Precision, binding, and the hippocampus: Precisely what are we talking about?

Endel Tulving's proposal that episodic memory is distinct from other memory systems like semantic memory remains an extremely influential idea in cognitive neuroscience research. As originally suggested by Tulving, episodic memory involves three key components that differentiate it from all other memory systems: spatiotemporal binding, mental time travel, and autonoetic consciousness. Here, we focus on the idea of spatiotemporal binding in episodic memory and, in particular, how consideration of the precision of spatiotemporal context helps expand our understanding of episodic memory. Precision also helps shed light on another key issue in cognitive neuroscience, the role of the hippocampus outside of episodic memory in perception, attention, and working memory. By considering precision alongside item-context bindings, we attempt to shed new light on both the nature of how we represent context and what roles the hippocampus plays in episodic memory and beyond.

[1]  G. Buzsáki,et al.  Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex , 2008, Nature Neuroscience.

[2]  Morgan D. Barense,et al.  The human medial temporal lobe processes online representations of complex objects , 2007, Neuropsychologia.

[3]  E. Tulving,et al.  Toward a theory of episodic memory: the frontal lobes and autonoetic consciousness. , 1997, Psychological bulletin.

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

[5]  E. Tulving Memory and consciousness. , 1985 .

[6]  Charan Ranganath,et al.  Effects of Unilateral Prefrontal Lesions on Familiarity, Recollection, and Source Memory , 2005, The Journal of Neuroscience.

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

[8]  S. Corkin Lasting Consequences of Bilateral Medial Temporal Lobectomy: Clinical Course and Experimental Findings in H.M. , 1984 .

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

[10]  C. Koch,et al.  Decoding visual inputs from multiple neurons in the human temporal lobe. , 2007, Journal of neurophysiology.

[11]  M. Jones-Gotman,et al.  Memory Deficits after Resection from Left or Right Anterior Temporal Lobe in Humans: A Meta‐Analytic Review , 2002, Epilepsia.

[12]  C. Stark,et al.  Pattern separation in the hippocampus , 2011, Trends in Neurosciences.

[13]  Lazar Fleysher,et al.  Macro-connectomics and microstructure predict dynamic plasticity patterns in the non-human primate brain , 2018, eLife.

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

[15]  Catalin V. Buhusi,et al.  What makes us tick? Functional and neural mechanisms of interval timing , 2005, Nature Reviews Neuroscience.

[16]  Andy C. H. Lee,et al.  Going beyond LTM in the MTL: A synthesis of neuropsychological and neuroimaging findings on the role of the medial temporal lobe in memory and perception , 2010, Neuropsychologia.

[17]  G. Buzsáki,et al.  Memory, navigation and theta rhythm in the hippocampal-entorhinal system , 2013, Nature Neuroscience.

[18]  M. Mishkin,et al.  Developmental amnesia associated with early hypoxic-ischaemic injury. , 2000, Brain : a journal of neurology.

[19]  Dwight J. Kravitz,et al.  The ventral visual pathway: an expanded neural framework for the processing of object quality , 2013, Trends in Cognitive Sciences.

[20]  Melina R. Uncapher,et al.  Episodic Encoding Is More than the Sum of Its Parts: An fMRI Investigation of Multifeatural Contextual Encoding , 2006, Neuron.

[21]  A. Hupbach,et al.  Reconsolidation of episodic memories: a subtle reminder triggers integration of new information. , 2007, Learning & memory.

[22]  Armin Brandt,et al.  Neural Activity in Human Hippocampal Formation Reveals the Spatial Context of Retrieved Memories , 2013, Science.

[23]  C. Koch,et al.  Category-specific visual responses of single neurons in the human medial temporal lobe , 2000, Nature Neuroscience.

[24]  S. Shipp The brain circuitry of attention , 2004, Trends in Cognitive Sciences.

[25]  Neal J. Cohen,et al.  Observing Degradation of Visual Representations over Short Intervals When Medial Temporal Lobe Is Damaged , 2011, Journal of Cognitive Neuroscience.

[26]  E Valenstein,et al.  Retrosplenial amnesia. , 1987, Brain : a journal of neurology.

[27]  Alexander D. Jacob,et al.  Dissociable contributions of thalamic nuclei to recognition memory: novel evidence from a case of medial dorsal thalamic damage , 2018, Learning & memory.

[28]  Daoyun Ji,et al.  Activities of visual cortical and hippocampal neurons co-fluctuate in freely moving rats during spatial behavior , 2015, eLife.

[29]  J. Lisman,et al.  Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding. , 2000, Journal of neurophysiology.

[30]  David E. Warren,et al.  Medial Temporal Lobe Damage Impairs Representation of Simple Stimuli , 2010, Front. Hum. Neurosci..

[31]  Maciej M. Jankowski,et al.  Dynamics of place, boundary and object encoding in rat anterior claustrum , 2015, Front. Behav. Neurosci..

[32]  C. Butler,et al.  Network-wide abnormalities explain memory variability in hippocampal amnesia , 2019, bioRxiv.

[33]  Roger C. Schank,et al.  SCRIPTS, PLANS, GOALS, AND UNDERSTANDING , 1988 .

[34]  W. Levy A computational approach to hippocampal function , 1989 .

[35]  A. Ekstrom,et al.  Close but no cigar: Spatial precision deficits following medial temporal lobe lesions provide novel insight into theoretical models of navigation and memory , 2018, Hippocampus.

[36]  Nicole M. Long,et al.  Recall dynamics reveal the retrieval of emotional context , 2015, Psychonomic bulletin & review.

[37]  Charan Ranganath,et al.  Prefrontal Cortex and Long-Term Memory Encoding: An Integrative Review of Findings from Neuropsychology and Neuroimaging , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[38]  Arne D. Ekstrom,et al.  Multiple interacting brain areas underlie successful spatiotemporal memory retrieval in humans , 2014, Scientific Reports.

[39]  R T Knight,et al.  Recollection and familiarity deficits in amnesia: convergence of remember-know, process dissociation, and receiver operating characteristic data. , 1998, Neuropsychology.

[40]  Michael D. Rugg,et al.  Decoding the content of recollection within the core recollection network and beyond , 2017, Cortex.

[41]  Ramona O Hopkins,et al.  Item memory, source memory, and the medial temporal lobe: concordant findings from fMRI and memory-impaired patients. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[42]  L. Nadel,et al.  Context and conditioning: A place for space , 1980 .

[43]  Colleen M. Parks,et al.  The hippocampus is particularly important for building associations across stimulus domains , 2017, Neuropsychologia.

[44]  Jeffrey M. Zacks,et al.  Event Segmentation , 2007, Current directions in psychological science.

[45]  William H Warren,et al.  Non-Euclidean navigation , 2019, Journal of Experimental Biology.

[46]  Andy C. H. Lee,et al.  Intact Memory for Irrelevant Information Impairs Perception in Amnesia , 2012, Neuron.

[47]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[48]  R. Henson,et al.  The neural basis of episodic memory: evidence from functional neuroimaging. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[49]  H. Eichenbaum,et al.  Hippocampal Neurons Encode Information about Different Types of Memory Episodes Occurring in the Same Location , 2000, Neuron.

[50]  Felicia Y. Ng,et al.  Linking pattern completion in the hippocampus to predictive coding in visual cortex , 2016, Nature Neuroscience.

[51]  Arne D. Ekstrom,et al.  Frequency–specific network connectivity increases underlie accurate spatiotemporal memory retrieval , 2013, Nature Neuroscience.

[52]  A. Yonelinas The hippocampus supports high-resolution binding in the service of perception, working memory and long-term memory , 2013, Behavioural Brain Research.

[53]  The role of reminding in long-term memory for temporal order , 2007, Memory & cognition.

[54]  Neal J Cohen,et al.  Hiding in plain view: Lesions of the medial temporal lobe impair online representation , 2012, Hippocampus.

[55]  Lars Nyberg,et al.  Hemispheric asymmetries of memory: the HERA model revisited , 2003, Trends in Cognitive Sciences.

[56]  Seth J. Ramus,et al.  Severity of memory impairment in monkeys as a function of locus and extent of damage within the medial temporal lobe memory system , 1994, Hippocampus.

[57]  Arne D. Ekstrom,et al.  Cellular networks underlying human spatial navigation , 2003, Nature.

[58]  Arne D. Ekstrom,et al.  A contextual binding theory of episodic memory: systems consolidation reconsidered , 2019, Nature Reviews Neuroscience.

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

[60]  Erik A. Wing,et al.  Hippocampal Contributions to the Large‐Scale Episodic Memory Network Predict Vivid Visual Memories , 2017, Cerebral cortex.

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

[62]  B. McNaughton,et al.  Hippocampal synaptic enhancement and information storage within a distributed memory system , 1987, Trends in Neurosciences.

[63]  H. Eichenbaum,et al.  Hippocampus as a memory map: Synaptic plasticity and memory encoding by hippocampal neurons , 1999, Hippocampus.

[64]  Rosemary A. Cowell,et al.  A Roadmap for Understanding Memory: Decomposing Cognitive Processes into Operations and Representations , 2019, eNeuro.

[65]  I. Fried,et al.  Internally Generated Reactivation of Single Neurons in Human Hippocampus During Free Recall , 2008, Science.

[66]  L R Squire,et al.  Intact perceptual memory in the absence of conscious memory. , 1997, Behavioral neuroscience.

[67]  K. Lehnertz,et al.  Differential Involvement of Left Temporolateral and Temporomesial Structures in Verbal Declarative Learning and Memory: Evidence from Temporal Lobe Epilepsy , 1997, Brain and Cognition.

[68]  B L McNaughton,et al.  Dynamics of the hippocampal ensemble code for space. , 1993, Science.

[69]  Ingrid R. Olson,et al.  Dissociation Between Memory Accuracy and Memory Confidence Following Bilateral Parietal Lesions , 2009, Cerebral cortex.

[70]  Ingrid R. Olson,et al.  Working Memory for Conjunctions Relies on the Medial Temporal Lobe , 2006, The Journal of Neuroscience.

[71]  Anthony Randal McIntosh,et al.  Transperceptual Encoding and Retrieval Processes in Memory: A PET Study of Visual and Haptic Objects , 2001, NeuroImage.

[72]  E. Tulving,et al.  Hippocampal PET activations of memory encoding and retrieval: The HIPER model , 1998, Hippocampus.

[73]  C. Koch,et al.  Invariant visual representation by single neurons in the human brain , 2005, Nature.

[74]  Andy C. H. Lee,et al.  It does not look odd to me: Perceptual impairments and eye movements in amnesic patients with medial temporal lobe damage , 2013, Neuropsychologia.

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

[76]  C. Ranganath,et al.  Two cortical systems for memory-guided behaviour , 2012, Nature Reviews Neuroscience.

[77]  L. Davachi,et al.  Hippocampal contributions to episodic encoding: insights from relational and item-based learning. , 2002, Journal of neurophysiology.

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

[79]  Sevan K Harootonian,et al.  Grid coding, spatial representation, and navigation: Should we assume an isomorphism? , 2019, Hippocampus.

[80]  Morris Moscovitch,et al.  The spatial scaffold: The effects of spatial context on memory for events. , 2016, Journal of experimental psychology. Learning, memory, and cognition.

[81]  Hongkeun Kim,et al.  Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies , 2011, NeuroImage.

[82]  M. Corballis,et al.  The evolution of foresight: What is mental time travel, and is it unique to humans? , 2007, The Behavioral and brain sciences.

[83]  Megan H. Papesh,et al.  Sparse and distributed coding of episodic memory in neurons of the human hippocampus , 2014, Proceedings of the National Academy of Sciences.

[84]  L. Squire,et al.  Recognition memory and familiarity judgments in severe amnesia: no evidence for a contribution of repetition priming. , 2000, Behavioral neuroscience.

[85]  R. Church,et al.  Hippocampus, time, and memory--a retrospective analysis. , 2013, Behavioral neuroscience.

[86]  Franziska R. Richter,et al.  Distinct neural mechanisms underlie the success, precision, and vividness of episodic memory , 2016, eLife.

[87]  Samuel Wiebe,et al.  Neuropsychological outcomes after epilepsy surgery: Systematic review and pooled estimates , 2011, Epilepsia.

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

[89]  M. Peterson Object Recognition Processes Can and Do Operate Before Figure–Ground Organization , 1994 .

[90]  Benjamin J. Kraus,et al.  Hippocampal “Time Cells”: Time versus Path Integration , 2013, Neuron.

[91]  Joshua D Koen,et al.  Visual short‐term memory for high resolution associations is impaired in patients with medial temporal lobe damage , 2017, Hippocampus.

[92]  D. Amaral,et al.  Human amnesia and the medial temporal lobe illuminated by neuropsychological and neurohistological findings for patient E.P. , 2013, Proceedings of the National Academy of Sciences.

[93]  D. Amaral,et al.  Three Cases of Enduring Memory Impairment after Bilateral Damage Limited to the Hippocampal Formation , 1996, The Journal of Neuroscience.

[94]  B. Gibson,et al.  Must Figure-Ground Organization Precede Object Recognition? An Assumption in Peril , 1994 .

[95]  Arne D. Ekstrom,et al.  Interacting networks of brain regions underlie human spatial navigation: a review and novel synthesis of the literature. , 2017, Journal of neurophysiology.

[96]  Richard N. Henson,et al.  The Hippocampal Film Editor: Sensitivity and Specificity to Event Boundaries in Continuous Experience , 2018, The Journal of Neuroscience.

[97]  W. Friedman Memory for the time of past events. , 1993 .

[98]  Bruce L. McNaughton,et al.  Sparse orthogonal population representation of spatial context in the retrosplenial cortex , 2017, Nature Communications.

[99]  B. Milner,et al.  Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M.☆ , 1968 .

[100]  E. Tulving Episodic memory: from mind to brain. , 2002, Annual review of psychology.

[101]  E. Tulving,et al.  PET studies of encoding and retrieval: The HERA model , 1996, Psychonomic bulletin & review.

[102]  Arne D. Ekstrom,et al.  Memory and Networks: Network-Based Approaches to Understanding the Neural Basis of Human Episodic Memory , 2016 .

[103]  Arne D. Ekstrom,et al.  Space, time, and episodic memory: The hippocampus is all over the cognitive map , 2018, Hippocampus.

[104]  James L. Keidel,et al.  Reinstatement of memory representations for lifelike events over the course of a week , 2017, Scientific Reports.

[105]  Maureen Ritchey,et al.  Cortico-hippocampal network connections support the multidimensional quality of episodic memory , 2019, bioRxiv.

[106]  W. Ma,et al.  Changing concepts of working memory , 2014, Nature Neuroscience.

[107]  Andrew P. Yonelinas,et al.  Detecting Changes in Scenes: The Hippocampus Is Critical for Strength-Based Perception , 2013, Neuron.

[108]  Arne D. Ekstrom,et al.  The Spectro-Contextual Encoding and Retrieval Theory of Episodic Memory , 2014, Front. Hum. Neurosci..

[109]  Tracy H. Wang,et al.  Recollection-Related Increases in Functional Connectivity Predict Individual Differences in Memory Accuracy , 2015, The Journal of Neuroscience.

[110]  Rachel A. Diana,et al.  Imaging recollection and familiarity in the medial temporal lobe: a three-component model , 2007, Trends in Cognitive Sciences.

[111]  Jon S. Simons,et al.  Specifying a Causal Role for Angular Gyrus in Autobiographical Memory , 2018, The Journal of Neuroscience.

[112]  Peter Gärdenfors,et al.  Navigating cognition: Spatial codes for human thinking , 2018, Science.

[113]  Arne D. Ekstrom,et al.  Impairments in precision, rather than spatial strategy, characterize performance on the virtual Morris Water Maze: A case study , 2016, Neuropsychologia.

[114]  Dagmar Zeithamova,et al.  Hippocampal and Ventral Medial Prefrontal Activation during Retrieval-Mediated Learning Supports Novel Inference , 2012, Neuron.

[115]  Adam N Mamelak,et al.  Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task , 2002, Behavioural Brain Research.

[116]  M. Gazzaniga,et al.  Understanding complexity in the human brain , 2011, Trends in Cognitive Sciences.

[117]  Dwight J Kravitz,et al.  Visual working memory directly alters perception , 2019, Nature Human Behaviour.

[118]  Arne D. Ekstrom,et al.  Flexible network community organization during the encoding and retrieval of spatiotemporal episodic memories , 2019, Network Neuroscience.

[119]  Arne D. Ekstrom,et al.  Human spatial navigation: representations across dimensions and scales , 2017, Current Opinion in Behavioral Sciences.

[120]  M. Wilson,et al.  Coordinated memory replay in the visual cortex and hippocampus during sleep , 2007, Nature Neuroscience.

[121]  Jason P. Mitchell,et al.  Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[122]  David E. Warren,et al.  Hippocampal Amnesia Impairs All Manner of Relational Memory , 2008, Frontiers in human neuroscience.

[123]  Alan Baddeley,et al.  Double Dissociations: Not Magic, but Still Useful , 2003, Cortex.

[124]  A. Zalesky,et al.  Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection , 2012, Proceedings of the National Academy of Sciences.

[125]  E. Plante,et al.  Memory and executive function in older adults: relationships with temporal and prefrontal gray matter volumes and white matter hyperintensities , 2004, Neuropsychologia.

[126]  Arne D Ekstrom,et al.  Temporal encoding strategies result in boosts to final free recall performance comparable to spatial ones , 2018, Memory & cognition.

[127]  Stanley Finger,et al.  The Monakow concept of diaschisis: origins and perspectives. , 2004, Archives of neurology.

[128]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[129]  Marcia K. Johnson,et al.  Memory and Reality , 2022 .