A Role for the Longitudinal Axis of the Hippocampus in Multiscale Representations of Large and Complex Spatial Environments and Mnemonic Hierarchies

The hippocampus is involved in spatial navigation and memory in rodents and humans. Anatomically, the hippocampus extends along a longitudinal axis that shows a combination of graded and specific interconnections with neocortical and subcortical brain areas. Functionally, place cells are found all along the longitudinal axis and exhibit gradients of properties including an increasing dorsal-to-ventral place field size. We propose a view of hippocampal function in which fine-dorsal to coarse-ventral overlapping representations collaborate to form a multi-level representation of spatial and episodic memory that is dominant during navigation in large and complex environments or when encoding complex memories. This view is supported by the fact that the effects of ventral hippocampal damage are generally only found in larger laboratoryscale environments, and by the finding that human virtual navigation studies associate ventral hippocampal involvement with increased environmental complexity. Other mechanisms such as the ability of place cells to exhibit multiple fields and their ability to scale their fields with changes in environment size may be utilized when forming large-scale cognitive maps. Coarse-grained ventral representations may overlap with and provide multi-modal global contexts to finer-grained intermediate and dorsal representations, a mechanism that may support mnemonic hierarchies of autobiographical memory in humans.

[1]  C. Grady,et al.  Event-related fMRI studies of episodic encoding and retrieval: Meta-analyses using activation likelihood estimation , 2009, Neuropsychologia.

[2]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[3]  Yaakov Stern,et al.  Functional connectivity of the posterior hippocampus is more dominant as we age , 2014, Cognitive neuroscience.

[4]  Adam Johnson,et al.  Neural Ensembles in CA3 Transiently Encode Paths Forward of the Animal at a Decision Point , 2007, The Journal of Neuroscience.

[5]  Thomas J. Wills,et al.  The development of the hippocampal neural representation of space , 2014, Current Opinion in Neurobiology.

[6]  Roddy M. Grieves,et al.  Place cells on a maze encode routes rather than destinations , 2016, eLife.

[7]  Pablo Billeke,et al.  A Role for the Insular Cortex in Long-Term Memory for Context-Evoked Drug Craving in Rats , 2012, Neuropsychopharmacology.

[8]  G Buzsáki,et al.  Spatial organization of physiological activity in the hippocampal region: relevance to memory formation. , 1990, Progress in brain research.

[9]  Susan Rotzinger,et al.  Cholecystokinin receptor subtypes: role in the modulation of anxiety-related and reward-related behaviours in animal models. , 2003, Journal of psychiatry & neuroscience : JPN.

[10]  Gong-Wu Wang,et al.  Reversible disconnection of the hippocampal-prelimbic cortical circuit impairs spatial learning but not passive avoidance learning in rats , 2008, Neurobiology of Learning and Memory.

[11]  K. Jeffery,et al.  Grid Cells Form a Global Representation of Connected Environments , 2015, Current Biology.

[12]  Christian F. Doeller,et al.  Memory hierarchies map onto the hippocampal long axis in humans , 2015, Nature Neuroscience.

[13]  Jason B. Mattingley,et al.  Dissociable Representations of Environmental Size and Complexity in the Human Hippocampus , 2013, The Journal of Neuroscience.

[14]  Yasuo Kawaguchi,et al.  Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin , 1987, Brain Research.

[15]  J. Feldon,et al.  Dissociation of function between the dorsal and the ventral hippocampus in spatial learning abilities of the rat: a within‐subject, within‐task comparison of reference and working spatial memory , 2004, The European journal of neuroscience.

[16]  Florin Dolcos,et al.  Reduced hippocampal and amygdala activity predicts memory distortions for trauma reminders in combat-related PTSD. , 2011, Journal of psychiatric research.

[17]  G. Quirk,et al.  Dissociable Roles of Prelimbic and Infralimbic Cortices, Ventral Hippocampus, and Basolateral Amygdala in the Expression and Extinction of Conditioned Fear , 2011, Neuropsychopharmacology.

[18]  Daniel L. Schacter,et al.  Spatial Representation in the Entorhinal Cortex , 2004 .

[19]  Edvard I Moser,et al.  Development of the Spatial Representation System in the Rat , 2010, Science.

[20]  B. McNaughton,et al.  The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats , 1983, Experimental Brain Research.

[21]  T. Ono,et al.  Task-dependent representations in rat hippocampal place neurons. , 1997, Journal of neurophysiology.

[22]  B. Poucet Spatial cognitive maps in animals: new hypotheses on their structure and neural mechanisms. , 1993, Psychological review.

[23]  S. Ciocchi,et al.  Selective information routing by ventral hippocampal CA1 projection neurons , 2015, Science.

[24]  Ila R Fiete,et al.  What Grid Cells Convey about Rat Location , 2008, The Journal of Neuroscience.

[25]  Jean-Marc Fellous,et al.  Hippocampal Anatomy Supports the Use of Context in Object Recognition: A Computational Model , 2013, Comput. Intell. Neurosci..

[26]  T. Bliss,et al.  The Hippocampus Book , 2006 .

[27]  Ashley N. Linder,et al.  The Spatial Periodicity of Grid Cells Is Not Sustained During Reduced Theta Oscillations , 2011, Science.

[28]  P. Andersen,et al.  Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  D. Amaral,et al.  Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat , 1990, The Journal of comparative neurology.

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

[31]  B. McNaughton,et al.  The Ventral Striatum in Off-Line Processing: Ensemble Reactivation during Sleep and Modulation by Hippocampal Ripples , 2004, The Journal of Neuroscience.

[32]  E. Asprodini,et al.  Differential expression of NMDA and AMPA receptor subunits in rat dorsal and ventral hippocampus , 2006, Neuroscience.

[33]  Arthur W. Toga,et al.  Genomic–anatomic evidence for distinct functional domains in hippocampal field CA1 , 2009, Proceedings of the National Academy of Sciences.

[34]  M. Fyhn,et al.  Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex , 2008, Hippocampus.

[35]  C. Barnes,et al.  Spatial Representation along the Proximodistal Axis of CA1 , 2010, Neuron.

[36]  K. Jeffery,et al.  Experience-dependent rescaling of entorhinal grids , 2007, Nature Neuroscience.

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

[38]  M Tsodyks,et al.  Attractor neural network models of spatial maps in hippocampus , 1999, Hippocampus.

[39]  Nobuaki Tamamaki,et al.  Disposition of the slab‐like modules formed by axon branches originating from single CA1 pyramidal neurons in the rat hippocampus , 1990, The Journal of comparative neurology.

[40]  May-Britt Moser,et al.  The entorhinal grid map is discretized , 2012, Nature.

[41]  D. Thomsen,et al.  Autobiographical Periods: A Review and Central Components of a Theory , 2015 .

[42]  T. Valiante,et al.  Functional and effective hippocampal-neocortical connectivity during construction and elaboration of autobiographical memory retrieval. , 2015, Cerebral cortex.

[43]  M. Moser,et al.  Reduced fear expression after lesions of the ventral hippocampus , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Morris Moscovitch,et al.  A Hippocampal Marker of Recollection Memory Ability among Healthy Young Adults: Contributions of Posterior and Anterior Segments , 2011, Neuron.

[45]  J. Rawlins,et al.  Ventral hippocampal lesions affect anxiety but not spatial learning , 2003, Behavioural Brain Research.

[46]  Kara L. Agster,et al.  Functional neuroanatomy of the parahippocampal region: The lateral and medial entorhinal areas , 2007, Hippocampus.

[47]  S. J. Martin,et al.  Double dissociation between the contributions of the septal and temporal hippocampus to spatial learning: The role of prior experience , 2014, Hippocampus.

[48]  J. Knierim,et al.  Major Dissociation Between Medial and Lateral Entorhinal Input to Dorsal Hippocampus , 2005, Science.

[49]  James N. Davis,et al.  Differential distribution of locus coeruleus projections to the hippocampal formation: anatomical and biochemical evidence , 1985, Brain Research.

[50]  D. Amaral,et al.  Intrinsic connections of the macaque monkey hippocampal formation: II. CA3 connections , 2009, The Journal of comparative neurology.

[51]  J. Knierim,et al.  Attractor dynamics of spatially correlated neural activity in the limbic system. , 2012, Annual review of neuroscience.

[52]  Olivier Potvin,et al.  Performance on spatial working memory tasks after dorsal or ventral hippocampal lesions and adjacent damage to the subiculum. , 2006, Behavioral neuroscience.

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

[54]  M. Witter,et al.  Cingulate cortex projections to the parahippocampal region and hippocampal formation in the rat , 2007, Hippocampus.

[55]  Suzanne Wood,et al.  Reduced posterior hippocampal volume in posttraumatic stress disorder. , 2008, The Journal of clinical psychiatry.

[56]  G. Einevoll,et al.  From grid cells to place cells: A mathematical model , 2006, Hippocampus.

[57]  J. Rawlins,et al.  Regional dissociations within the hippocampus—memory and anxiety , 2004, Neuroscience & Biobehavioral Reviews.

[58]  J. O’Neill,et al.  The reorganization and reactivation of hippocampal maps predict spatial memory performance , 2010, Nature Neuroscience.

[59]  Alexandra T. Keinath,et al.  Precise spatial coding is preserved along the longitudinal hippocampal axis , 2014, Hippocampus.

[60]  Eleanor A Maguire,et al.  Exploring anterograde associative memory in London taxi drivers , 2012, Neuroreport.

[61]  R. Chambers,et al.  Regulation of affect by the lateral septum: implications for neuropsychiatry , 2004, Brain Research Reviews.

[62]  B Poucet,et al.  Place cells in the ventral hippocampus of rats , 1994, Neuroreport.

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

[64]  T. L. Holdstock,et al.  Dissociation of function within the hippocampus. , 1972, Physiology & behavior.

[65]  Mark G. Packard,et al.  Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat , 1994, Brain Research Bulletin.

[66]  A. Weindl,et al.  Immunohistochemistry of vasopressin, oxytocin and neurophysin in the hypothalamus and extrahypothalamic regions of the human and primate brain. , 1981, Acta histochemica. Supplementband.

[67]  E. Maguire,et al.  What does the retrosplenial cortex do? , 2009, Nature Reviews Neuroscience.

[68]  Anil Nanda,et al.  Julius Caesar Arantius (Giulio Cesare Aranzi, 1530-1589) and the hippocampus of the human brain: history behind the discovery. , 2015, Journal of neurosurgery.

[69]  M. Moser,et al.  Functional differentiation in the hippocampus , 1998, Hippocampus.

[70]  D. Nitz Tracking Route Progression in the Posterior Parietal Cortex , 2006, Neuron.

[71]  J. Rawlins,et al.  Dissociating context and space within the hippocampus: effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning. , 1999, Behavioral neuroscience.

[72]  Nachum Ulanovsky,et al.  Vectorial representation of spatial goals in the hippocampus of bats , 2017, Science.

[73]  David Eilam,et al.  Traveling Companions Add Complexity and Hinder Performance in the Spatial Behavior of Rats , 2016, PloS one.

[74]  N Burgess,et al.  Place cells, navigational accuracy, and the human hippocampus. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[75]  Kechen Zhang,et al.  Megamap: flexible representation of a large space embedded with nonspatial information by a hippocampal attractor network. , 2016, Journal of neurophysiology.

[76]  Mieke Verfaellie,et al.  The life stories of adults with amnesia: Insights into the contribution of the medial temporal lobes to the organization of autobiographical memory , 2017, Neuropsychologia.

[77]  Bruce L McNaughton,et al.  Apparent Encoding of Sequential Context in Rat Medial Prefrontal Cortex Is Accounted for by Behavioral Variability , 2006, The Journal of Neuroscience.

[78]  Tamás F Freund,et al.  Interneuron Diversity series: Rhythm and mood in perisomatic inhibition , 2003, Trends in Neurosciences.

[79]  Raymond P. Kesner,et al.  Dissociations across the dorsal–ventral axis of CA3 and CA1 for encoding and retrieval of contextual and auditory-cued fear , 2008, Neurobiology of Learning and Memory.

[80]  Larry R Squire,et al.  Spatial memory, recognition memory, and the hippocampus. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[81]  Randolf Menzel,et al.  Navigation outside of the box: what the lab can learn from the field and what the field can learn from the lab , 2014, Movement ecology.

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

[83]  R. Morris,et al.  Locus coeruleus and dopaminergic consolidation of everyday memory , 2016, Nature.

[84]  Laurenz Wiskott,et al.  Spatial representations of place cells in darkness are supported by path integration and border information , 2014, Front. Behav. Neurosci..

[85]  E. Maguire,et al.  London taxi drivers and bus drivers: A structural MRI and neuropsychological analysis , 2006, Hippocampus.

[86]  René Hen,et al.  Serotonin receptor expression along the dorsal–ventral axis of mouse hippocampus , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[87]  R. Kesner,et al.  Encoding versus retrieval of spatial memory: Double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus , 2004, Hippocampus.

[88]  Jean-Marc Fellous,et al.  Contextual reminders fail to trigger memory reconsolidation in aged rats and aged humans , 2015, Neurobiology of Learning and Memory.

[89]  L. Acsády,et al.  Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus , 1996, Neuroscience.

[90]  B. J. Clark,et al.  Disruption of the head direction cell network impairs the parahippocampal grid cell signal , 2015, Science.

[91]  Nachum Ulanovsky,et al.  Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation , 2015, Nature Reviews Neuroscience.

[92]  Tobias Meilinger,et al.  Local and Global Reference Frames for Environmental Spaces , 2014, Quarterly journal of experimental psychology.

[93]  Hallvard Røe Evensmoen,et al.  Long-axis specialization of the human hippocampus , 2013, Trends in Cognitive Sciences.

[94]  M. Moser,et al.  Optogenetic Dissection of Entorhinal-Hippocampal Functional Connectivity , 2013, Science.

[95]  György Buzsáki,et al.  Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance , 2007, Proceedings of the National Academy of Sciences.

[96]  T. Freund,et al.  Interneurons Containing Calretinin Are Specialized to Control Other Interneurons in the Rat Hippocampus , 1996, The Journal of Neuroscience.

[97]  Simon Kemp,et al.  Themes, events, and episodes in autobiographical memory , 2003, Memory & cognition.

[98]  H. T. Blair,et al.  Hippocampal Place Cells Acquire Location-Specific Responses to the Conditioned Stimulus during Auditory Fear Conditioning , 2003, Neuron.

[99]  D. R. Euston,et al.  The Role of Medial Prefrontal Cortex in Memory and Decision Making , 2012, Neuron.

[100]  Jean-Marc Fellous,et al.  A new rat-compatible robotic framework for spatial navigation behavioral experiments , 2018, Journal of Neuroscience Methods.

[101]  Daniel L. Schacter,et al.  The neural correlates of gist-based true and false recognition , 2012, NeuroImage.

[102]  Roy G. Thompson,et al.  Differential distribution of norepinephrine and serotonin along the dorsal-ventral axis of the hippocampal formation , 1980, Brain Research Bulletin.

[103]  S. Molden,et al.  Accumulation of Hippocampal Place Fields at the Goal Location in an Annular Watermaze Task , 2001, The Journal of Neuroscience.

[104]  Brad E. Pfeiffer,et al.  Hippocampal place cell sequences depict future paths to remembered goals , 2013, Nature.

[105]  Stephen L. Cowen,et al.  Organization of hippocampal cell assemblies based on theta phase precession , 2006, Hippocampus.

[106]  R. Morris,et al.  Spatial learning with a minislab in the dorsal hippocampus. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[107]  Takaichi Fukuda,et al.  Distribution of nonprincipal neurons in the rat hippocampus, with special reference to their dorsoventral difference , 1997, Brain Research.

[108]  E. Lein,et al.  Functional organization of the hippocampal longitudinal axis , 2014, Nature Reviews Neuroscience.

[109]  Thomas Wolbers,et al.  Challenges for identifying the neural mechanisms that support spatial navigation: the impact of spatial scale , 2014, Front. Hum. Neurosci..

[110]  E. Maguire,et al.  Acquiring “the Knowledge” of London's Layout Drives Structural Brain Changes , 2011, Current Biology.

[111]  Daniel Johnston,et al.  Differential expression of HCN subunits alters voltage-dependent gating of h-channels in CA1 pyramidal neurons from dorsal and ventral hippocampus. , 2013, Journal of neurophysiology.

[112]  Maxim Bazhenov,et al.  Hippocampal CA1 Ripples as Inhibitory Transients , 2016, PLoS Comput. Biol..

[113]  C. Verney,et al.  Mesolimbic dopaminergic neurons innervating the hippocampal formation in the rat: a combined retrograde tracing and immunohistochemical study , 1994, Brain Research.

[114]  M. Moser,et al.  Distributed Encoding and Retrieval of Spatial Memory in the Hippocampus , 1998, The Journal of Neuroscience.

[115]  J. O’Keefe,et al.  Grid cell firing patterns signal environmental novelty by expansion , 2012, Proceedings of the National Academy of Sciences.

[116]  D. Amaral,et al.  Entorhinal cortex of the rat: Topographic organization of the cells of origin of the perforant path projection to the dentate gyrus , 1998, The Journal of comparative neurology.

[117]  Janina Ferbinteanu,et al.  Both dorsal and ventral hippocampus contribute to spatial learning in Long–Evans rats , 2003, Neuroscience Letters.

[118]  D. Shohamy,et al.  Integrating Memories in the Human Brain: Hippocampal-Midbrain Encoding of Overlapping Events , 2008, Neuron.

[119]  J. Rawlins,et al.  Dissociation of function within the hippocampus: effects of dorsal, ventral and complete excitotoxic hippocampal lesions on spatial navigation , 2004, Neuroscience.

[120]  L. Swanson,et al.  Connections of the rat lateral septal complex 1 Published on the World Wide Web on 2 June 1997. 1 , 1997, Brain Research Reviews.

[121]  P. Somogyi,et al.  Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations , 2008, Science.

[122]  T. Kosaka,et al.  Patterns of expression of neuropeptides in GABAergic nonprincipal neurons in the mouse hippocampus: Quantitative analysis with optical disector , 2003, The Journal of comparative neurology.

[123]  Jarle Ladstein,et al.  From details to large scale: The representation of environmental positions follows a granularity gradient along the human hippocampal and entorhinal anterior–posterior axis , 2015, Hippocampus.

[124]  G. Quirk,et al.  Neurons in medial prefrontal cortex signal memory for fear extinction , 2002, Nature.

[125]  T. Hafting,et al.  Finite Scale of Spatial Representation in the Hippocampus , 2008, Science.

[126]  Dave G. Mumby,et al.  Incidental (unreinforced) and reinforced spatial learning in rats with ventral and dorsal lesions of the hippocampus , 2009, Behavioural Brain Research.

[127]  György Buzsáki,et al.  Hippocampal CA3 pyramidal cells selectively innervate aspiny interneurons , 2006, The European journal of neuroscience.

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

[129]  Hong-wei Dong,et al.  Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? , 2010, Neuron.

[130]  Eleanor A. Maguire,et al.  Navigational expertise may compromise anterograde associative memory , 2009, Neuropsychologia.

[131]  David N. Lyttle,et al.  Spatial scale and place field stability in a grid‐to‐place cell model of the dorsoventral axis of the hippocampus , 2013, Hippocampus.

[132]  M. Witter,et al.  Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoagglutinin , 1987, Neuroscience.

[133]  Lynn Nadel,et al.  Spatial Cognition and the Hippocampus: The Anterior–Posterior Axis , 2013, Journal of Cognitive Neuroscience.

[134]  M. Witter Intrinsic and extrinsic wiring of CA3: indications for connectional heterogeneity. , 2007, Learning & memory.

[135]  Tobias Meilinger,et al.  The Network of Reference Frames Theory: A Synthesis of Graphs and Cognitive Maps , 2008, Spatial Cognition.

[136]  R. Muller,et al.  The firing of hippocampal place cells in the dark depends on the rat's recent experience , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[138]  Jean-Christophe Cassel,et al.  The ventral hippocampus is necessary for expressing a spatial memory , 2011, Brain Structure and Function.

[139]  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.

[140]  Attila I Gulyás,et al.  Convergence of excitatory and inhibitory inputs onto CCK‐containing basket cells in the CA1 area of the rat hippocampus , 2004, The European journal of neuroscience.

[141]  D. Amaral,et al.  Entorhinal cortex of the rat: Organization of intrinsic connections , 1998, The Journal of comparative neurology.

[142]  Sanghoon Han,et al.  The Inferior Parietal Lobule and Recognition Memory: Expectancy Violation or Successful Retrieval? , 2010, The Journal of Neuroscience.

[143]  M. Segal,et al.  Striking Variations in Corticosteroid Modulation of Long-Term Potentiation along the Septotemporal Axis of the Hippocampus , 2007, The Journal of Neuroscience.

[144]  Roddy M. Grieves,et al.  Lesions of the Head Direction Cell System Increase Hippocampal Place Field Repetition , 2017, Current Biology.

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

[146]  Costas Papatheodoropoulos,et al.  Differential expression of γ‐aminobutyric acid‐A receptor subunits in rat dorsal and ventral hippocampus , 2005, Journal of neuroscience research.

[147]  Michael E. Hasselmo,et al.  Time Constants of h Current in Layer II Stellate Cells Differ along the Dorsal to Ventral Axis of Medial Entorhinal Cortex , 2008, The Journal of Neuroscience.

[148]  T. Robbins,et al.  Putting a spin on the dorsal–ventral divide of the striatum , 2004, Trends in Neurosciences.

[149]  Fred H. Gage,et al.  Endogenous norepinephrine and serotonin within the hippocampal formation during the development and recovery from septal hyperractivity , 1978, Pharmacology Biochemistry and Behavior.

[150]  G. A. Ascoli,et al.  Non-homogeneous stereological properties of the rat hippocampus from high-resolution 3D serial reconstruction of thin histological sections , 2012, Neuroscience.

[151]  Stephen Maren,et al.  Hippocampus and Pavlovian fear conditioning in rats: muscimol infusions into the ventral, but not dorsal, hippocampus impair the acquisition of conditional freezing to an auditory conditional stimulus. , 2004, Behavioral neuroscience.

[152]  A. V Olypher,et al.  Quantifying location-specific information in the discharge of rat hippocampal place cells , 2003, Journal of Neuroscience Methods.

[153]  K. D. Taylor Range of Movement and Activity of Common Rats (Rattus norvegicus) on Agricultural Land , 1978 .

[154]  L. Swanson,et al.  Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex , 2007, Brain Research Reviews.

[155]  Daniel Johnston,et al.  Intrinsic excitability of CA1 pyramidal neurones from the rat dorsal and ventral hippocampus , 2012, The Journal of physiology.

[156]  D. Amaral,et al.  Organization of CA1 projections to the subiculum: A PHA‐L analysis in the rat , 1991, Hippocampus.

[157]  R. J. McDonald,et al.  Dorsal/ventral hippocampus, fornix, and conditioned place preference , 2001, Hippocampus.

[158]  E. Maguire,et al.  The Well-Worn Route and the Path Less Traveled Distinct Neural Bases of Route Following and Wayfinding in Humans , 2003, Neuron.

[159]  Nicola Maggio,et al.  Unique regulation of long term potentiation in the rat ventral hippocampus , 2007, Hippocampus.

[160]  L. Descarries,et al.  Quantified distribution of the noradrenaline innervation in the hippocampus of adult rat , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[161]  Martin Llofriu,et al.  Goal-oriented robot navigation learning using a multi-scale space representation , 2015, Neural Networks.

[162]  Raymond P. Kesner,et al.  Prefrontal and hippocampal contributions to encoding and retrieval of spatial memory , 2010, Neurobiology of Learning and Memory.

[163]  William W Lytton,et al.  Unmasking the CA1 Ensemble Place Code by Exposures to Small and Large Environments: More Place Cells and Multiple, Irregularly Arranged, and Expanded Place Fields in the Larger Space , 2008, The Journal of Neuroscience.

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

[165]  György Buzsáki,et al.  What does gamma coherence tell us about inter-regional neural communication? , 2015, Nature Neuroscience.

[166]  T. Otto,et al.  Differential contributions of dorsal vs. ventral hippocampus to auditory trace fear conditioning , 2007, Neurobiology of Learning and Memory.

[167]  Nikolaus Weiskopf,et al.  Detecting Representations of Recent and Remote Autobiographical Memories in vmPFC and Hippocampus , 2012, The Journal of Neuroscience.

[168]  Devdeep Aikath,et al.  Role of Self-Generated Odor Cues in Contextual Representation , 2014, Hippocampus.

[169]  A. Ylinen,et al.  Reciprocal Connections between the Amygdala and the Hippocampal Formation, Perirhinal Cortex, and Postrhinal Cortex in Rat: A Review , 2000, Annals of the New York Academy of Sciences.

[170]  M. Moser,et al.  Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus , 2007, Science.

[171]  H. Nielsen,et al.  Transcriptome differentiation along the dorso–ventral axis in laser-captured microdissected rat hippocampal granular cell layer , 2010, Neuroscience.

[172]  B. McNaughton,et al.  Hippocampus Leads Ventral Striatum in Replay of Place-Reward Information , 2009, PLoS biology.

[173]  Natalie L. M. Cappaert,et al.  The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network , 2009, Nature Reviews Neuroscience.

[174]  G. Buzsáki,et al.  Distinct Representations and Theta Dynamics in Dorsal and Ventral Hippocampus , 2010, The Journal of Neuroscience.

[175]  Costas Papatheodoropoulos,et al.  Weaker synaptic inhibition in CA1 region of ventral compared to dorsal rat hippocampal slices , 2002, Brain Research.

[176]  Jean-Marc Fellous,et al.  Dorsoventral and Proximodistal Hippocampal Processing Account for the Influences of Sleep and Context on Memory (Re)consolidation: A Connectionist Model , 2017, Comput. Intell. Neurosci..

[177]  Fred H. Gage,et al.  Reinnervation of the partially deafferented hippocampus by compensatory collateral sprouting from spared cholinergic and noradrenergic afferents , 1983, Brain Research.

[178]  Sreedharan Sajikumar,et al.  Dopamine D1/D5 receptor signaling regulates synaptic cooperation and competition in hippocampal CA1 pyramidal neurons via sustained ERK1/2 activation , 2015, Hippocampus.

[179]  Antoine Lutti,et al.  Investigating the functions of subregions within anterior hippocampus , 2015, Cortex.

[180]  María Busch,et al.  Movements of Norway rats (Rattus norvegicus) in two poultry farms, Exaltación de la Cruz, Buenos Aires, Argentina , 2008 .

[181]  B. McNaughton,et al.  Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[182]  Ping He,et al.  AMELIORATIVE EFFECTS OF HISTAMINE ON SPATIAL MEMORY DEFICITS INDUCED BY SCOPOLAMINE INFUSION INTO BILATERAL DORSAL OR VENTRAL HIPPOCAMPUS AS EVALUATED BY THE RADIAL ARM MAZE TASK , 2009, Clinical and experimental pharmacology & physiology.

[183]  Andrew P Maurer,et al.  The influence of objects on place field expression and size in distal hippocampal CA1 , 2011, Hippocampus.

[184]  B. McNaughton,et al.  Offline reactivation of experience-dependent neuronal firing patterns in the rat ventral tegmental area. , 2015, Journal of neurophysiology.

[185]  E. Kandel,et al.  Dopamine release from the locus coeruleus to the dorsal hippocampus promotes spatial learning and memory , 2016, Proceedings of the National Academy of Sciences.

[186]  T. Hafting,et al.  Microstructure of a spatial map in the entorhinal cortex , 2005, Nature.

[187]  Martin Stemmler,et al.  Optimal Population Codes for Space: Grid Cells Outperform Place Cells , 2012, Neural Computation.

[188]  B. Staresina,et al.  Mind the Gap: Binding Experiences across Space and Time in the Human Hippocampus , 2009, Neuron.

[189]  D. Kumaran,et al.  Double Dissociation between Hippocampal and Parahippocampal Responses to Object–Background Context and Scene Novelty , 2011, The Journal of Neuroscience.

[190]  A. Treves,et al.  Hippocampal remapping and grid realignment in entorhinal cortex , 2007, Nature.

[191]  T. Freund,et al.  Differences between Somatic and Dendritic Inhibition in the Hippocampus , 1996, Neuron.

[192]  Albert K. Lee,et al.  Large environments reveal the statistical structure governing hippocampal representations , 2014, Science.

[193]  J. Rawlins,et al.  Double dissociation of function within the hippocampus: spatial memory and hyponeophagia. , 2002, Behavioral neuroscience.

[194]  A. Fenton,et al.  Ensemble Place Codes in Hippocampus: CA1, CA3, and Dentate Gyrus Place Cells Have Multiple Place Fields in Large Environments , 2011, PloS one.