How the Hippocampus Represents Memories: Making Sense of Memory Allocation Studies

In recent years there has been a wealth of studies investigating how memories are allocated in the hippocampus. Some of those studies showed that it is possible to manipulate the identity of neurons recruited to represent a given memory without affecting the memory's behavioral expression. Those findings raised questions about how the hippocampus represents memories, with some researchers arguing that hippocampal neurons do not represent fixed stimuli. Herein, an alternative hypothesis is argued. Neurons in high‐order brain regions can be tuned to multiple dimensions, forming complex, abstract representations. It is argued that such complex receptive fields allow those neurons to show some flexibility in their responses while still representing relatively fixed sets of stimuli. Moreover, it is pointed out that changes induced by artificial manipulation of cell assemblies are not completely redundant—the observed behavioral redundancy does not imply cognitive redundancy, as different, but similar, memories may induce the same behavior.

[1]  E. Tolman Cognitive maps in rats and men. , 1948, Psychological review.

[2]  G. Lynch,et al.  Heterosynaptic depression: a postsynaptic correlate of long-term potentiation , 1977, Nature.

[3]  Terrence J. Sejnowski,et al.  Network model of shape-from-shading: neural function arises from both receptive and projective fields , 1988, Nature.

[4]  Richard Granger,et al.  A cortical model of winner-take-all competition via lateral inhibition , 1992, Neural Networks.

[5]  B. McNaughton,et al.  Independence of Firing Correlates of Anatomically Proximate Hippocampal Pyramidal Cells , 2001, The Journal of Neuroscience.

[6]  N. Kasthuri,et al.  Long-term dendritic spine stability in the adult cortex , 2002, Nature.

[7]  Terence D Sanger,et al.  Neural population codes , 2003, Current Opinion in Neurobiology.

[8]  S. Royer,et al.  Conservation of total synaptic weight through balanced synaptic depression and potentiation , 2003, Nature.

[9]  Kathryn J Jeffery,et al.  Heterogeneous Modulation of Place Cell Firing by Changes in Context , 2003, The Journal of Neuroscience.

[10]  K. Jeffery,et al.  Preserved performance in a hippocampal‐dependent spatial task despite complete place cell remapping , 2003, Hippocampus.

[11]  E. Kandel,et al.  Increased Attention to Spatial Context Increases Both Place Field Stability and Spatial Memory , 2004, Neuron.

[12]  B. McNaughton,et al.  Local Sensory Cues and Place Cell Directionality: Additional Evidence of Prospective Coding in the Hippocampus , 2004, The Journal of Neuroscience.

[13]  W. Gan,et al.  Development of Long-Term Dendritic Spine Stability in Diverse Regions of Cerebral Cortex , 2005, Neuron.

[14]  Bruno Poucet,et al.  Goal-Related Activity in Hippocampal Place Cells , 2007, The Journal of Neuroscience.

[15]  Kathryn J Jeffery,et al.  Integration of the sensory inputs to place cells: What, where, why, and how? , 2007, Hippocampus.

[16]  John F. Guzowski,et al.  Neuronal Competition and Selection During Memory Formation , 2006, Science.

[17]  Joseph E LeDoux The amygdala , 2007, Current Biology.

[18]  Alcino J. Silva,et al.  CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala , 2009, Nature Neuroscience.

[19]  M. López de Armentia,et al.  Enhanced CREB-dependent gene expression increases the excitability of neurons in the basal amygdala and primes the consolidation of contextual and cued fear memory. , 2009, Learning & memory.

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

[21]  G. Kreiman,et al.  Measuring sparseness in the brain: comment on Bowers (2009). , 2010, Psychological review.

[22]  R. Muller,et al.  Attention-Like Modulation of Hippocampus Place Cell Discharge , 2010, The Journal of Neuroscience.

[23]  M. Bergami,et al.  A fight for survival: The challenges faced by a newborn neuron integrating in the adult hippocampus , 2012, Developmental neurobiology.

[24]  Rosa H. M. Chan,et al.  A Nonlinear Model for Hippocampal Cognitive Prosthesis: Memory Facilitation by Hippocampal Ensemble Stimulation , 2012, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[25]  Robert E. Hampson,et al.  Donor/recipient enhancement of memory in rat hippocampus , 2013, Front. Syst. Neurosci..

[26]  Edvard I. Moser,et al.  Grid Cells and Neural Coding in High-End Cortices , 2013, Neuron.

[27]  Lacey J. Kitch,et al.  Long-term dynamics of CA1 hippocampal place codes , 2013, Nature Neuroscience.

[28]  Fred H. Gage,et al.  Molecular layer perforant path-associated cells contribute to feed-forward inhibition in the adult dentate gyrus , 2013, Proceedings of the National Academy of Sciences.

[29]  Denise J. Cai,et al.  Synaptic tagging during memory allocation , 2014, Nature Reviews Neuroscience.

[30]  Christian Tetzlaff,et al.  The formation of multi-synaptic connections by the interaction of synaptic and structural plasticity and their functional consequences , 2014, BMC Neuroscience.

[31]  Haim Sompolinsky,et al.  Computational neuroscience: beyond the local circuit , 2014, Current Opinion in Neurobiology.

[32]  Brian J. Wiltgen,et al.  Cortical Representations Are Reinstated by the Hippocampus during Memory Retrieval , 2014, Neuron.

[33]  Paul W. Frankland,et al.  Neurons Are Recruited to a Memory Trace Based on Relative Neuronal Excitability Immediately before Training , 2014, Neuron.

[34]  Neil Burgess,et al.  What do grid cells contribute to place cell firing? , 2014, Trends in Neurosciences.

[35]  Yaniv Ziv,et al.  Hippocampal ensemble dynamics timestamp events in long-term memory , 2015, eLife.

[36]  J. Macke,et al.  Neural population coding: combining insights from microscopic and mass signals , 2015, Trends in Cognitive Sciences.

[37]  Caswell Barry,et al.  Grid cell symmetry is shaped by environmental geometry , 2015, Nature.

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

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

[40]  Susumu Tonegawa,et al.  Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons , 2015, Nature Neuroscience.

[41]  Mark J. Schnitzer,et al.  Impermanence of dendritic spines in live adult CA1 hippocampus , 2015, Nature.

[42]  Stephen Maren,et al.  Prefrontal-Hippocampal Interactions in Memory and Emotion , 2015, Front. Syst. Neurosci..

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

[44]  J. Knierim The hippocampus , 2015, Current Biology.

[45]  Andrea Klug,et al.  The Hippocampus Book , 2016 .

[46]  A. Holtmaat,et al.  Functional and structural underpinnings of neuronal assembly formation in learning , 2016, Nature Neuroscience.

[47]  Thomas J. Wills,et al.  Absence of Visual Input Results in the Disruption of Grid Cell Firing in the Mouse , 2016, Current Biology.

[48]  J. Gonçalves,et al.  Adult Neurogenesis in the Hippocampus: From Stem Cells to Behavior , 2016, Cell.

[49]  P. Frankland,et al.  Neuronal Allocation to a Hippocampal Engram , 2016, Neuropsychopharmacology.

[50]  M. Nitabach,et al.  Multisensory integration in C. elegans , 2017, Current Opinion in Neurobiology.

[51]  Daniel A. Dombeck,et al.  Increased Prevalence of Calcium Transients across the Dendritic Arbor during Place Field Formation , 2017, Neuron.

[52]  György Buzsáki,et al.  Space and time in the brain , 2017, Science.

[53]  Mehrdad Jazayeri,et al.  Navigating the Neural Space in Search of the Neural Code , 2017, Neuron.

[54]  Sébastien Royer,et al.  Place cells are more strongly tied to landmarks in deep than in superficial CA1 , 2017, Nature Communications.

[55]  P. Latham,et al.  Cracking the Neural Code for Sensory Perception by Combining Statistics, Intervention, and Behavior , 2017, Neuron.

[56]  L. Nadel,et al.  Viewpoints: how the hippocampus contributes to memory, navigation and cognition , 2017, Nature Neuroscience.

[57]  Dmitriy Aronov,et al.  Mapping of a non-spatial dimension by the hippocampal/entorhinal circuit , 2017, Nature.

[58]  M. A. MacIver,et al.  Neuroscience Needs Behavior: Correcting a Reductionist Bias , 2017, Neuron.

[59]  W. Gerstner,et al.  Hebbian plasticity requires compensatory processes on multiple timescales , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[60]  Konrad Paul Kording,et al.  Could a Neuroscientist Understand a Microprocessor? , 2016, bioRxiv.

[61]  Thiago F. A. França Plasticity and redundancy in the integration of adult born neurons in the hippocampus , 2018, Neurobiology of Learning and Memory.

[62]  Christof Koch,et al.  A large-scale, standardized physiological survey reveals higher order coding throughout the mouse visual cortex , 2018, bioRxiv.

[63]  Thomas J McHugh,et al.  The hippocampal engram maps experience but not place , 2018, Science.

[64]  Milenna Tamara van Dijk,et al.  On How the Dentate Gyrus Contributes to Memory Discrimination , 2017, Neuron.

[65]  C. Desplan,et al.  Large-Scale CRISPR-Mediated Somatic Mutagenesis Identifies a Signaling Pathway that Guides Retinal Development , 2018, Neuron.

[66]  Tsuyoshi Murata,et al.  {m , 1934, ACML.