Rhythmic coordination of hippocampal neurons during associative memory processing

Hippocampal oscillations are dynamic, with unique oscillatory frequencies present during different behavioral states. To examine the extent to which these oscillations reflect neuron engagement in distinct local circuit processes that are important for memory, we recorded single cell and local field potential activity from the CA1 region of the hippocampus as rats performed a context-guided odor-reward association task. We found that theta (4–12 Hz), beta (15–35 Hz), low gamma (35–55 Hz), and high gamma (65–90 Hz) frequencies exhibited dynamic amplitude profiles as rats sampled odor cues. Interneurons and principal cells exhibited unique engagement in each of the four rhythmic circuits in a manner that related to successful performance of the task. Moreover, principal cells coherent to each rhythm differentially represented task dimensions. These results demonstrate that distinct processing states arise from the engagement of rhythmically identifiable circuits, which have unique roles in organizing task-relevant processing in the hippocampus. DOI: http://dx.doi.org/10.7554/eLife.09849.001

[1]  G. Buzsáki,et al.  Hippocampal theta activity following selective lesion of the septal cholinergic systeM , 1994, Neuroscience.

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

[3]  A. Chiba,et al.  Cell Assemblies of the Basal Forebrain , 2015, The Journal of Neuroscience.

[4]  H. Eichenbaum,et al.  The global record of memory in hippocampal neuronal activity , 1999, Nature.

[5]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

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

[7]  Mark A. Kramer,et al.  Rate-adjusted spike–LFP coherence comparisons from spike-train statistics , 2015, Journal of Neuroscience Methods.

[8]  Frances S. Chance,et al.  Erratum: Orthogonal micro-organization of orientation and spatial frequency in primate primary visual cortex , 2013, Nature Neuroscience.

[9]  E. Moser,et al.  Gamma oscillations in the hippocampus. , 2010, Physiology.

[10]  N. Hatsopoulos,et al.  Propagating waves mediate information transfer in the motor cortex , 2006, Nature Neuroscience.

[11]  H. Eichenbaum,et al.  Robust Conjunctive Item–Place Coding by Hippocampal Neurons Parallels Learning What Happens Where , 2009, The Journal of Neuroscience.

[12]  G. Buzsáki,et al.  Inhibition-Induced Theta Resonance in Cortical Circuits , 2013, Neuron.

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

[14]  Claire Martin,et al.  An olfacto-hippocampal network is dynamically involved in odor-discrimination learning. , 2007, Journal of neurophysiology.

[15]  Dimitri M. Kullmann,et al.  Oscillatory multiplexing of population codes for selective communication in the mammalian brain , 2014, Nature Reviews Neuroscience.

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

[17]  Sean M Montgomery,et al.  Behavior-Dependent Coordination of Multiple Theta Dipoles in the Hippocampus , 2009, The Journal of Neuroscience.

[18]  Adriano B. L. Tort,et al.  Theta–gamma coupling increases during the learning of item–context associations , 2009, Proceedings of the National Academy of Sciences.

[19]  H. Eichenbaum,et al.  Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. , 2010, Journal of neurophysiology.

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

[21]  Miles A. Whittington,et al.  Neurosystems: brain rhythms and cognitive processing , 2013, The European journal of neuroscience.

[22]  G. Ermentrout,et al.  Gamma rhythms and beta rhythms have different synchronization properties. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  H. Eichenbaum,et al.  Memory Representation within the Parahippocampal Region , 1997, The Journal of Neuroscience.

[24]  W. Freeman,et al.  Bidirectional processing in the olfactory-limbic axis during olfactory behavior. , 1998, Behavioral neuroscience.

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

[26]  Vaughn L. Hetrick,et al.  Transient 23–30 Hz oscillations in mouse hippocampus during exploration of novel environments , 2008, Hippocampus.

[27]  Claire Martin,et al.  Directional coupling from the olfactory bulb to the hippocampus during a go/no-go odor discrimination task. , 2010, Journal of neurophysiology.

[28]  Sachin S. Deshmukh,et al.  Representation of Non-Spatial and Spatial Information in the Lateral Entorhinal Cortex , 2011, Front. Behav. Neurosci..

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

[30]  Nancy Kopell,et al.  Analysis of State-Dependent Transitions in Frequency and Long-Distance Coordination in a Model Oscillatory Cortical Circuit , 2003, Journal of Computational Neuroscience.

[31]  G. Buzsáki,et al.  Hippocampal CA1 interneurons: an in vivo intracellular labeling study , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  A. Chiba,et al.  Theta and beta oscillatory dynamics in the dentate gyrus reveal a shift in network processing state during cue encounters , 2015, Front. Syst. Neurosci..

[33]  G. Buzsáki,et al.  Interneurons of the hippocampus , 1998, Hippocampus.

[34]  G Buzsáki,et al.  Interneurons in the Hippocampal Dentate Gyrus: an In Vivo intracellular Study , 1997, The European journal of neuroscience.

[35]  György Buzsáki,et al.  Neural Syntax: Cell Assemblies, Synapsembles, and Readers , 2010, Neuron.

[36]  György Buzsáki,et al.  Editorial overview: Brain rhythms and dynamic coordination , 2015, Current Opinion in Neurobiology.

[37]  Eric L. Denovellis,et al.  Synchronous Oscillatory Neural Ensembles for Rules in the Prefrontal Cortex , 2012, Neuron.

[38]  Li Lu,et al.  Coordination of entorhinal–hippocampal ensemble activity during associative learning , 2014, Nature.

[39]  R. Muller,et al.  Spatial firing properties of hippocampal theta cells , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  G. Buzsáki,et al.  Interdependence of Multiple Theta Generators in the Hippocampus: a Partial Coherence Analysis , 1999, The Journal of Neuroscience.

[41]  Miles A Whittington,et al.  Long-range synchronization of gamma and beta oscillations and the plasticity of excitatory and inhibitory synapses: a network model. , 2002, Journal of neurophysiology.

[42]  H. Eichenbaum,et al.  Brain Rhythms: Towards a Coherent Picture of Ensemble Development in Learning , 2014, Current Biology.

[43]  György Buzsáki,et al.  Tasks for inhibitory interneurons in intact brain circuits , 2015, Neuropharmacology.

[44]  G. Buzsáki,et al.  Theta Oscillations Provide Temporal Windows for Local Circuit Computation in the Entorhinal-Hippocampal Loop , 2009, Neuron.

[45]  A. Chiba,et al.  Learning‐dependent dynamics of beta‐frequency oscillations in the basal forebrain of rats , 2010, The European journal of neuroscience.

[46]  Jack W. Tsao,et al.  Observed brain dynamics, P.P. Mitra, H. Bokil. Oxford University Press (2008), ISBN-13: 978-0-19-517808-1, 381 pages, $65.00 , 2009 .

[47]  G. Buzsáki,et al.  Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. , 2004, Journal of neurophysiology.

[48]  Daniel K. Leventhal,et al.  Basal Ganglia Beta Oscillations Accompany Cue Utilization , 2012, 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]  Roger D. Traub,et al.  Long-Range Synchronization of γ and β Oscillations and the Plasticity of Excitatory and Inhibitory Synapses: A Network Model , 2002 .

[51]  Eran Stark,et al.  In vivo optogenetic identification and manipulation of GABAergic interneuron subtypes. , 2023, ArXiv.