Neural dynamics in a model of the thalamocortical system. I. Layers, loops and the emergence of fast synchronous rhythms.

A large-scale computer model was constructed to gain insight into the structural basis for the generation of fast synchronous rhythms (20-60 Hz) in the thalamocortical system. The model consisted of 65,000 spiking neurons organized topographically to represent sectors of a primary and secondary area of mammalian visual cortex, and two associated regions of the dorsal thalamus and the thalamic reticular nucleus. Cortical neurons, both excitatory and inhibitory, were organized in supragranular layers, infraganular layers and layer IV. Reciprocal intra- and interlaminar, interareal, thalamocortical, corticothalamic and thalamoreticular connections were set up based on known anatomical constraints. Simulations of neuronal responses to visual input revealed sporadic epochs of synchronous oscillations involving all levels of the model, similar to the fast rhythms recorded in vivo. By systematically modifying physiological and structural parameters in the model, specific network properties were found to play a major role in the generation of this rhythmic activity. For example, fast synchronous rhythms could be sustained autonomously by lateral and interlaminar interactions within and among local cortical circuits. In addition, these oscillations were propagated to the thalamus and amplified by corticothalamocortical loops, including the thalamic reticular complex. Finally, synchronous oscillations were differentially affected by lesioning forward and backward interareal connections.

[1]  V. Mountcastle Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

[2]  C. Galletti,et al.  Maintained activity of single neurons in striate and non-striate areas of the cat visual cortex. , 1973, Brain research.

[3]  P. Milner A model for visual shape recognition. , 1974, Psychological review.

[4]  C. Gilbert,et al.  Laminar patterns of geniculocortical projection in the cat , 1976, Brain Research.

[5]  B. Cleland,et al.  Organization of visual inputs to interneurons of lateral geniculate nucleus of the cat. , 1977, Journal of neurophysiology.

[6]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[7]  G. Henry,et al.  Neural path taken by afferent streams in striate cortex of the cat. , 1979, Journal of neurophysiology.

[8]  B. Connors,et al.  Electrophysiological properties of neocortical neurons in vitro. , 1982, Journal of neurophysiology.

[9]  J. Robson The morphology of corticofugal axons to the dorsal lateral geniculate nucleus in the cat , 1983, The Journal of comparative neurology.

[10]  M. Colonnier,et al.  The number of neurons in the different laminae of the binocular and monocular regions of area 17 in the cat , 1983, The Journal of comparative neurology.

[11]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  M. Colonnier,et al.  A laminar analysis of the number of round‐asymmetrical and flat‐symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat , 1985, The Journal of comparative neurology.

[13]  C. Legéndy,et al.  Bursts and recurrences of bursts in the spike trains of spontaneously active striate cortex neurons. , 1985, Journal of neurophysiology.

[14]  D. Whitteridge,et al.  Innervation of cat visual areas 17 and 18 by physiologically identified X‐ and Y‐ type thalamic afferents. I. Arborization patterns and quantitative distribution of postsynaptic elements , 1985, The Journal of comparative neurology.

[15]  W. Singer,et al.  Topographic organization of the orientation column system in large flat‐mounts of the cat visual cortex: A 2‐deoxyglucose study , 1987, The Journal of comparative neurology.

[16]  E Kaplan,et al.  Contrast affects the transmission of visual information through the mammalian lateral geniculate nucleus. , 1987, The Journal of physiology.

[17]  Ronald J. MacGregor,et al.  Neural and brain modeling , 1987 .

[18]  S. Shipp,et al.  The functional logic of cortical connections , 1988, Nature.

[19]  H. Swadlow Efferent neurons and suspected interneurons in binocular visual cortex of the awake rabbit: receptive fields and binocular properties. , 1988, Journal of neurophysiology.

[20]  S. Zeki,et al.  The Organization of Connections between Areas V5 and V2 in Macaque Monkey Visual Cortex , 1989, The European journal of neuroscience.

[21]  K. Rockland,et al.  Terminal arbors of individual “Feedback” axons projecting from area V2 to V1 in the macaque monkey: A study using immunohistochemistry of anterogradely transported Phaseolus vulgaris‐leucoagglutinin , 1989, The Journal of comparative neurology.

[22]  J. Kaas,et al.  Cortical integration of parallel pathways in the visual system of primates , 1989, Brain Research.

[23]  S. Zeki,et al.  Modular Connections between Areas V2 and V4 of Macaque Monkey Visual Cortex , 1989, The European journal of neuroscience.

[24]  R. Traub,et al.  Model of the origin of rhythmic population oscillations in the hippocampal slice. , 1989, Science.

[25]  J. Bullier,et al.  Visual activity in area V2 during reversible inactivation of area 17 in the macaque monkey. , 1989, Journal of neurophysiology.

[26]  R. Kalil,et al.  Synaptic connections between corticogeniculate axons and interneurons in the dorsal lateral geniculate nucleus of the cat , 1989, The Journal of comparative neurology.

[27]  Matthew A. Wilson,et al.  The simulation of large-scale neural networks , 1989 .

[28]  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.

[29]  B W Connors,et al.  Synchronized excitation and inhibition driven by intrinsically bursting neurons in neocortex. , 1989, Journal of neurophysiology.

[30]  N. Daw,et al.  The location and function of NMDA receptors in cat and kitten visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  Antonio R. Damasio,et al.  The Brain Binds Entities and Events by Multiregional Activation from Convergence Zones , 1989, Neural Computation.

[32]  B. Connors,et al.  Intrinsic firing patterns of diverse neocortical neurons , 1990, Trends in Neurosciences.

[33]  Nobuo Kato,et al.  Cortico-thalamo-cortical projection between visual cortices , 1990, Brain Research.

[34]  Jos J. Eggermont The Correlative Brain , 1990 .

[35]  Paul Antoine Salin,et al.  Projections from Areas 18 and 19 to Cat Striate Cortex: Divergence and Laminar Specificity , 1991, The European journal of neuroscience.

[36]  D. Whitteridge,et al.  An intracellular analysis of the visual responses of neurones in cat visual cortex. , 1991, The Journal of physiology.

[37]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[38]  P König,et al.  Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[39]  C. Gilbert,et al.  Synaptic physiology of horizontal connections in the cat's visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  G Tononi,et al.  Modeling perceptual grouping and figure-ground segregation by means of active reentrant connections. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[41]  R. Llinás,et al.  Of dreaming and wakefulness , 1991, Neuroscience.

[42]  D. Paré,et al.  Fast oscillations (20-40 Hz) in thalamocortical systems and their potentiation by mesopontine cholinergic nuclei in the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[43]  C. Koch,et al.  A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  K. Stratford,et al.  Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  R. Llinás,et al.  In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[46]  P A Salin,et al.  Visual activity in macaque area V4 depends on area 17 input. , 1991, Neuroreport.

[47]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[48]  Rodney J. Douglas,et al.  Synchronization of Bursting Action Potential Discharge in a Model Network of Neocortical Neurons , 1991, Neural Computation.

[49]  M. Cynader,et al.  Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). , 1992, Cerebral cortex.

[50]  G. Edelman,et al.  Reentry and the problem of integrating multiple cortical areas: simulation of dynamic integration in the visual system. , 1992, Cerebral cortex.

[51]  William H. Press,et al.  Numerical Recipes in C, 2nd Edition , 1992 .

[52]  Paul Antoine Salin,et al.  Spatial and temporal coherence in cortico-cortical connections: a cross-correlation study in areas 17 and 18 in the cat. , 1992, Visual neuroscience.

[53]  B. Sakmann,et al.  Fast and slow components of unitary EPSCs on stellate cells elicited by focal stimulation in slices of rat visual cortex. , 1992, The Journal of physiology.

[54]  U. Eysel,et al.  Cellular organization of reciprocal patchy networks in layer III of cat visual cortex (area 17) , 1992, Neuroscience.

[55]  D. Ferster,et al.  EPSP-IPSP interactions in cat visual cortex studied with in vivo whole- cell patch recording , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  J. Bower,et al.  Cortical oscillations and temporal interactions in a computer simulation of piriform cortex. , 1992, Journal of neurophysiology.

[57]  W. Singer,et al.  Synchronization of oscillatory neuronal responses in cat striate cortex: Temporal properties , 1992, Visual Neuroscience.

[58]  D. Perrett,et al.  Time course of neural responses discriminating different views of the face and head. , 1992, Journal of neurophysiology.

[59]  I. Módy,et al.  Differential activation of GABAA and GABAB receptors by spontaneously released transmitter. , 1992, Journal of neurophysiology.

[60]  K. Rockland,et al.  Configuration, in serial reconstruction, of individual axons projecting from area V2 to V4 in the macaque monkey. , 1992, Cerebral cortex.

[61]  Erik D. Lumer,et al.  Selective Attention to Perceptual Groups: the Phase Tracking Mechanism , 1992, Int. J. Neural Syst..

[62]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[63]  M. Deschenes,et al.  Voltage-dependent 40-Hz * oscillations in rat reticular thalamic neurons in vivo , 1992, Neuroscience.

[64]  B R Payne,et al.  Evidence for visual cortical area homologs in cat and macaque monkey. , 1993, Cerebral cortex.

[65]  A. Peters,et al.  Neuronal organization in area 17 of cat visual cortex. , 1993, Cerebral cortex.

[66]  E. G. Jones,et al.  GABAergic neurons and their role in cortical plasticity in primates. , 1993, Cerebral cortex.

[67]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[68]  U. Eysel,et al.  Functional and Structural Topography of Horizontal Inhibitory Connections in Cat Visual Cortex , 1993, The European journal of neuroscience.

[69]  C D Woody,et al.  Electrophysiological characterization of different types of neurons recorded in vivo in the motor cortex of the cat. II. Membrane parameters, action potentials, current-induced voltage responses and electrotonic structures. , 1993, Journal of neurophysiology.

[70]  R. Llinás,et al.  Coherent 40-Hz oscillation characterizes dream state in humans. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[71]  I. Módy,et al.  Characterization of synaptically elicited GABAB responses using patch‐clamp recordings in rat hippocampal slices. , 1993, The Journal of physiology.

[72]  W. Singer,et al.  Squint Affects Synchronization of Oscillatory Responses in Cat Visual Cortex , 1993, The European journal of neuroscience.

[73]  D. V. van Essen,et al.  A neurobiological model of visual attention and invariant pattern recognition based on dynamic routing of information , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[74]  D. Contreras,et al.  Electrophysiological properties of intralaminar thalamocortical cells discharging rhythmic (≈40 HZ) spike-bursts at ≈1000 HZ during waking and rapid eye movement sleep , 1993, Neuroscience.

[75]  B. Connors,et al.  Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[76]  G. Orban,et al.  Laminar distribution of NMDA receptors in cat and monkey visual cortex visualized by [3H]‐MK‐801 binding , 1993, The Journal of comparative neurology.

[77]  S. Bressler,et al.  Episodic multiregional cortical coherence at multiple frequencies during visual task performance , 1993, Nature.

[78]  A. Peters,et al.  Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. , 1993, Cerebral cortex.

[79]  C D Gilbert,et al.  Circuitry, architecture, and functional dynamics of visual cortex. , 1993, Cerebral cortex.

[80]  K. Rockland,et al.  Direct temporal-occipital feedback connections to striate cortex (V1) in the macaque monkey. , 1994, Cerebral cortex.

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

[82]  George L. Gerstein,et al.  Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex , 1994, Nature.

[83]  R. Eckhorn,et al.  Stimulus-specific fast oscillations at zero phase between visual areas V1 and V2 of awake monkey. , 1994, Neuroreport.

[84]  Y. Kang,et al.  Spatiotemporally differential inhibition of pyramidal cells in the cat motor cortex. , 1994, Journal of neurophysiology.

[85]  T. Bonhoeffer,et al.  Relationship Between Lateral Inhibitory Connections and the Topography of the Orientation Map in Cat Visual Cortex , 1994, The European journal of neuroscience.

[86]  J. C. Anderson,et al.  Polyneuronal innervation of spiny stellate neurons in cat visual cortex , 1994, The Journal of comparative neurology.

[87]  J. Rinzel,et al.  Synchronization properties of spindle oscillations in a thalamic reticular nucleus model. , 1994, Journal of neurophysiology.

[88]  H. Dinse,et al.  The timing of processing along the visual pathway in the cat. , 1994, Neuroreport.

[89]  Françoise Condé,et al.  Local circuit neurons immunoreactive for calretinin, calbindin D‐28k or parvalbumin in monkey prefronatal cortex: Distribution and morphology , 1994, The Journal of comparative neurology.

[90]  K. Rockland,et al.  Divergent feedback connections from areas V4 and TEO in the macaque , 1994, Visual Neuroscience.

[91]  Y. Kawaguchi Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[92]  P. Rakic A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution , 1995, Trends in Neurosciences.

[93]  S. Bressler Large-scale cortical networks and cognition , 1995, Brain Research Reviews.

[94]  S. Nelson,et al.  An emergent model of orientation selectivity in cat visual cortical simple cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[95]  J Bullier,et al.  Structural basis of cortical synchronization. II. Effects of cortical lesions. , 1995, Journal of neurophysiology.

[96]  T. Sejnowski,et al.  A selection model for motion processing in area MT of primates , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[97]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

[98]  M. Nicolelis,et al.  Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. , 1995, Science.

[99]  C. Koch,et al.  Recurrent excitation in neocortical circuits , 1995, Science.

[100]  P A Salin,et al.  Corticocortical connections in the visual system: structure and function. , 1995, Physiological reviews.

[101]  M Stemmler,et al.  Lateral interactions in primary visual cortex: a model bridging physiology and psychophysics. , 1995, Science.

[102]  P. Somogyi,et al.  Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons , 1995, Nature.

[103]  W. Singer,et al.  Long-range synchronization of oscillatory light responses in the cat retina and lateral geniculate nucleus , 1996, Nature.

[104]  D. Contreras,et al.  Synchronization of fast (30-40 Hz) spontaneous oscillations in intrathalamic and thalamocortical networks , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[105]  G. Orban,et al.  Model circuit of spiking neurons generating directional selectivity in simple cells. , 1996, Journal of neurophysiology.

[106]  G. Edelman,et al.  Neural dynamics in a model of the thalamocortical system. II. The role of neural synchrony tested through perturbations of spike timing. , 1997, Cerebral cortex.