Manipulating Hippocampal Place Cell Activity by Single-Cell Stimulation in Freely Moving Mice.

Learning critically depends on the ability to rapidly form and store non-overlapping representations of the external world. In line with their postulated role in episodic memory, hippocampal place cells can undergo a rapid reorganization of their firing fields upon contextual manipulations. To explore the mechanisms underlying such global remapping, we juxtacellularly stimulated 42 hippocampal neurons in freely moving mice during spatial exploration. We found that evoking spike trains in silent neurons was sufficient for creating place fields, while in place cells, juxtacellular stimulation induced a rapid remapping of their place fields to the stimulus location. The occurrence of complex spikes was most predictive of place field plasticity. Our data thus indicate that plasticity-inducing stimuli are able to rapidly bias place cell activity, simultaneously suppressing existing place fields. We propose that such competitive place field dynamics could support the orthogonalization of the hippocampal map during global remapping.

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

[2]  Esther Rodriguez-Villegas,et al.  TaiNi: Maximizing research output whilst improving animals’ welfare in neurophysiology experiments , 2017, Scientific Reports.

[3]  Wulfram Gerstner,et al.  Intrinsic Stabilization of Output Rates by Spike-Based Hebbian Learning , 2001, Neural Computation.

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

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

[6]  Yoko Yamaguchi,et al.  Conserving total synaptic weight ensures one-trial sequence learning of place fields in the hippocampus , 2006, Neural Networks.

[7]  Katie C. Bittner,et al.  Behavioral time scale synaptic plasticity underlies CA1 place fields , 2017, Science.

[8]  W. Singer,et al.  Relations Between Long‐term Synaptic Modifications and Paired‐pulse Interactions in the Rat Neocortex , 1997, The European journal of neuroscience.

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

[10]  Christopher M. Lee,et al.  Heterosynaptic Plasticity Prevents Runaway Synaptic Dynamics , 2013, The Journal of Neuroscience.

[11]  Michael Brecht,et al.  Juxtacellular recording and morphological identification of single neurons in freely moving rats , 2014, Nature Protocols.

[12]  Michael Brecht,et al.  Intracellular Determinants of Hippocampal CA1 Place and Silent Cell Activity in a Novel Environment , 2011, Neuron.

[13]  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.

[14]  M. Volgushev,et al.  Heterosynaptic Plasticity , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[15]  M. Brecht,et al.  Spiking Irregularity and Frequency Modulate the Behavioral Report of Single-Neuron Stimulation , 2014, Neuron.

[16]  K. Miller,et al.  Synaptic Economics: Competition and Cooperation in Synaptic Plasticity , 1996, Neuron.

[17]  Terrence J. Sejnowski,et al.  Synaptic Learning Rules and Sparse Coding in a Model Sensory System , 2008, PLoS Comput. Biol..

[18]  G. Lynch,et al.  Heterosynaptic depression: a postsynaptic correlate of long-term potentiation , 1977, Nature.

[19]  Doyun Lee,et al.  Hippocampal Place Fields Emerge upon Single-Cell Manipulation of Excitability During Behavior , 2012, Science.

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

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

[22]  T. Elliott,et al.  Multiplicative Synaptic Normalization and a Nonlinear Hebb Rule Underlie a Neurotrophic Model of Competitive Synaptic Plasticity , 2002, Neural Computation.

[23]  Maik C. Stüttgen,et al.  Temporally precise control of single-neuron spiking by juxtacellular nanostimulation. , 2017, Journal of neurophysiology.

[24]  Chenglin Miao,et al.  Place cells in the hippocampus: Eleven maps for eleven rooms , 2014, Proceedings of the National Academy of Sciences.

[25]  B. McNaughton,et al.  Synaptic enhancement in fascia dentata: Cooperativity among coactive afferents , 1978, Brain Research.

[26]  Alessandro Treves,et al.  Stable and Rapid Recurrent Processing in Realistic Autoassociative Memories , 1998, Neural Computation.

[27]  L. Abbott,et al.  Synaptic plasticity: taming the beast , 2000, Nature Neuroscience.

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

[29]  Nils Z. Borgesius,et al.  A Novel Mechanism for the Grid-to-Place Cell Transformation Revealed by Transgenic Depolarization of Medial Entorhinal Cortex Layer II , 2017, Neuron.

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

[31]  D. Dupret,et al.  Recoding a cocaine-place memory engram to a neutral engram in the hippocampus , 2016, Nature Neuroscience.

[32]  Maria Diamantaki,et al.  Priming Spatial Activity by Single-Cell Stimulation in the Dentate Gyrus of Freely Moving Rats , 2016, Current Biology.

[33]  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.

[34]  Edward S Boyden,et al.  Transient optogenetic inactivation of the medial entorhinal cortex biases the active population of hippocampal neurons , 2016, Hippocampus.

[35]  M. Brecht,et al.  Behavioural report of single neuron stimulation in somatosensory cortex , 2008, Nature.

[36]  Jozsef Csicsvari,et al.  Activity-dependent plasticity of hippocampal place maps , 2016, Nature Communications.

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

[38]  Andrea Burgalossi,et al.  Linking neuronal structure to function in rodent hippocampus: a methodological prospective , 2017, Cell and Tissue Research.

[39]  L. Frank,et al.  Behavioral/Systems/Cognitive Hippocampal Plasticity across Multiple Days of Exposure to Novel Environments , 2022 .

[40]  S. Kaplan.  The Physiology of Thought , 1950 .

[41]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[42]  Maria Diamantaki,et al.  Sparse activity of identified dentate granule cells during spatial exploration , 2016, eLife.

[43]  H. Yamahachi,et al.  Hippocampal Remapping after Partial Inactivation of the Medial Entorhinal Cortex , 2015, Neuron.

[44]  M. Moser,et al.  Understanding memory through hippocampal remapping , 2008, Trends in Neurosciences.

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

[46]  A. J. Hill.  First occurrence of hippocampal spatial firing in a new environment , 1978, Experimental Neurology.

[47]  D. Pinault,et al.  A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin , 1996, Journal of Neuroscience Methods.

[48]  Michael Brecht,et al.  Nanostimulation: manipulation of single neuron activity by juxtacellular current injection. , 2010, Journal of neurophysiology.

[49]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[50]  Hugo J. Spiers,et al.  Place Field Repetition and Purely Local Remapping in a Multicompartment Environment , 2013, Cerebral cortex.

[51]  Jeremy D. Cohen,et al.  Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments , 2017, eLife.