Subcircuits of Deep and Superficial CA1 Place Cells Support Efficient Spatial Coding across Heterogeneous Environments

The hippocampus is thought to guide navigation by forming a cognitive map of space. However, the behavioral demands for such a map can vary depending on particular features of a given environment. For example, an environment rich in cues may require a finer resolution map than an open space. It is unclear how the hippocampal cognitive map adjusts to meet these distinct behavioral demands. To address this issue, we examined the spatial coding characteristics of hippocampal neurons in mice and rats navigating different environments. We found that CA1 place cells located in the superficial sublayer were more active in cue-poor environments, and preferentially used a firing rate code driven by intra-hippocampal inputs. In contrast, place cells located in the deep sublayer were more active in cue-rich environments and expressed a phase code driven by entorhinal inputs. Switching between these two spatial coding modes was supported by the interaction between excitatory gamma inputs and local inhibition.

[1]  A. Treves,et al.  Distinct Ensemble Codes in Hippocampal Areas CA3 and CA1 , 2004, Science.

[2]  L. Slomianka,et al.  Hippocampal pyramidal cells: the reemergence of cortical lamination , 2011, Brain Structure and Function.

[3]  Ethan Meyers,et al.  The neural decoding toolbox , 2013, Front. Neuroinform..

[4]  May-Britt Moser,et al.  Functional diversity along the transverse axis of hippocampal area CA1 , 2014, FEBS letters.

[5]  Antal Berényi,et al.  Role of Hippocampal CA2 Region in Triggering Sharp-Wave Ripples , 2016, Neuron.

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

[7]  Richard Kempter,et al.  Quantifying circular–linear associations: Hippocampal phase precession , 2012, Journal of Neuroscience Methods.

[8]  Jadin C. Jackson,et al.  Quantitative measures of cluster quality for use in extracellular recordings , 2005, Neuroscience.

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

[10]  L. Colgin,et al.  Slow and Fast Gamma Rhythms Coordinate Different Spatial Coding Modes in Hippocampal Place Cells , 2014, Neuron.

[11]  Sébastien Royer,et al.  Place cells are more strongly tied to landmarks in deep than in superficial CA1 , 2017, Nature Communications.

[12]  György Buzsáki,et al.  Preexisting hippocampal network dynamics constrain optogenetically induced place fields , 2019, Neuron.

[13]  J. O’Keefe,et al.  Dual phase and rate coding in hippocampal place cells: Theoretical significance and relationship to entorhinal grid cells , 2005, Hippocampus.

[14]  Farnaz Sharif,et al.  Implantation of Chronic Silicon Probes and Recording of Hippocampal Place Cells in an Enriched Treadmill Apparatus. , 2017, Journal of visualized experiments : JoVE.

[15]  M. Witter,et al.  Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region , 1989, Progress in Neurobiology.

[16]  David H. Brann,et al.  Medial and Lateral Entorhinal Cortex Differentially Excite Deep versus Superficial CA1 Pyramidal Neurons. , 2017, Cell reports.

[17]  Andrea Navas-Olive,et al.  Multimodal determinants of phase-locked dynamics across deep-superficial hippocampal sublayers during theta oscillations , 2020, Nature Communications.

[18]  Manuel Valero,et al.  Multimodal determinants of phase-locked dynamics across deep-superficial hippocampal sublayers during theta oscillations , 2020, bioRxiv.

[19]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[20]  Alexander J Morley,et al.  Parsing Hippocampal Theta Oscillations by Nested Spectral Components during Spatial Exploration and Memory-Guided Behavior , 2018, Neuron.

[21]  Thomas Klausberger,et al.  Hippocampal Place Cells Couple to Three Different Gamma Oscillations during Place Field Traversal , 2016, Neuron.

[22]  B. McNaughton,et al.  Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. , 1998, Journal of neurophysiology.

[23]  Farnaz Sharif,et al.  Differential Representation of Landmark and Self-Motion Information along the CA1 Radial Axis: Self-Motion Generated Place Fields Shift toward Landmarks during Septal Inactivation , 2018, The Journal of Neuroscience.

[24]  G. Buzsáki,et al.  Temporal Encoding of Place Sequences by Hippocampal Cell Assemblies , 2006, Neuron.

[25]  A. Jacobi von Wangelin,et al.  Reductive cross-coupling reactions between two electrophiles. , 2014, Chemistry.

[26]  Kenneth D. Harris,et al.  High-Dimensional Cluster Analysis with the Masked EM Algorithm , 2013, Neural Computation.

[27]  Mayank R. Mehta,et al.  Multisensory Control of Hippocampal Spatiotemporal Selectivity , 2013, Science.

[28]  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.

[29]  Mark P. Brandon,et al.  THE MEDIAL ENTORHINAL CORTEX IS NECESSARY FOR TEMPORAL ORGANIZATION OF HIPPOCAMPAL NEURONAL ACTIVITY , 2015, Nature Neuroscience.

[30]  Jozsef Csicsvari,et al.  Dynamic Reconfiguration of Hippocampal Interneuron Circuits during Spatial Learning , 2013, Neuron.

[31]  G. Buzsáki,et al.  Hippocampal CA1 pyramidal cells form functionally distinct sublayers , 2011, Nature Neuroscience.

[32]  N. Spruston,et al.  Brain-derived neurotrophic factor differentially modulates excitability of two classes of hippocampal output neurons , 2016, Journal of neurophysiology.

[33]  Beat Lutz,et al.  Cannabinoid Control of Learning and Memory through HCN Channels , 2016, Neuron.

[34]  G. Buzsáki,et al.  Entorhinal-CA3 Dual-Input Control of Spike Timing in the Hippocampus by Theta-Gamma Coupling , 2017, Neuron.

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

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

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

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

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

[40]  Oscar Herreras,et al.  Identifying the synaptic origin of ongoing neuronal oscillations through spatial discrimination of electric fields , 2012, Front. Comput. Neurosci..

[41]  Susumu Tonegawa,et al.  Hippocampal CA3 Output Is Crucial for Ripple-Associated Reactivation and Consolidation of Memory , 2009, Neuron.

[42]  D. Amaral,et al.  The three-dimensional organization of the hippocampal formation: A review of anatomical data , 1989, Neuroscience.

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

[44]  Jeffrey D. Zaremba,et al.  Distinct Contribution of Adult-Born Hippocampal Granule Cells to Context Encoding , 2016, Neuron.

[45]  Daniel Gomez-Dominguez,et al.  Determinants of different deep and superficial CA1 pyramidal cell dynamics during sharp-wave ripples , 2015, Nature Neuroscience.

[46]  T. Hafting,et al.  Frequency of gamma oscillations routes flow of information in the hippocampus , 2009, Nature.

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

[48]  M. R. Mehta,et al.  Role of experience and oscillations in transforming a rate code into a temporal code , 2002, Nature.

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

[50]  Noah J. Cowan,et al.  Recalibration of path integration in hippocampal place cells , 2018, bioRxiv.

[51]  Antal Berényi,et al.  Spatial coding and physiological properties of hippocampal neurons in the Cornu Ammonis subregions , 2016, Hippocampus.

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

[53]  Lynn Hazan,et al.  Klusters, NeuroScope, NDManager: A free software suite for neurophysiological data processing and visualization , 2006, Journal of Neuroscience Methods.

[54]  Farnaz Sharif,et al.  Micro-drive and headgear for chronic implant and recovery of optoelectronic probes , 2017, Scientific Reports.

[55]  Kamran Diba,et al.  Activity dynamics and behavioral correlates of CA3 and CA1 hippocampal pyramidal neurons , 2012, Hippocampus.

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

[57]  Christiane E. I. Knappke,et al.  Reductive Cross‐Coupling Reactions Between Two Electrophiles , 2014 .

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

[59]  Susumu Tonegawa,et al.  Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons , 2015, Nature Neuroscience.

[60]  Christof Koch,et al.  Theta Phase Segregation of Input-Specific Gamma Patterns in Entorhinal-Hippocampal Networks , 2014, Neuron.

[61]  G. Buzsáki,et al.  Transformation of a Spatial Map across the Hippocampal-Lateral Septal Circuit , 2018, Neuron.

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

[63]  Sandro Romani,et al.  Inhibitory suppression of heterogeneously tuned excitation enhances spatial coding in CA1 place cells , 2017, Nature Neuroscience.

[64]  B. McNaughton,et al.  Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences , 1996, Hippocampus.

[65]  Oscar Herreras,et al.  Schaffer-Specific Local Field Potentials Reflect Discrete Excitatory Events at Gamma Frequency That May Fire Postsynaptic Hippocampal CA1 Units , 2012, The Journal of Neuroscience.

[66]  G. Buzsáki,et al.  Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[68]  Mark S. Cembrowski,et al.  Spatial Gene-Expression Gradients Underlie Prominent Heterogeneity of CA1 Pyramidal Neurons , 2016, Neuron.

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

[70]  Heydar Davoudi,et al.  Acute silencing of hippocampal CA3 reveals a dominant role in place field responses , 2018, Nature Neuroscience.

[71]  G. Buzsáki,et al.  Pyramidal Cell-Interneuron Circuit Architecture and Dynamics in Hippocampal Networks , 2017, Neuron.

[72]  G. Buzsáki,et al.  Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells , 2002, Nature.

[73]  Attila Losonczy,et al.  Parvalbumin-Positive Basket Cells Differentiate among Hippocampal Pyramidal Cells , 2014, Neuron.

[74]  John O'Keefe,et al.  Independent rate and temporal coding in hippocampal pyramidal cells , 2003, Nature.

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

[76]  David J. Foster,et al.  Hippocampal theta sequences , 2007, Hippocampus.