Interactions between Core and Matrix Thalamocortical Projections in Human Sleep Spindle Synchronization

Sleep spindles are bursts of 11–15 Hz that occur during non-rapid eye movement sleep. Spindles are highly synchronous across the scalp in the electroencephalogram (EEG) but have low spatial coherence and exhibit low correlation with the EEG when simultaneously measured in the magnetoencephalogram (MEG). We developed a computational model to explore the hypothesis that the spatial coherence spindles in the EEG is a consequence of diffuse matrix projections of the thalamus to layer 1 compared with the focal projections of the core pathway to layer 4 recorded in the MEG. Increasing the fanout of thalamocortical connectivity in the matrix pathway while keeping the core pathway fixed led to increased synchrony of the spindle activity in the superficial cortical layers in the model. In agreement with cortical recordings, the latency for spindles to spread from the core to the matrix was independent of the thalamocortical fanout but highly dependent on the probability of connections between cortical areas.

[1]  D. Contreras,et al.  Mechanisms underlying the synchronizing action of corticothalamic feedback through inhibition of thalamic relay cells. , 1998, Journal of neurophysiology.

[2]  T. Sejnowski,et al.  Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. , 1996, Journal of neurophysiology.

[3]  T. Sejnowski,et al.  A model of spindle rhythmicity in the isolated thalamic reticular nucleus. , 1994, Journal of neurophysiology.

[4]  Y. Amitai,et al.  Propagating neuronal discharges in neocortical slices: computational and experimental study. , 1997, Journal of neurophysiology.

[5]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[6]  P. Schwindt,et al.  Modal gating of Na+ channels as a mechanism of persistent Na+ current in pyramidal neurons from rat and cat sensorimotor cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  D. Contreras,et al.  Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm. , 1996, The Journal of physiology.

[8]  Paul H. E. Tiesinga,et al.  A New Correlation-Based Measure of Spike Timing Reliability , 2002, Neurocomputing.

[9]  P. Nunez,et al.  Electric fields of the brain , 1981 .

[10]  M. Steriade,et al.  Brainstem Control of Wakefulness and Sleep , 1990, Springer US.

[11]  T. Sejnowski,et al.  Computational Models of Thalamocortical Augmenting Responses , 1998, The Journal of Neuroscience.

[12]  D. McCormick,et al.  Spindle waves are propagating synchronized oscillations in the ferret LGNd in vitro. , 1995, Journal of neurophysiology.

[13]  E. Halgren,et al.  Divergent Cortical Generators of MEG and EEG during Human Sleep Spindles Suggested by Distributed Source Modeling , 2010, PloS one.

[14]  E. G. Jones,et al.  The thalamic matrix and thalamocortical synchrony , 2001, Trends in Neurosciences.

[15]  R. Traub,et al.  A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. , 1991, Journal of neurophysiology.

[16]  T. Sejnowski,et al.  Origin of slow cortical oscillations in deafferented cortical slabs. , 2000, Cerebral cortex.

[17]  T. Sejnowski,et al.  Spatiotemporal Patterns of Spindle Oscillations in Cortex and Thalamus , 1997, The Journal of Neuroscience.

[18]  J R Huguenard,et al.  GABA(A)-receptor-mediated rebound burst firing and burst shunting in thalamus. , 1997, Journal of neurophysiology.

[19]  D. L. Bassett,et al.  ELECTRICAL ACTIVITY OF THE THALAMUS AND BASAL GANGLIA IN DECORTICATE CATS , 1946 .

[20]  T. Sejnowski,et al.  Model of Thalamocortical Slow-Wave Sleep Oscillations and Transitions to Activated States , 2002, The Journal of Neuroscience.

[21]  E. Halgren,et al.  Magnetoencephalography demonstrates multiple asynchronous generators during human sleep spindles. , 2010, Journal of neurophysiology.

[22]  R. Traub,et al.  Multiple Modes of Neuronal Population Activity Emerge after Modifying Specific Synapses in a Model of the CA3 Region of the Hippocampus , 1991, Annals of the New York Academy of Sciences.

[23]  J R Huguenard,et al.  A fast transient potassium current in thalamic relay neurons: kinetics of activation and inactivation. , 1991, Journal of neurophysiology.

[24]  G. Lawton Why do we sleep? , 2000, Nature Neuroscience.

[25]  D. McCormick,et al.  Cellular mechanisms of a synchronized oscillation in the thalamus. , 1993, Science.

[26]  F. D. Silva,et al.  Source localization of MEG sleep spindles and the relation to sources of alpha band rhythms , 2002, Clinical Neurophysiology.

[27]  K. Iramina,et al.  Source models of sleep spindles using MEG and EEG measurements , 2005, Brain Topography.

[28]  D. McCormick,et al.  Periodicity of Thalamic Synchronized Oscillations: the Role of Ca2+-Mediated Upregulation of Ih , 1998, Neuron.

[29]  D. McCormick,et al.  Properties of a hyperpolarization‐activated cation current and its role in rhythmic oscillation in thalamic relay neurones. , 1990, The Journal of physiology.

[30]  F. Clascá,et al.  Thalamic input to distal apical dendrites in neocortical layer 1 is massive and highly convergent. , 2009, Cerebral cortex.

[31]  R Llinás,et al.  Kinetic and stochastic properties of a persistent sodium current in mature guinea pig cerebellar Purkinje cells. , 1998, Journal of neurophysiology.

[32]  E. Halgren,et al.  Emergence of synchronous EEG spindles from asynchronous MEG spindles , 2011, Human brain mapping.

[33]  D. McCormick,et al.  What Stops Synchronized Thalamocortical Oscillations? , 1996, Neuron.

[34]  Maxime Bonjean,et al.  Corticothalamic Feedback Controls Sleep Spindle Duration In Vivo , 2011, The Journal of Neuroscience.

[35]  T. J. Sejnowski,et al.  Self–sustained rhythmic activity in the thalamic reticular nucleus mediated by depolarizing GABAA receptor potentials , 1999, Nature Neuroscience.

[36]  D Contreras,et al.  Mechanisms of long‐lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. , 1996, The Journal of physiology.

[37]  M Steriade,et al.  Spiking-bursting activity in the thalamic reticular nucleus initiates sequences of spindle oscillations in thalamic networks. , 2000, Journal of neurophysiology.

[38]  D. McCormick,et al.  Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. , 1992, Journal of neurophysiology.

[39]  R. Llinás,et al.  The functional states of the thalamus and the associated neuronal interplay. , 1988, Physiological reviews.

[40]  N Nakasato,et al.  Magnetic detection of sleep spindles in normal subjects. , 1990, Electroencephalography and clinical neurophysiology.

[41]  H. Barbas,et al.  Parallel Driving and Modulatory Pathways Link the Prefrontal Cortex and Thalamus , 2007, PloS one.

[42]  E. G. Jones,et al.  Thalamic circuitry and thalamocortical synchrony. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[43]  T. Sejnowski,et al.  Control of Spatiotemporal Coherence of a Thalamic Oscillation by Corticothalamic Feedback , 1996, Science.

[44]  Nima Dehghani,et al.  Topographical frequency dynamics within EEG and MEG sleep spindles , 2011, Clinical Neurophysiology.

[45]  I. Fried,et al.  Regional Slow Waves and Spindles in Human Sleep , 2011, Neuron.

[46]  T. Sejnowski,et al.  [Letters to nature] , 1996, Nature.

[47]  B N Cuffin,et al.  Relationship of the magnetoencephalogram to the electroencephalogram. Normal wake and sleep activity. , 1976, Electroencephalography and clinical neurophysiology.

[48]  A Babloyantz,et al.  A model of the inward current Ih and its possible role in thalamocortical oscillations. , 1993, Neuroreport.