo,et al.  Posterior parietal cortex mediates fear renewal in a novel context , 2020, Molecular Brain.

[3]  Susumu Tonegawa,et al.  Memory engrams: Recalling the past and imagining the future , 2020, Science.

[4]  Melissa Hebscher,et al.  Rapid Cortical Plasticity Supports Long-Term Memory Formation , 2019, Trends in Cognitive Sciences.

[5]  M. Erb,et al.  Fast track to the neocortex: A memory engram in the posterior parietal cortex , 2018, Science.

[6]  Maureen Ritchey,et al.  Neural reactivation in parietal cortex enhances memory for episodically linked information , 2018, Proceedings of the National Academy of Sciences.

[7]  Kaoru Inokuchi,et al.  Behavioral, cellular, and synaptic tagging frameworks , 2018, Neurobiology of Learning and Memory.

[8]  Mark D. Morrissey,et al.  The role of engram cells in the systems consolidation of memory , 2018, Nature Reviews Neuroscience.

[9]  K. Inokuchi,et al.  Synapse-specific representation of the identity of overlapping memory engrams , 2018, Science.

[10]  Demba E. Ba,et al.  Corticoamygdala Transfer of Socially Derived Information Gates Observational Learning , 2018, Cell.

[11]  M. Maravall,et al.  Cortical Lifelogging: The Posterior Parietal Cortex as Sensory History Buffer , 2018, Neuron.

[12]  R. G. Parsons,et al.  Behavioral and neural mechanisms by which prior experience impacts subsequent learning , 2017, Neurobiology of Learning and Memory.

[13]  Charles D. Kopec,et al.  Posterior parietal cortex represents sensory history and mediates its effects on behaviour , 2017, Nature.

[14]  Asaf Gilboa,et al.  Neurobiology of Schemas and Schema-Mediated Memory , 2017, Trends in Cognitive Sciences.

[15]  K. Nader,et al.  An Update on Memory Reconsolidation Updating , 2017, Trends in Cognitive Sciences.

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

[17]  Maurizio Corbetta,et al.  The contribution of the human posterior parietal cortex to episodic memory , 2017, Nature Reviews Neuroscience.

[18]  Akinobu Suzuki,et al.  Overlapping memory trace indispensable for linking, but not recalling, individual memories , 2017, Science.

[19]  K. Doya,et al.  Neural substrate of dynamic Bayesian inference in the cerebral cortex , 2016, Nature Neuroscience.

[20]  Akinobu Suzuki,et al.  Cellular tagging as a neural network mechanism for behavioural tagging , 2016, Nature Communications.

[21]  Paul W. Frankland,et al.  Competition between engrams influences fear memory formation and recall , 2016, Science.

[22]  Alcino J. Silva,et al.  A shared neural ensemble links distinct contextual memories encoded close in time , 2016, Nature.

[23]  Tobias Sommer,et al.  The Emergence of Knowledge and How it Supports the Memory for Novel Related Information , 2016, Cerebral cortex.

[24]  S. Lissek,et al.  Learning models of PTSD: Theoretical accounts and psychobiological evidence. , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[25]  O. Masseck,et al.  Optogenetic Destabilization of the Memory Trace in CA1: Insights into Reconsolidation and Retrieval Processes , 2015, Cerebral cortex.

[26]  C. Honey,et al.  Hierarchical process memory: memory as an integral component of information processing , 2015, Trends in Cognitive Sciences.

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

[28]  Margaret L. Schlichting,et al.  Memory integration: neural mechanisms and implications for behavior , 2015, Current Opinion in Behavioral Sciences.

[29]  S. Tonegawa,et al.  Creating a False Memory in the Hippocampus , 2013, Science.

[30]  N. Canteras,et al.  The many paths to fear , 2012, Nature Reviews Neuroscience.

[31]  I. Izquierdo,et al.  Posterior parietal cortex and long-term memory: some data from laboratory animals , 2012, Front. Integr. Neurosci..

[32]  Satoshi Kida,et al.  Hippocampal function is not required for the precision of remote place memory , 2012, Molecular Brain.

[33]  Dorothy Tse,et al.  Schema-Dependent Gene Activation and Memory Encoding in Neocortex , 2011, Science.

[34]  Roberto Cabeza,et al.  Annals of the New York Academy of Sciences the Porous Boundaries between Explicit and Implicit Memory: Behavioral and Neural Evidence , 2022 .

[35]  T. Egner,et al.  Emotional processing in anterior cingulate and medial prefrontal cortex , 2011, Trends in Cognitive Sciences.

[36]  Sven Bestmann,et al.  New approaches to the study of human brain networks underlying spatial attention and related processes , 2010, Experimental Brain Research.

[37]  Y. Rossetti,et al.  Optic ataxia and the function of the dorsal stream: Contributions to perception and action , 2009, Neuropsychologia.

[38]  Bruno Poucet,et al.  Role of the parietal cortex in long-term representation of spatial information in the rat , 2009, Neurobiology of Learning and Memory.

[39]  E. Kuramoto,et al.  High-level transgene expression in neurons by lentivirus with Tet-Off system , 2009, Neuroscience Research.

[40]  Roberto Cabeza,et al.  Parietal Lobe and Episodic Memory: Bilateral Damage Causes Impaired Free Recall of Autobiographical Memory , 2007, The Journal of Neuroscience.

[41]  Dorothy Tse,et al.  References and Notes Supporting Online Material Materials and Methods Figs. S1 to S5 Tables S1 to S3 Electron Impact (ei) Mass Spectra Chemical Ionization (ci) Mass Spectra References Schemas and Memory Consolidation Research Articles Research Articles Research Articles Research Articles , 2022 .

[42]  Parashkev Nachev,et al.  Space and the parietal cortex , 2007, Trends in Cognitive Sciences.

[43]  P. Frankland,et al.  The organization of recent and remote memories , 2005, Nature Reviews Neuroscience.

[44]  Bruce L. McNaughton,et al.  Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles , 1999, Nature Neuroscience.

[45]  M. Fanselow.  Factors governing one-trial contextual conditioning , 1990 .

[46]  A. Ehlers,et al.  Understanding and Treating Unwanted Trauma Memories in Posttraumatic Stress Disorder , 2010, Zeitschrift fur Psychologie.