Prefrontal–hippocampal interactions for spatial navigation

Animals have the ability to navigate to a desired location by making use of information about environmental landmarks and their own movements. While decades of neuroscience research have identified neurons in the hippocampus and parahippocampal structures that represent an animal's position in space, it is still largely unclear how an animal can choose the next movement direction to reach a desired goal. As the goal destination is typically located somewhere outside of the range of sensory perception, the animal is required to rely on the internal metric of space to estimate the direction and distance of the destination to plan a next action. Therefore, the hippocampal spatial map should interact with action-planning systems in other cortical regions. In accordance with this idea, several recent studies have indicated the importance of functional interactions between the hippocampus and the prefrontal cortex for goal-directed navigation. In this paper, I will review these studies and discuss how an animal can estimate its future positions correspond to a next movement. Investigation of the navigation problem may further provide general insights into internal models of the brain for action planning.

[1]  Morris Moscovitch,et al.  Remote spatial memory in an amnesic person with extensive bilateral hippocampal lesions , 2000, Nature Neuroscience.

[2]  E. Save,et al.  Spatial Firing of Hippocampal Place Cells in Blind Rats , 1998, The Journal of Neuroscience.

[3]  R. Morris Spatial Localization Does Not Require the Presence of Local Cues , 1981 .

[4]  T. Jay,et al.  Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris‐leucoagglutinin , 1991, The Journal of comparative neurology.

[5]  L. Frank,et al.  Awake Hippocampal Sharp-Wave Ripples Support Spatial Memory , 2012, Science.

[6]  Alexander Mathis,et al.  Connecting multiple spatial scales to decode the population activity of grid cells , 2015, Science Advances.

[7]  Timothy E. J. Behrens,et al.  Organizing conceptual knowledge in humans with a gridlike code , 2016, Science.

[8]  E. Bertram,et al.  Thalamic excitation of hippocampal CA1 neurons: a comparison with the effects of CA3 stimulation , 1999, Neuroscience.

[9]  Wei Xu,et al.  A Neural Circuit for Memory Specificity and Generalization , 2013, Science.

[10]  R. Vertes,et al.  The reuniens and rhomboid nuclei: Neuroanatomy, electrophysiological characteristics and behavioral implications , 2013, Progress in Neurobiology.

[11]  L. Nadel,et al.  Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex , 1998, Neuropsychologia.

[12]  Anoopum S. Gupta,et al.  Segmentation of spatial experience by hippocampal theta sequences , 2012, Nature Neuroscience.

[13]  M. Moser,et al.  Spatial Memory in the Rat Requires the Dorsolateral Band of the Entorhinal Cortex , 2005, Neuron.

[14]  Emilio Kropff,et al.  Place cells, grid cells, and the brain's spatial representation system. , 2008, Annual review of neuroscience.

[15]  R. M. Siegel,et al.  Encoding of spatial location by posterior parietal neurons. , 1985, Science.

[16]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[17]  T. Bonhoeffer,et al.  Grid cells and cortical representation , 2014, Nature Reviews Neuroscience.

[18]  B Poucet,et al.  Medial prefrontal lesions in the rat and spatial navigation: evidence for impaired planning. , 1995, Behavioral neuroscience.

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

[20]  Margaret F. Carr,et al.  Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval , 2011, Nature Neuroscience.

[21]  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.

[22]  Stefano Fusi,et al.  Hippocampal-prefrontal input supports spatial encoding in working memory , 2015, Nature.

[23]  David J. Foster,et al.  Reverse replay of behavioural sequences in hippocampal place cells during the awake state , 2006, Nature.

[24]  W E Skaggs,et al.  Deciphering the hippocampal polyglot: the hippocampus as a path integration system. , 1996, The Journal of experimental biology.

[25]  H. Eichenbaum,et al.  Hippocampal representation in place learning , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  Howard Eichenbaum,et al.  Distinct Pathways for Rule-Based Retrieval and Spatial Mapping of Memory Representations in Hippocampal Neurons , 2013, The Journal of Neuroscience.

[27]  Albert K. Lee,et al.  Memory of Sequential Experience in the Hippocampus during Slow Wave Sleep , 2002, Neuron.

[28]  M. Moser,et al.  A prefrontal–thalamo–hippocampal circuit for goal-directed spatial navigation , 2015, Nature.

[29]  Bruno Poucet,et al.  Prefrontal Cortex Focally Modulates Hippocampal Place Cell Firing Patterns , 2013, The Journal of Neuroscience.

[30]  Edvard I. Moser,et al.  Speed cells in the medial entorhinal cortex , 2015, Nature.

[31]  E. Save,et al.  Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[33]  Ehren L. Newman,et al.  Phase coding by grid cells in unconstrained environments: two‐dimensional phase precession , 2013, The European journal of neuroscience.

[34]  E. Tolman,et al.  Studies in spatial learning: Orientation and the short-cut. , 1946, Journal of experimental psychology.

[35]  Jean-Christophe Cassel,et al.  The Ventral Midline Thalamus Contributes to Strategy Shifting in a Memory Task Requiring Both Prefrontal Cortical and Hippocampal Functions , 2013, The Journal of Neuroscience.

[36]  M. Wilson,et al.  Trajectory Encoding in the Hippocampus and Entorhinal Cortex , 2000, Neuron.

[37]  B. McNaughton,et al.  Spatial information content and reliability of hippocampal CA1 neurons: Effects of visual input , 1994, Hippocampus.

[38]  J. Csicsvari,et al.  Theta phase–specific codes for two-dimensional position, trajectory and heading in the hippocampus , 2008, Nature Neuroscience.

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

[40]  Erika Cerasti,et al.  Retrospectively and Prospectively Modulated Hippocampal Place Responses Are Differentially Distributed along a Common Path in a Continuous T-Maze , 2014, The Journal of Neuroscience.

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

[42]  R. Vertes,et al.  Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat , 2007, Brain Structure and Function.

[43]  R. Wehner,et al.  PATH INTEGRATION IN DESERT ANTS. APPROACHING A LONG-STANDING PUZZLE IN INSECT NAVIGATION , 2013 .

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

[45]  E Save,et al.  Sensory and Memory Properties of Hippocampal Place Cells , 2000, Reviews in the neurosciences.

[46]  P W Burgess,et al.  Strategy application disorder: the role of the frontal lobes in human multitasking , 2000, Psychological research.

[47]  L. Swanson,et al.  A direct projection from Ammon's horn to prefrontal cortex in the rat , 1981, Brain Research.

[48]  E. Maguire,et al.  The Human Hippocampus and Spatial and Episodic Memory , 2002, Neuron.

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

[50]  N Burgess,et al.  Bilateral hippocampal pathology impairs topographical and episodic memory but not visual pattern matching , 2001, Hippocampus.

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

[52]  K. Lohmann,et al.  Geomagnetic imprinting: A unifying hypothesis of long-distance natal homing in salmon and sea turtles , 2008, Proceedings of the National Academy of Sciences.

[53]  G. Buzsáki Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning , 2015, Hippocampus.

[54]  M. Jung,et al.  Prefrontal cortex and hippocampus subserve different components of working memory in rats. , 2008, Learning & memory.

[55]  Hugo J. Spiers,et al.  Keeping the goal in mind: Prefrontal contributions to spatial navigation , 2008, Neuropsychologia.

[56]  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.

[57]  M. Herkenham The connections of the nucleus reuniens thalami: Evidence for a direct thalamo‐hippocampal pathway in the rat , 1978, The Journal of comparative neurology.

[58]  M. Witter,et al.  Projection from the nucleus reuniens thalami to the hippocampal region: Light and electron microscopic tracing study in the rat with the anterograde tracer Phaseolus vulgaris‐leucoagglutinin , 1990, The Journal of comparative neurology.

[59]  G. Buzsáki,et al.  Selective suppression of hippocampal ripples impairs spatial memory , 2009, Nature Neuroscience.

[60]  R. Wehner Astronavigation in insects , 1984 .

[61]  R. Mair,et al.  Inactivation of ventral midline thalamus produces selective spatial delayed conditional discrimination impairment in the rat , 2012, Hippocampus.

[62]  B. Cosquer,et al.  The Ventral Midline Thalamus (Reuniens and Rhomboid Nuclei) Contributes to the Persistence of Spatial Memory in Rats , 2012, The Journal of Neuroscience.

[63]  Conor Liston,et al.  Projections from neocortex mediate top-down control of memory retrieval , 2015, Nature.

[64]  R. Andersen,et al.  Head position signals used by parietal neurons to encode locations of visual stimuli , 1995, Nature.

[65]  J. Glowinski,et al.  Anatomical and electrophysiological evidence for a direct projection from ammon's horn to the medial prefrontal cortex in the rat , 2004, Experimental Brain Research.

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

[67]  Torkel Hafting,et al.  Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex , 2006, Science.

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

[69]  B. Milner Some cognitive effects of frontal-lobe lesions in man. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[70]  I. Fried,et al.  Direct recordings of grid-like neuronal activity in human spatial navigation , 2013, Nature Neuroscience.

[71]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[72]  Larry R. Squire,et al.  Memory for places learned long ago is intact after hippocampal damage , 1999, Nature.

[73]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

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

[75]  R. Vertes,et al.  Nucleus reuniens of the midline thalamus: Link between the medial prefrontal cortex and the hippocampus , 2007, Brain Research Bulletin.

[76]  Andrew M. Wikenheiser,et al.  Hippocampal theta sequences reflect current goals , 2015, Nature Neuroscience.

[77]  R. Wehner,et al.  The Ant Odometer: Stepping on Stilts and Stumps , 2006, Science.

[78]  Elisa Ciaramelli,et al.  The role of ventromedial prefrontal cortex in navigation: A case of impaired wayfinding and rehabilitation , 2008, Neuropsychologia.

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

[80]  R. Mair,et al.  Lesions of reuniens and rhomboid thalamic nuclei impair radial maze win‐shift performance , 2010, Hippocampus.

[81]  R Wehner,et al.  Path integration in desert ants, Cataglyphis fortis. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[82]  T. Shallice Specific impairments of planning. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[84]  Mark A. Rossi,et al.  Prefrontal cortical mechanisms underlying delayed alternation in mice. , 2012, Journal of neurophysiology.

[85]  Julia Mehlhorn,et al.  Neurobiology of the homing pigeon—a review , 2009, Naturwissenschaften.