Transformation of the head-direction signal into a spatial code

Animals integrate multiple sensory inputs to successfully navigate in their environments. Head direction (HD), boundary vector, grid and place cells in the entorhinal-hippocampal network form the brain’s navigational system that allows to identify the animal’s current location, but how the functions of these specialized neuron types are acquired remain to be understood. Here we report that activity of HD neurons is influenced by the ambulatory constraints imposed upon the animal by the boundaries of the explored environment, leading to spurious spatial information. However, in the post-subiculum, the main cortical stage of HD signal processing, HD neurons convey true spatial information in the form of border modulated activity through the integration of additional sensory modalities relative to egocentric position, unlike their driving thalamic inputs. These findings demonstrate how the combination of HD and egocentric information can be transduced into a spatial code.A cognitive map of space must integrate allocentric cues such as head direction (HD) with various egocentric cues. Here the authors report that anterior thalamic (ADn) neurons encode a pure HD signal, while neurons in post-subiculum represent a conjunction of HD and egocentric cues such as body posture with respect to environment boundaries.

[1]  R. Muller,et al.  On the directional firing properties of hippocampal place cells , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  Bruce L. McNaughton,et al.  An Information-Theoretic Approach to Deciphering the Hippocampal Code , 1992, NIPS.

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

[4]  Lisa M. Giocomo,et al.  Topography of Head Direction Cells in Medial Entorhinal Cortex , 2014, Current Biology.

[5]  Markus Frey,et al.  Anatomical organization of presubicular head-direction circuits , 2016, eLife.

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

[7]  Nachum Ulanovsky,et al.  Encoding of Head Direction by Hippocampal Place Cells in Bats , 2014, The Journal of Neuroscience.

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

[9]  Mark P. Brandon,et al.  Reduction of Theta Rhythm Dissociates Grid Cell Spatial Periodicity from Directional Tuning , 2011, Science.

[10]  Roland Maurer,et al.  Resetting the path integrator: a basic condition for route-based navigation , 2004, Journal of Experimental Biology.

[11]  Surya Ganguli,et al.  Environmental Boundaries as an Error Correction Mechanism for Grid Cells , 2015, Neuron.

[12]  Mayank R. Mehta,et al.  Causal Influence of Visual Cues on Hippocampal Directional Selectivity , 2016, Cell.

[13]  Neil Burgess,et al.  Characterizing multiple independent behavioral correlates of cell firing in freely moving animals , 2005, Hippocampus.

[14]  Song-Lin Ding,et al.  Comparative anatomy of the prosubiculum, subiculum, presubiculum, postsubiculum, and parasubiculum in human, monkey, and rodent , 2013, The Journal of comparative neurology.

[15]  Thomas J. Wills,et al.  Development of the Hippocampal Cognitive Map in Preweanling Rats , 2010, Science.

[16]  H. T. Blair,et al.  The anatomical and computational basis of the rat head-direction cell signal , 2001, Trends in Neurosciences.

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

[18]  Thomas J. Wills,et al.  Theta-Modulated Place-by-Direction Cells in the Hippocampal Formation in the Rat , 2004, The Journal of Neuroscience.

[19]  Thomas J. Wills,et al.  The Development of the Head Direction System before Eye Opening in the Rat , 2015, Current Biology.

[20]  B. J. Clark,et al.  Interaction of Egocentric and World-Centered Reference Frames in the Rat Posterior Parietal Cortex , 2014, The Journal of Neuroscience.

[21]  J. Taube,et al.  Interaction between the Postsubiculum and Anterior Thalamus in the Generation of Head Direction Cell Activity , 1997, The Journal of Neuroscience.

[22]  Benjamin J Clark,et al.  Control of anterodorsal thalamic head direction cells by environmental boundaries: Comparison with conflicting distal landmarks , 2012, Hippocampus.

[23]  Jonathan D. Cohen,et al.  Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex , 2006 .

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

[25]  Christian F. Doeller,et al.  Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory , 2008, Proceedings of the National Academy of Sciences.

[26]  P. Dudchenko The hippocampus as a cognitive map , 2010 .

[27]  Ryan P. Adams,et al.  Mapping Sub-Second Structure in Mouse Behavior , 2015, Neuron.

[28]  Michael E. Hasselmo,et al.  Multiple Running Speed Signals in Medial Entorhinal Cortex , 2016, Neuron.

[29]  E. J. Green,et al.  Head-direction cells in the rat posterior cortex , 1994, Experimental Brain Research.

[30]  K. Harris Neural signatures of cell assembly organization , 2005, Nature Reviews Neuroscience.

[31]  L. Christophorou Science , 2018, Emerging Dynamics: Science, Energy, Society and Values.

[32]  G. Buzsáki,et al.  Internally-organized mechanisms of the head direction sense , 2015, Nature Neuroscience.

[33]  J. Taube Head direction cells recorded in the anterior thalamic nuclei of freely moving rats , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  Karel Svoboda,et al.  Neural coding in barrel cortex during whisker-guided locomotion , 2015, eLife.

[35]  K M Gothard,et al.  Dynamics of Mismatch Correction in the Hippocampal Ensemble Code for Space: Interaction between Path Integration and Environmental Cues , 1996, The Journal of Neuroscience.

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

[37]  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.

[38]  J. O’Keefe,et al.  Boundary Vector Cells in the Subiculum of the Hippocampal Formation , 2009, The Journal of Neuroscience.

[39]  S Leutgeb,et al.  Convergence of Head Direction and Place Information in the Ca1 Region of Hippocampus Subjects and Behavioral Testing , 2000 .

[40]  G. Buzsáki,et al.  Hippocampal Network Dynamics Constrain the Time Lag between Pyramidal Cells across Modified Environments , 2008, The Journal of Neuroscience.

[41]  Michael Brecht,et al.  Functional Architecture of the Rat Parasubiculum , 2016, The Journal of Neuroscience.

[42]  G. Buzsáki Theta Oscillations in the Hippocampus , 2002, Neuron.

[43]  M. Brecht,et al.  Head-Directional Tuning and Theta Modulation of Anatomically Identified Neurons in the Presubiculum , 2015, The Journal of Neuroscience.

[44]  J. O’Keefe,et al.  An oscillatory interference model of grid cell firing , 2007, Hippocampus.

[45]  P. E. Sharp Multiple spatial/behavioral correlates for cells in the rat postsubiculum: multiple regression analysis and comparison to other hippocampal areas. , 1996, Cerebral cortex.

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

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

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

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

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

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

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

[53]  M. Moser,et al.  Representation of Geometric Borders in the Developing Rat , 2014, Neuron.

[54]  Ariane S Etienne,et al.  Path integration in mammals , 2004, Hippocampus.

[55]  R. Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  J. Csicsvari,et al.  Organization of cell assemblies in the hippocampus , 2003, Nature.

[57]  Edvard I. Moser,et al.  Shearing-induced asymmetry in entorhinal grid cells , 2015, Nature.

[58]  J. O’Keefe,et al.  Neural Representations of Location Composed of Spatially Periodic Bands , 2012, Science.

[59]  Charlotte N. Boccara,et al.  Grid cells in pre- and parasubiculum , 2010, Nature Neuroscience.

[60]  R U Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  M. Moser,et al.  Coherence among Head Direction Cells before Eye Opening in Rat Pups , 2015, Current Biology.

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

[63]  A. Berthoz,et al.  Background, But Not Foreground, Spatial Cues Are Taken as References for Head Direction Responses by Rat Anterodorsal Thalamus Neurons , 2001, The Journal of Neuroscience.

[64]  H. Shibata Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat , 1993, The Journal of comparative neurology.

[65]  M. Moser,et al.  Representation of Geometric Borders in the Entorhinal Cortex , 2008, Science.

[66]  Uri T Eden,et al.  A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects. , 2005, Journal of neurophysiology.

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

[68]  Y. Benjamini,et al.  Estimating wall guidance and attraction in mouse free locomotor behavior , 2007, Genes, brain, and behavior.

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

[70]  H. Mittelstaedt,et al.  Homing by path integration in a mammal , 1980, Naturwissenschaften.

[71]  J. Knierim,et al.  Influence of boundary removal on the spatial representations of the medial entorhinal cortex , 2008, Hippocampus.

[72]  A. Berthoz,et al.  Rapid Spatial Reorientation and Head Direction Cells , 2003, The Journal of Neuroscience.

[73]  J. Taube The head direction signal: origins and sensory-motor integration. , 2007, Annual review of neuroscience.