Context Prediction Analysis and Episodic Memory

Events that happen at a particular place and time come to define our episodic memories. Extensive experimental and clinical research illustrate that the hippocampus is central to the processing of episodic memories, and this is in large part due to its analysis of context information according to spatial and temporal references. In this way, hippocampus defines ones expectations for a given context as well as detects errors in predicted contextual features. The detection of context prediction errors is hypothesized to distinguished events into meaningful epochs that come to be recalled as separate episodic memories. The nature of the spatial and temporal context information processed by hippocampus is described, as is a hypothesis that the apparently self-regulatory nature of hippocampal context processing may ultimately be mediated by natural homeostatic operations and plasticity. Context prediction errors by hippocampus are suggested to be valued by the midbrain dopamine system, the output of which is ultimately fed back to hippocampus to update memory-driven context expectations for future events. Thus, multiple network functions (both within and outside hippocampus) combine to result in adaptive episodic memories.

[1]  N. Cohen From Conditioning to Conscious Recollection Memory Systems of the Brain. Oxford Psychology Series, Volume 35. , 2001 .

[2]  S. Wiener,et al.  Position and behavioral modulation of synchronization of hippocampal and accumbens neuronal discharges in freely moving rats , 2000, Hippocampus.

[3]  P. Jonas,et al.  Shunting Inhibition Improves Robustness of Gamma Oscillations in Hippocampal Interneuron Networks by Homogenizing Firing Rates , 2006, Neuron.

[4]  R. C. Honey,et al.  Conditioning and contextual retrieval in hippocampal rats. , 1991 .

[5]  M. Shapiro,et al.  Prospective and Retrospective Memory Coding in the Hippocampus , 2003, Neuron.

[6]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[7]  C. Schreiner,et al.  A synaptic memory trace for cortical receptive field plasticity , 2007, Nature.

[8]  J. Lisman,et al.  Storage, recall, and novelty detection of sequences by the hippocampus: Elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine , 2001, Hippocampus.

[9]  J. O’Keefe,et al.  Geometric determinants of the place fields of hippocampal neurons , 1996, Nature.

[10]  David M. Smith,et al.  Hippocampal and neocortical interactions during context discrimination: Electrophysiological evidence from the rat , 2007, Hippocampus.

[11]  R. Morris,et al.  Dopamine and Memory: Modulation of the Persistence of Memory for Novel Hippocampal NMDA Receptor-Dependent Paired Associates , 2010, The Journal of Neuroscience.

[12]  S. Mizumori,et al.  Context-dependent reorganization of spatial and movement representations by simultaneously recorded hippocampal and striatal neurons during performance of allocentric and egocentric tasks. , 2004, Behavioral neuroscience.

[13]  D. Olton,et al.  Spatial correlates of hippocampal unit activity , 1978, Experimental Neurology.

[14]  G. Turrigiano The Self-Tuning Neuron: Synaptic Scaling of Excitatory Synapses , 2008, Cell.

[15]  E. Save,et al.  Contribution of multiple sensory information to place field stability in hippocampal place cells , 2000, Hippocampus.

[16]  Michael E Hasselmo,et al.  The role of hippocampal regions CA3 and CA1 in matching entorhinal input with retrieval of associations between objects and context: theoretical comment on Lee et al. (2005). , 2005, Behavioral neuroscience.

[17]  J. B. Ranck,et al.  Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. , 1973, Experimental neurology.

[18]  B L McNaughton,et al.  Path Integration and Cognitive Mapping in a Continuous Attractor Neural Network Model , 1997, The Journal of Neuroscience.

[19]  J. Gray,et al.  Précis of The neuropsychology of anxiety: An enquiry into the functions of the septo-hippocampal system , 1982, Behavioral and Brain Sciences.

[20]  Matthijs A. A. van der Meer,et al.  Frontiers in Integrative Neuroscience Integrative Neuroscience Low and High Gamma Oscillations in Rat Ventral Striatum Have Distinct Relationships to Behavior, Reward, and Spiking Activity on a Learned Spatial Decision Task , 2022 .

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

[22]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

[23]  Sheri J Y Mizumori,et al.  Ventral tegmental area disruption selectively affects CA1/CA2 but not CA3 place fields during a differential reward working memory task , 2011, Hippocampus.

[24]  M. Just,et al.  Collaborative Activity between Parietal and Dorso-Lateral Prefrontal Cortex in Dynamic Spatial Working Memory Revealed by fMRI , 2000, NeuroImage.

[25]  B. McNaughton,et al.  Independent Codes for Spatial and Episodic Memory in Hippocampal Neuronal Ensembles , 2005, Science.

[26]  J. Lisman,et al.  The Hippocampal-VTA Loop: Controlling the Entry of Information into Long-Term Memory , 2005, Neuron.

[27]  Brice A. Kuhl,et al.  Resistance to forgetting associated with hippocampus-mediated reactivation during new learning , 2010, Nature Neuroscience.

[28]  Evgueniy V. Lubenov,et al.  Prefrontal Phase Locking to Hippocampal Theta Oscillations , 2005, Neuron.

[29]  K. Jeffery,et al.  A proposed architecture for the neural representation of spatial context , 2004, Neuroscience & Biobehavioral Reviews.

[30]  David M. Smith,et al.  Mnemonic contributions of hippocampal place cells , 2007 .

[31]  M. Gluck,et al.  Context, conditioning, and hippocampal rerepresentation in animal learning. , 1994, Behavioral neuroscience.

[32]  Patricia E. Sharp,et al.  The neural basis of navigation : evidence from single cell recording , 2002 .

[33]  C. Pennartz,et al.  Reward-associated gamma oscillations in ventral striatum are regionally differentiated and modulate local firing activity. , 2010, Journal of neurophysiology.

[34]  R. Nudo Neural bases of recovery after brain injury. , 2011, Journal of Communication Disorders.

[35]  L. Nadel The hippocampus and context revisited. , 2008 .

[36]  A D Redish,et al.  Prediction, sequences and the hippocampus , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  G. Turrigiano Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. , 2012, Cold Spring Harbor perspectives in biology.

[38]  M. Gabriel,et al.  Context-specific multi-site cingulate cortical, limbic thalamic, and hippocampal neuronal activity during concurrent discriminative approach and avoidance training in rabbits , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  S. Mizumori,et al.  Effects of Prefrontal Cortical Inactivation on Neural Activity in the Ventral Tegmental Area , 2013, The Journal of Neuroscience.

[40]  D. Kumaran,et al.  Match–Mismatch Processes Underlie Human Hippocampal Responses to Associative Novelty , 2007, The Journal of Neuroscience.

[41]  S. Mizumori,et al.  Homeostatic Regulation of Memory Systems and Adaptive Decisions , 2013, Hippocampus.

[42]  M. Hasselmo What is the function of hippocampal theta rhythm?—Linking behavioral data to phasic properties of field potential and unit recording data , 2005, Hippocampus.

[43]  M. Gabriel,et al.  Limbic thalamic, cingulate cortical and hippocampal neuronal correlates of discriminative approach learning in rabbits , 1996, Behavioural Brain Research.

[44]  M. Wilson,et al.  Theta Rhythms Coordinate Hippocampal–Prefrontal Interactions in a Spatial Memory Task , 2005, PLoS biology.

[45]  Eve Marder,et al.  Current Compensation in Neuronal Homeostasis , 2003, Neuron.

[46]  Mehdi Khamassi,et al.  Coherent Theta Oscillations and Reorganization of Spike Timing in the Hippocampal- Prefrontal Network upon Learning , 2010, Neuron.

[47]  R. C. Honey,et al.  Conditioning and contextual retrieval in hippocampal rats. , 1991, Behavioral neuroscience.

[48]  Stephen Grossberg,et al.  How Do Spatial Learning and Memory Occur in the Brain? Coordinated Learning of Entorhinal Grid Cells and Hippocampal Place Cells , 2012, Journal of Cognitive Neuroscience.

[49]  Niraj S. Desai,et al.  Activity-dependent scaling of quantal amplitude in neocortical neurons , 1998, Nature.

[50]  M. W. Brown,et al.  Novel spatial arrangements of familiar visual stimuli promote activity in the rat hippocampal formation but not the parahippocampal cortices: a c-fos expression study , 2004, Neuroscience.

[51]  Michael E. Hasselmo,et al.  Neuromodulation, theta rhythm and rat spatial navigation , 2002, Neural Networks.

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

[53]  O. Paulsen,et al.  A model of hippocampal memory encoding and retrieval: GABAergic control of synaptic plasticity , 1998, Trends in Neurosciences.

[54]  S. Mizumori A Context for Hippocampal Place Cells during Learning , 2008 .

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

[56]  Marc W Howard,et al.  Gradual Changes in Hippocampal Activity Support Remembering the Order of Events , 2007, Neuron.

[57]  D. A. Bergstrom,et al.  Multisecond periodicities in basal ganglia firing rates correlate with theta bursts in transcortical and hippocampal EEG. , 2002, Journal of neurophysiology.

[58]  E. Marder,et al.  Variability, compensation and homeostasis in neuron and network function , 2006, Nature Reviews Neuroscience.

[59]  James J Knierim,et al.  Dynamic Interactions between Local Surface Cues, Distal Landmarks, and Intrinsic Circuitry in Hippocampal Place Cells , 2002, The Journal of Neuroscience.

[60]  Sisir Roy,et al.  The ‘prediction imperative’ as the basis for self-awareness , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[61]  Eric A. Zilli,et al.  Hippocampal CA1 spiking during encoding and retrieval: Relation to theta phase , 2007, Neurobiology of Learning and Memory.

[62]  P. Mitra,et al.  Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task , 2007, Proceedings of the National Academy of Sciences.

[63]  T. Prescott,et al.  The ventral basal ganglia, a selection mechanism at the crossroads of space, strategy, and reward. , 2010, Progress in Neurobiology.

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

[65]  David M. Smith,et al.  Learning-Related Development of Context-Specific Neuronal Responses to Places and Events: The Hippocampal Role in Context Processing , 2006, The Journal of Neuroscience.

[66]  H. Eichenbaum,et al.  From Conditioning to Conscious Recollection , 2001 .

[67]  J. O’Keefe,et al.  Hippocampal place units in the freely moving rat: Why they fire where they fire , 1978, Experimental Brain Research.

[68]  Nikolaus R. McFarland,et al.  Striatonigrostriatal Pathways in Primates Form an Ascending Spiral from the Shell to the Dorsolateral Striatum , 2000, The Journal of Neuroscience.

[69]  E Save,et al.  Object exploration and reactions to spatial and nonspatial changes in hooded rats following damage to parietal cortex or hippocampal formation. , 1992, Behavioral neuroscience.

[70]  S. Mizumori,et al.  Parallel processing across neural systems: Implications for a multiple memory system hypothesis , 2004, Neurobiology of Learning and Memory.

[71]  J. Berke,et al.  Fast oscillations in cortical‐striatal networks switch frequency following rewarding events and stimulant drugs , 2009, The European journal of neuroscience.

[72]  Bruce L. McNaughton,et al.  Progressive Transformation of Hippocampal Neuronal Representations in “Morphed” Environments , 2005, Neuron.

[73]  Nigel Foreman,et al.  Exploratory activity and response to a spatial change in rats with hippocampal or posterior parietal cortical lesions , 1992, Behavioural Brain Research.

[74]  J. B. Ranck,et al.  Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. II. Hippocampal slow waves and theta cell firing during bar pressing and other behaviors. , 1973, Experimental neurology.

[75]  M. Bouton,et al.  Contextual and Temporal Modulation of Extinction: Behavioral and Biological Mechanisms , 2006, Biological Psychiatry.

[76]  D. Buonomano,et al.  The neural basis of temporal processing. , 2004, Annual review of neuroscience.

[77]  Eric A. Zilli,et al.  Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior , 2005, Hippocampus.

[78]  R. Oostenveld,et al.  Tactile Spatial Attention Enhances Gamma-Band Activity in Somatosensory Cortex and Reduces Low-Frequency Activity in Parieto-Occipital Areas , 2006, The Journal of Neuroscience.

[79]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[80]  Hippocampus, context, and conditioning. , 1991, Behavioral neuroscience.

[81]  Lila Davachi,et al.  Evidence for area CA1 as a match/mismatch detector: A high‐resolution fMRI study of the human hippocampus , 2012, Hippocampus.

[82]  M. Fanselow,et al.  Modality-specific retrograde amnesia of fear. , 1992, Science.

[83]  K. Duncan,et al.  Memory’s Penumbra: Episodic Memory Decisions Induce Lingering Mnemonic Biases , 2012, Science.

[84]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[85]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[86]  M. Fyhn,et al.  Hippocampal Neurons Responding to First-Time Dislocation of a Target Object , 2002, Neuron.

[87]  H. Eichenbaum,et al.  Critical role of the hippocampus in memory for sequences of events , 2002, Nature Neuroscience.

[88]  J. Knierim,et al.  Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3 , 2004, Nature.

[89]  C. Y. Yim,et al.  Rhythmic delta-frequency activities in the nucleus accumbens of anesthetized and freely moving rats. , 1993, Canadian journal of physiology and pharmacology.

[90]  G. Buzsáki,et al.  A 4 Hz Oscillation Adaptively Synchronizes Prefrontal, VTA, and Hippocampal Activities , 2011, Neuron.

[91]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[92]  Joaquín M. Fuster,et al.  Cortex and Memory: Emergence of a New Paradigm , 2009, Journal of Cognitive Neuroscience.

[93]  R. Muller,et al.  The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[94]  R. O’Reilly,et al.  Conjunctive representations in learning and memory: principles of cortical and hippocampal function. , 2001, Psychological review.

[95]  György Buzsáki,et al.  Cognitive neuroscience: Time, space and memory , 2013, Nature.

[96]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

[97]  Joseph E LeDoux,et al.  Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. , 1992, Behavioral neuroscience.

[98]  R. Hampson,et al.  Sequential dependencies regulate sensory evoked responses of single units in the rat hippocampus , 1987, Brain Research.

[99]  Oxana Eschenko,et al.  Non-commercial Research and Educational Use including without Limitation Use in Instruction at Your Institution, Sending It to Specific Colleagues That You Know, and Providing a Copy to Your Institution's Administrator. All Other Uses, Reproduction and Distribution, including without Limitation Comm , 2022 .

[100]  M. Sabatino,et al.  Striatal and septal influence on hippocampal theta and spikes in the cat , 1985, Neuroscience Letters.

[101]  Greg D. Gale,et al.  Hippocampus and contextual fear conditioning: Recent controversies and advances , 2001, Hippocampus.

[102]  J. Csicsvari,et al.  Mechanisms of Gamma Oscillations in the Hippocampus of the Behaving Rat , 2003, Neuron.

[103]  Kechen Zhang,et al.  Sensory Feedback, Error Correction, and Remapping in a Multiple Oscillator Model of Place-Cell Activity , 2011, Front. Comput. Neurosci..

[104]  D. Shohamy,et al.  Feedback Timing Modulates Brain Systems for Learning in Humans , 2011, The Journal of Neuroscience.

[105]  Bruce L. McNaughton,et al.  Path integration and the neural basis of the 'cognitive map' , 2006, Nature Reviews Neuroscience.

[106]  Jian Li,et al.  Parallel contributions of distinct human memory systems during probabilistic learning , 2011, NeuroImage.

[107]  J. O’Keefe Place units in the hippocampus of the freely moving rat , 1976, Experimental Neurology.

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

[109]  S. Nelson,et al.  Homeostatic plasticity in the developing nervous system , 2004, Nature Reviews Neuroscience.

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

[111]  H. T. Blair,et al.  Putting Fear in Its Place: Remapping of Hippocampal Place Cells during Fear Conditioning , 2004, The Journal of Neuroscience.

[112]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[113]  David M. Smith,et al.  Fornix lesions impair context-related cingulothalamic neuronal patterns and concurrent discrimination learning in rabbits (Oryctolagus cuniculus). , 2004, Behavioral neuroscience.

[114]  A. Arnsten,et al.  Neuromodulation of Thought: Flexibilities and Vulnerabilities in Prefrontal Cortical Network Synapses , 2012, Neuron.

[115]  K M Gothard,et al.  Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[116]  Brian H. Bland,et al.  Basal ganglia–hippocampal interactions support the role of the hippocampal formation in sensorimotor integration , 2004, Experimental Neurology.

[117]  Stephen Grossberg,et al.  How Entorhinal Grid Cells May Learn Multiple Spatial Scales from a Dorsoventral Gradient of Cell Response Rates in a Self-organizing Map , 2012, PLoS Comput. Biol..

[118]  S. Mizumori,et al.  Specific changes in hippocampal spatial codes predict spatial working memory performance , 2006, Behavioural Brain Research.

[119]  David M. Smith,et al.  Hippocampal episode fields develop with learning , 2011, Hippocampus.

[120]  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 .

[121]  D. Turner,et al.  Cellular Links between Neuronal Activity and Energy Homeostasis , 2012, Front. Pharmacol..

[122]  Stefan Leutgeb,et al.  A neural systems analysis of adaptive navigation , 2000, Molecular Neurobiology.

[123]  S. Mizumori,et al.  Age-associated changes in the hippocampal-ventral striatum-ventral tegmental loop that impact learning, prediction, and context discrimination , 2012, Front. Ag. Neurosci..

[124]  C. Elger,et al.  Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling , 2001, Nature Neuroscience.

[125]  J. Knierim,et al.  Hippocampal place cells: Parallel input streams, subregional processing, and implications for episodic memory , 2006, Hippocampus.

[126]  S J Mizumori,et al.  Hippocampal Representational Organization and Spatial Context , 1999, Hippocampus.

[127]  Bryan Kolb,et al.  Structural plasticity associated with exposure to drugs of abuse , 2004, Neuropharmacology.

[128]  H. Eichenbaum,et al.  The global record of memory in hippocampal neuronal activity , 1999, Nature.

[129]  S. Mizumori,et al.  Conjunctive encoding of movement and reward by ventral tegmental area neurons in the freely navigating rodent. , 2010, Behavioral neuroscience.

[130]  H. Eichenbaum,et al.  Correlates of hippocampal complex-spike cell activity in rats performing a nonspatial radial maze task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[131]  S. Mizumori,et al.  Neural systems analysis of decision making during goal-directed navigation , 2012, Progress in Neurobiology.

[132]  H. Eichenbaum,et al.  The Hippocampus, Memory, and Place Cells Is It Spatial Memory or a Memory Space? , 1999, Neuron.

[133]  Joseph E LeDoux,et al.  Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. , 1994, Learning & memory.

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

[135]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[136]  H. Eichenbaum,et al.  Oscillatory Entrainment of Striatal Neurons in Freely Moving Rats , 2004, Neuron.

[137]  G. Turrigiano Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same , 1999, Trends in Neurosciences.

[138]  A. Pérez-Villalba Rhythms of the Brain, G. Buzsáki. Oxford University Press, Madison Avenue, New York (2006), Price: GB £42.00, p. 448, ISBN: 0-19-530106-4 , 2008 .

[139]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[140]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[141]  R. Hirsh The hippocampus and contextual retrieval of information from memory: a theory. , 1974, Behavioral biology.

[142]  G. Glover,et al.  Associative retrieval processes in the human medial temporal lobe: hippocampal retrieval success and CA1 mismatch detection. , 2011, Learning & memory.

[143]  Andrew M. Wikenheiser,et al.  Changes in reward contingency modulate the trial-to-trial variability of hippocampal place cells. , 2011, Journal of neurophysiology.

[144]  Conditioned effects of apomorphine are manifest in regional EEG of rats both in hippocampus and in striatum , 1993, Naunyn-Schmiedeberg's Archives of Pharmacology.

[145]  H. Eichenbaum,et al.  Discordance of spatial representation in ensembles of hippocampal place cells , 1997, Hippocampus.

[146]  Robert Oostenveld,et al.  Localizing human visual gamma-band activity in frequency, time and space , 2006, NeuroImage.

[147]  S. Wiener Spatial, behavioral and sensory correlates of hippocampal CA1 complex spike cell activity: Implications for information processing functions , 1996, Progress in Neurobiology.

[148]  J. Fuster The cognit: a network model of cortical representation. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[149]  H. Mallot,et al.  Inactivation of the rat dorsal striatum impairs performance in spatial tasks and alters hippocampal theta in the freely moving rat , 2005, Behavioural Brain Research.

[150]  Asohan Amarasingham,et al.  Internally Generated Cell Assembly Sequences in the Rat Hippocampus , 2008, Science.

[151]  Ann M Graybiel,et al.  Oscillations of local field potentials in the rat dorsal striatum during spontaneous and instructed behaviors. , 2007, Journal of neurophysiology.

[152]  Andrew M. Poulos,et al.  The neuroscience of mammalian associative learning. , 2005, Annual review of psychology.

[153]  H. Scheich,et al.  Stimulus-related gamma oscillations in primate auditory cortex. , 2002, Journal of neurophysiology.

[154]  J F Disterhoft,et al.  Hippocampal encoding of non‐spatial trace conditioning , 1999, Hippocampus.

[155]  C. H. Vanderwolf,et al.  Hippocampal electrical activity and voluntary movement in the rat. , 1969, Electroencephalography and clinical neurophysiology.

[156]  Stephen Maren Neurobiology of Pavlovian fear conditioning. , 2001, Annual review of neuroscience.

[157]  David M. Smith,et al.  Hippocampal place cells, context, and episodic memory , 2006, Hippocampus.

[158]  Joel E. Brown,et al.  Concordant and discordant coding of spatial location in populations of hippocampal CA1 pyramidal cells. , 2002, Journal of neurophysiology.

[159]  O. Vinogradova Expression, control, and probable functional significance of the neuronal theta-rhythm , 1995, Progress in Neurobiology.