Zero-lag long-range synchronization via hippocampal dynamical relaying

Oscillations of cortical areas in gamma frequencies has been extensively studied, however, distant cortical areas are able to synchronize in other ranges besides the gamma band. Local field potentials recorded from the frontal (F) and visual (V) cortical areas of a rat performing exploratory motor behavior (active state) and motor quiescent (passive state) present distinct features concerning to the zero-lag synchronization of the two cortical regions. In this work, we study the occurrence of zero-lag synchronization of distant cortical areas in the theta band mediated by the hippocampus (H). We propose to model the different behavioral states (passive and active) with the dynamical relaying mechanism [1-3]. The model shows good agreement with the experiment as displayed in Fig. ​Fig.1,1, for the density of peaks obtained from the sliding window of the filtered average membrane potential cross-correlograms. Figure 1 Comparison between numerical simulations and experimental data for both active and passive states. The curves represent the normalized histogram of the density of peaks in each of the cross-correlogram sliding window (from -300 to 300 ms) of 1 minute ...

[1]  Leonardo L. Gollo,et al.  Dynamical relaying can yield zero time lag neuronal synchrony despite long conduction delays , 2008, Proceedings of the National Academy of Sciences.

[2]  Mercedes Atienza,et al.  The Role of Neural Synchronization in the Emergence of Cognition Across the Wake-Sleep Cycle , 2005, Reviews in the neurosciences.

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

[4]  S. Baker,et al.  Cortico-cerebellar coherence during a precision grip task in the monkey. , 2006, Journal of neurophysiology.

[5]  G. Edelman,et al.  Spike-timing dynamics of neuronal groups. , 2004, Cerebral cortex.

[6]  Y. Yaari,et al.  Extracellular Calcium Modulates Persistent Sodium Current-Dependent Burst-Firing in Hippocampal Pyramidal Neurons , 2001, The Journal of Neuroscience.

[7]  T. Womelsdorf,et al.  The role of neuronal synchronization in selective attention , 2007, Current Opinion in Neurobiology.

[8]  A. McIntosh,et al.  Mapping cognition to the brain through neural interactions. , 1999, Memory.

[9]  Peter Dayan,et al.  Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems , 2001 .

[10]  Leonardo L. Gollo,et al.  Dynamic control for synchronization of separated cortical areas through thalamic relay , 2010, NeuroImage.

[11]  Andreas Knoblauch,et al.  Synaptic plasticity, conduction delays, and inter-areal phase relations of spike activity in a model of reciprocally connected areas , 2003, Neurocomputing.

[12]  L STAN LEUNG,et al.  Generation of Theta and Gamma Rhythms in the Hippocampus , 1998, Neuroscience & Biobehavioral Reviews.

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

[14]  W. Singer,et al.  Visuomotor integration is associated with zero time-lag synchronization among cortical areas , 1997, Nature.

[15]  M. Hasselmo What is the function of hippocampal theta rhythm?—Linking behavioral data to phasic properties of field potential and unit recording data , 2005, Hippocampus.

[16]  G. Buzsáki,et al.  Hippocampal network patterns of activity in the mouse , 2003, Neuroscience.

[17]  Karl J. Friston,et al.  Zero-lag synchronous dynamics in triplets of interconnected cortical areas , 2001, Neural Networks.

[18]  Eugene M. Izhikevich,et al.  Simple model of spiking neurons , 2003, IEEE Trans. Neural Networks.

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

[20]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[21]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[22]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

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

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

[25]  Rony Paz,et al.  Theta synchronizes the activity of medial prefrontal neurons during learning. , 2008, Learning & memory.

[26]  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.

[27]  Jesse Jackson,et al.  Self-generated theta oscillations in the hippocampus , 2009, Nature Neuroscience.

[28]  Andrew M. Clark,et al.  Stimulus onset quenches neural variability: a widespread cortical phenomenon , 2010, Nature Neuroscience.

[29]  M. Kahana The Cognitive Correlates of Human Brain Oscillations , 2006, The Journal of Neuroscience.

[30]  Michael J Kahana,et al.  Sleep-dependent theta oscillations in the human hippocampus and neocortex. , 2003, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  M. D’Esposito,et al.  Directing the mind's eye: prefrontal, inferior and medial temporal mechanisms for visual working memory , 2005, Current Opinion in Neurobiology.

[32]  Miguel A. L. Nicolelis,et al.  Licking-Induced Synchrony in the Taste–Reward Circuit Improves Cue Discrimination during Learning , 2010, The Journal of Neuroscience.

[33]  V. Doyère,et al.  Long-term potentiation of hippocampal afferents and efferents to prefrontal cortex: Implications for associative learning , 1993, Neuropsychologia.

[34]  W. Singer,et al.  Neural Synchrony in Cortical Networks: History, Concept and Current Status , 2009, Front. Integr. Neurosci..

[35]  Michael E. Hasselmo,et al.  Modeling goal-directed spatial navigation in the rat based on physiological data from the hippocampal formation , 2003, Neural Networks.

[36]  A. Pérez-Villalba Rhythms of the Brain, G. Buzsáki. Oxford University Press, Madison Avenue, New York (2006), Price: GB £42.00, p. 448, ISBN: 0-19-530106-4 , 2008 .

[37]  Raul Vicente,et al.  Zero-lag long-range synchronization via dynamical relaying. , 2006, Physical review letters.

[38]  Michael E. Hasselmo,et al.  Working Memory Performance Correlates with Prefrontal-Hippocampal Theta Interactions but not with Prefrontal Neuron Firing Rates , 2009, Front. Integr. Neurosci..

[39]  R. Stickgold,et al.  Sleep-Dependent θ Oscillations in the Human Hippocampus and Neocortex , 2003, The Journal of Neuroscience.

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

[41]  M. Kahana,et al.  Theta returns , 2001, Current Opinion in Neurobiology.

[42]  G B Ermentrout,et al.  Fine structure of neural spiking and synchronization in the presence of conduction delays. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Stefano Boccaletti,et al.  Functional neural networks underlying semantic encoding of associative memories , 2010, NeuroImage.

[44]  Neil McNaughton,et al.  Coupling of theta oscillations between anterior and posterior midline cortex and with the hippocampus in freely behaving rats. , 2009, Cerebral cortex.

[45]  Robert P. Vertes,et al.  Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat , 2006, Neuroscience.

[46]  P. M. Wall,et al.  The hippocampal formation — orbitomedial prefrontal cortex circuit in the attentional control of active memory , 2001, Behavioural Brain Research.

[47]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.