Phase organization of network computations

Coupled oscillations are hypothesized to organize the processing of information across distributed brain circuits. This idea is supported by recent evidence, and newly developed techniques promise to put such theoretical framework to mechanistic testing. We review evidence suggesting that individual oscillatory cycles constitute a functional unit that organizes activity in neural networks, and that oscillatory phase (defined as the fraction of the wave cycle that has elapsed relative to the start of the cycle) is a key oscillatory parameter to implement the functions of oscillations in limbic networks. We highlight neural manipulation techniques that currently allow for causal testing of these hypotheses.

[1]  J. T. Erichsen,et al.  Nucleus reuniens of the thalamus contains head direction cells , 2014, eLife.

[2]  L Kellényi,et al.  Depth profiles of hippocampal rhythmic slow activity ('theta rhythm') depend on behaviour. , 1985, Electroencephalography and clinical neurophysiology.

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

[4]  György Buzsáki,et al.  Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance , 2007, Proceedings of the National Academy of Sciences.

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

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

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

[8]  A. Treves,et al.  Theta-paced flickering between place-cell maps in the hippocampus , 2011, Nature.

[9]  Matthew A Wilson,et al.  Enhancement of encoding and retrieval functions through theta phase-specific manipulation of hippocampus , 2014, eLife.

[10]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

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

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

[13]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[14]  M. Hasselmo,et al.  What is the Functional Relevance of Prefrontal Cortex Entrainment to Hippocampal Theta Rhythms? , 2011, Front. Neurosci..

[15]  Evgueniy V. Lubenov,et al.  Prefrontal Phase Locking to Hippocampal Theta Oscillations , 2005, Neuron.

[16]  M. Wilson,et al.  Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat , 2009, Hippocampus.

[17]  Markus Siegel,et al.  Corticostriatal Coordination through Coherent Phase-Amplitude Coupling , 2014, The Journal of Neuroscience.

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

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

[20]  M. Quirk,et al.  Experience-Dependent Asymmetric Shape of Hippocampal Receptive Fields , 2000, Neuron.

[21]  T. Womelsdorf,et al.  Neuronal coherence during selective attentional processing and sensory–motor integration , 2006, Journal of Physiology-Paris.

[22]  Matthew A. Wilson,et al.  Hippocampal Replay of Extended Experience , 2009, Neuron.

[23]  Mark P. Brandon,et al.  Segregation of cortical head direction cell assemblies on alternating theta cycles , 2013, Nature Neuroscience.

[24]  J E Lisman,et al.  Storage of 7 +/- 2 short-term memories in oscillatory subcycles , 1995, Science.

[25]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

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

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

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

[29]  M. Wilson,et al.  Cingulate-Hippocampus Coherence and Trajectory Coding in a Sequential Choice Task , 2014, Neuron.

[30]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[31]  Jai Y. Yu,et al.  Hippocampal–cortical interaction in decision making , 2015, Neurobiology of Learning and Memory.

[32]  M. Wilson,et al.  Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm , 2005, Hippocampus.

[33]  Eric A. Zilli,et al.  Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior , 2005, Hippocampus.

[34]  Y. Sakurai,et al.  Oscillatory interaction between amygdala and hippocampus coordinates behavioral modulation based on reward expectation , 2013, Front. Behav. Neurosci..

[35]  M. Wilson,et al.  Theta Rhythms Coordinate Hippocampal–Prefrontal Interactions in a Spatial Memory Task , 2005, PLoS biology.

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

[37]  M. Hasselmo,et al.  Stimulation in Hippocampal Region CA1 in Behaving Rats Yields Long-Term Potentiation when Delivered to the Peak of Theta and Long-Term Depression when Delivered to the Trough , 2003, The Journal of Neuroscience.

[38]  Mehdi Khamassi,et al.  Coherent Theta Oscillations and Reorganization of Spike Timing in the Hippocampal- Prefrontal Network upon Learning , 2010, Neuron.

[39]  E. Miller,et al.  Increases in Functional Connectivity between Prefrontal Cortex and Striatum during Category Learning , 2014, Neuron.