Derivation and Analysis of Basic Computational Operations of Thalamocortical Circuits

Shared anatomical and physiological features of primary, secondary, tertiary, polysensory, and associational neocortical areas are used to formulate a novel extended hypothesis of thalamocortical circuit operation. A simplified anatomically based model of topographically and nontopographically projecting (core and matrix) thalamic nuclei, and their differential connections with superficial, middle, and deep neocortical laminae, is described. Synapses in the model are activated and potentiated according to physiologically based rules. Features incorporated into the models include differential time courses of excitatory versus inhibitory postsynaptic potentials, differential axonal arborization of pyramidal cells versus interneurons, and different laminar afferent and projection patterns. Observation of the model's responses to static and time-varying inputs indicates that topographic core circuits operate to organize stored memories into natural similarity-based hierarchies, whereas diffuse matrix circuits give rise to efficient storage of time-varying input into retrievable sequence chains. Examination of these operations shows their relationships with well-studied algorithms for related functions, including categorization via hierarchical clustering, and sequential storage via hash or scatter-storage. Analysis demonstrates that the derived thalamocortical algorithms exhibit desirable efficiency, scaling, and space and time cost characteristics. Implications of the hypotheses for central issues of perceptual reaction times and memory capacity are discussed. It is conjectured that the derived functions are fundamental building blocks recurrent throughout the neo cortex, which, through combination, gives rise to powerful perceptual, motor, and cognitive mechanisms.

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

[2]  B. Cragg The density of synapses and neurones in the motor and visual areas of the cerebral cortex. , 1967, Journal of anatomy.

[3]  Donald Ervin Knuth,et al.  The Art of Computer Programming , 1968 .

[4]  Dorothy S. Russell,et al.  Pathology of Tumours of the Nervous System , 1972 .

[5]  Ford F. Ebner,et al.  Two Different Types of Thalamocortical Projections to a Single Cortical Area in Mammals; pp. 141–155 , 1972 .

[6]  H. Killackey,et al.  Two different types of thalamocortical projections to a single cortical area in mammals. , 1972, Brain, behavior and evolution.

[7]  C. von der Malsburg Self-organization of orientation sensitive cells in the striate cortex. , 1973, Kybernetik.

[8]  H. Killackey,et al.  Convergent Projection of Three Separate Thalamic Nuclei on to a Single Cortical Area , 1973, Science.

[9]  H. Killackey,et al.  Differential telencephalic projections of the medial and ventral divisions of the medial geniculate body of the rat. , 1974, Brain research.

[10]  J. Szentágothai The ‘module-concept’ in cerebral cortex architecture , 1975, Brain Research.

[11]  A. Peters,et al.  An autoradiographic study of the projections from the lateral geniculate body of the rat , 1975, Brain Research.

[12]  D. Hubel,et al.  Ferrier lecture - Functional architecture of macaque monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[13]  T. Wiesel,et al.  Functional architecture of macaque monkey visual cortex , 1977 .

[14]  Vernon B Mountcastle,et al.  Brain Mechanisms for Directed Attention 1 , 1978, Journal of the Royal Society of Medicine.

[15]  Donald Ervin Knuth,et al.  The Art of Computer Programming, 2nd Ed. (Addison-Wesley Series in Computer Science and Information , 1978 .

[16]  T. Powell,et al.  The basic uniformity in structure of the neocortex. , 1980, Brain : a journal of neurology.

[17]  M. Herkenham Laminar organization of thalamic projections to the rat neocortex. , 1980, Science.

[18]  J. Kelly,et al.  Laminar connections of the cat's auditory cortex , 1981, Brain Research.

[19]  Jones Eg Functional subdivision and synaptic organization of the mammalian thalamus. , 1981 .

[20]  E. Jones Functional subdivision and synaptic organization of the mammalian thalamus. , 1981, International review of physiology.

[21]  E. Rosch,et al.  Categorization of Natural Objects , 1981 .

[22]  M. Colonnier,et al.  A laminar analysis of the number of neurons, glia, and synapses in the visual cortex (area 17) of adult macaque monkeys , 1982, The Journal of comparative neurology.

[23]  H. Swadlow Efferent systems of primary visual cortex: A review of structure and function , 1983, Brain Research Reviews.

[24]  D. B. Bender Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus , 1983, Brain Research.

[25]  Frank H. Duffy,et al.  Human cerebral potentials associated with REM sleep rapid eye movements: links to PGO waves and waking potentials , 1983, Brain Research.

[26]  Stephen M. Kosslyn,et al.  Pictures and names: Making the connection , 1984, Cognitive Psychology.

[27]  R. Rieck,et al.  Organization of the rostral thalamus in the rat: Evidence for connections to layer I of visual cortex , 1985, The Journal of comparative neurology.

[28]  N. Mizuno,et al.  Morphology and laminar organization of electrophysiologically identified neurons in the primary auditory cortex in the cat , 1985, The Journal of comparative neurology.

[29]  David Zipser,et al.  Feature Discovery by Competive Learning , 1986, Cogn. Sci..

[30]  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.

[31]  M. Herkenham,et al.  New Perspectives on the Organization and Evolution of Nonspecific Thalamocortical Projections , 1986 .

[32]  E Harth,et al.  The inversion of sensory processing by feedback pathways: a model of visual cognitive functions. , 1987, Science.

[33]  E. G. Jones,et al.  Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  J. Winer,et al.  Patterns of reciprocity in auditory thalamocortical and corticothalamic connections: Study with horseradish peroxidase and autoradiographic methods in the rat medial geniculate body , 1987, The Journal of comparative neurology.

[35]  KF Jensen,et al.  Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. I. The normal morphology of specific thalamocortical afferents , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  T. Teyler,et al.  Long-term potentiation. , 1987, Annual review of neuroscience.

[37]  J. Lund,et al.  Distribution of GABAergic neurons and axon terminals in the macaque striate cortex , 1987, The Journal of comparative neurology.

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

[39]  K Toyama,et al.  Long-term potentiation of synaptic transmission in kitten visual cortex. , 1988, Journal of neurophysiology.

[40]  A. Burkhalter,et al.  Intrinsic connections of rat primary visual cortex: Laminar organization of axonal projections , 1989, The Journal of comparative neurology.

[41]  E. G. Jones,et al.  Differential Calcium Binding Protein Immunoreactivity Distinguishes Classes of Relay Neurons in Monkey Thalamic Nuclei , 1989, The European journal of neuroscience.

[42]  Edward L. White,et al.  Triads: a synaptic network component in the cerebral cortex , 1989, Brain Research.

[43]  D. Whitteridge,et al.  Arborisation pattern and postsynaptic targets of physiologically identified thalamocortical afferents in striate cortex of the macaque monkey , 1989, The Journal of comparative neurology.

[44]  C. Stevens,et al.  NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus , 1989, Nature.

[45]  G Oakson,et al.  Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  J Ambros-Ingerson,et al.  Simulation of paleocortex performs hierarchical clustering. , 1990, Science.

[47]  Michael Conley,et al.  Organization of the Visual Sector of the Thalamic Reticular Nucleus in Galago , 1990, The European journal of neuroscience.

[48]  C Baumgartner,et al.  Laminar analysis of extracellular field potentials in rat vibrissa/barrel cortex. , 1990, Journal of neurophysiology.

[49]  D. McCormick,et al.  Functional implications of burst firing and single spike activity in lateral geniculate relay neurons , 1990, Neuroscience.

[50]  F. Crépel,et al.  Use‐dependent changes in synaptic efficacy in rat prefrontal neurons in vitro. , 1990, The Journal of physiology.

[51]  Richard Granger,et al.  Higher olfactory processes: perceptual learning and memory , 1991, Current Opinion in Neurobiology.

[52]  H. Groenewegen,et al.  Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat , 1991, Neuroscience.

[53]  Richard Granger,et al.  Behavioral Tests of a Prediction from a Cortical Network Simulation , 1991 .

[54]  Mario Wiesendanger,et al.  Patterns of corticothalamic terminations following injection of Phaseolus vulgaris leucoagglutinin (PHA-L) in the sensorimotor cortex of the rat , 1991, Neuroscience Letters.

[55]  E. Welker,et al.  Morphology of corticothalamic terminals arising from the auditory cortex of the rat: A Phaseolus vulgaris-leucoagglutinin (PHA-L) tracing study , 1991, Hearing Research.

[56]  A. Keller,et al.  Long-term potentiation of thalamic input to the motor cortex induced by coactivation of thalamocortical and corticocortical afferents. , 1991, Journal of neurophysiology.

[57]  J. DeFelipe,et al.  Parvalbumin immunoreactivity reveals layer IV of monkey cerebral cortex as a mosaic of microzones of thalamic afferent terminations , 1991, Brain Research.

[58]  Richard Granger,et al.  Short-Latency Single Unit Processing in Olfactory Cortex , 1991, Journal of Cognitive Neuroscience.

[59]  S. Sherman,et al.  Relative contributions of burst and tonic responses to the receptive field properties of lateral geniculate neurons in the cat. , 1992, Journal of neurophysiology.

[60]  E. G. Jones,et al.  Calbindin and parvalbumin cells in monkey VPL thalamic nucleus: distribution, laminar cortical projections, and relations to spinothalamic terminations , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  Richard Granger,et al.  A cortical model of winner-take-all competition via lateral inhibition , 1992, Neural Networks.

[62]  F. Ebner,et al.  Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: Dependence on the barrel field cortex , 1992, The Journal of comparative neurology.

[63]  F. Ebner,et al.  Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus , 1992, The Journal of comparative neurology.

[64]  C R Olson,et al.  Topographic organization of cortical and subcortical projections to posterior cingulate cortex in the cat: Evidence for somatic, ocular, and complex subregions , 1992, The Journal of comparative neurology.

[65]  T. Freund,et al.  gamma-Aminobutyric acid-containing basal forebrain neurons innervate inhibitory interneurons in the neocortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[66]  D Mumford,et al.  On the computational architecture of the neocortex. II. The role of cortico-cortical loops. , 1992, Biological cybernetics.

[67]  Mark F. Bear,et al.  Neocortical long-term potentiation , 1993, Current Opinion in Neurobiology.

[68]  Mircea Steriade,et al.  Central core modulation of spontaneous oscillations and sensory transmission in thalamocortical systems , 1993, Current Opinion in Neurobiology.

[69]  M A Gluck,et al.  Computational models of the neural bases of learning and memory. , 1993, Annual review of neuroscience.

[70]  E. White,et al.  Cortical modules in the posteromedial barrel subfield (Sml) of the mouse , 1993, The Journal of comparative neurology.

[71]  M. Bear,et al.  Common forms of synaptic plasticity in the hippocampus and neocortex in vitro. , 1993, Science.

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

[73]  J. Budd,et al.  A numerical analysis of the geniculocortical input to striate cortex in the monkey. , 1994, Cerebral cortex.

[74]  R Granger,et al.  Non-Hebbian properties of long-term potentiation enable high-capacity encoding of temporal sequences. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[75]  Thierry Bal,et al.  Sensory gating mechanisms of the thalamus , 1994, Current Opinion in Neurobiology.

[76]  D. Prince,et al.  Clonazepam suppresses GABAB-mediated inhibition in thalamic relay neurons through effects in nucleus reticularis. , 1994, Journal of neurophysiology.

[77]  T. Teyler,et al.  Laminar pattern of synaptic activity in rat primary visual cortex: comparison of in vivo and in vitro studies employing the current source density analysis , 1994, Brain Research.

[78]  H. Asanuma,et al.  Long-term potentiation within the cat motor cortex. , 1994, Neuroreport.

[79]  M. Molinari,et al.  Chemical Compartmentation and Relationships between Calcium‐binding Protein Immunoreactivity and Layer‐specific Cortical and Caudate‐projecting Cells in the Anterior Intralaminar Nuclei of the Cat , 1994, The European journal of neuroscience.

[80]  Richard Granger,et al.  Sparse random networks with LTP learning rules approximate Bayes classifiers via Parzen's method , 1994, Neural Networks.

[81]  Richard Granger,et al.  Learning and Classification in a Noisy Environment by a Simulated Cortical Network , 1995 .

[82]  B. Connors,et al.  Properties of excitatory synaptic events in neurons of primary somatosensory cortex of neonatal rats. , 1995, Cerebral cortex.

[83]  J. Donoghue,et al.  Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[84]  E. Kaplan,et al.  Dynamics of neurons in the cat lateral geniculate nucleus: in vivo electrophysiology and computational modeling. , 1995, Journal of neurophysiology.

[85]  T. van Groen,et al.  Projections from the anterodorsal and anteroveniral nucleus of the thalamus to the limbic cortex in the rat , 1995, The Journal of comparative neurology.

[86]  D Contreras,et al.  Relations between cortical and thalamic cellular events during transition from sleep patterns to paroxysmal activity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[87]  S. Sherman,et al.  Receiver operating characteristic (ROC) analysis of neurons in the cat's lateral geniculate nucleus during tonic and burst response mode , 1995, Visual Neuroscience.

[88]  J. Bourassa,et al.  Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer , 1995, Neuroscience.

[89]  M. Molinari,et al.  Auditory thalamocortical pathways defined in monkeys by calcium‐binding protein immunoreactivity , 1995, The Journal of comparative neurology.

[90]  T. Freund,et al.  Interneurons Containing Calretinin Are Specialized to Control Other Interneurons in the Rat Hippocampus , 1996, The Journal of Neuroscience.

[91]  J. Donoghue,et al.  Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex. , 1996, Journal of neurophysiology.

[92]  Richard Granger,et al.  Effects of LTP on Response Selectivity of Simulated Cortical Neurons , 1996, Journal of Cognitive Neuroscience.

[93]  Robert Miller,et al.  Cortico-thalamic interplay and the security of operation of neural assemblies and temporal chains in the cerebral cortex , 1996, Biological Cybernetics.

[94]  Richard Granger,et al.  An algorithm derived from thalamocortical circuitry stores and retrieves temporal sequences , 1996, Proceedings of 13th International Conference on Pattern Recognition.

[95]  G Lynch,et al.  Distinct memory circuits composing the hippocampal region , 1996, Hippocampus.

[96]  H. Barbas,et al.  Cortical structure predicts the pattern of corticocortical connections. , 1997, Cerebral cortex.

[97]  R W Guillery,et al.  Quantification without pontification: Choosing a method for counting objects in sectioned tissues , 1997, The Journal of comparative neurology.

[98]  D. Prince,et al.  Nucleus reticularis neurons mediate diverse inhibitory effects in thalamus. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[99]  M. Steriade Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. , 1997, Cerebral cortex.

[100]  K. Martin,et al.  Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat , 1997, The Journal of comparative neurology.

[101]  Stanislaw Sobotka,et al.  Saccadic eye movements, even in darkness, generate event-related potentials recorded in medial septum and medial temporal cortex , 1997, Brain Research.

[102]  D. Prince,et al.  GABAA receptor-mediated Cl- currents in rat thalamic reticular and relay neurons. , 1997, Journal of neurophysiology.

[103]  B. Connors,et al.  THALAMOCORTICAL SYNAPSES , 1997, Progress in Neurobiology.

[104]  M. Mishkin,et al.  Serial and parallel processing in rhesus monkey auditory cortex , 1997, The Journal of comparative neurology.

[105]  F. Schlaghecken On Processing BEASTS and BIRDS: An Event-Related Potential Study on the Representation of Taxonomic Structure , 1998, Brain and Language.

[106]  M M Merzenich,et al.  Optical imaging and electrophysiology of rat barrel cortex. I. Responses to small single-vibrissa deflections. , 1998, Cerebral cortex.

[107]  D. Buonomano,et al.  Cortical plasticity: from synapses to maps. , 1998, Annual review of neuroscience.

[108]  P. Reber,et al.  Contrasting cortical activity associated with category memory and recognition memory. , 1998, Learning & memory.

[109]  K. Murakami,et al.  An ultrastructural study of the neural circuit between the prefrontal cortex and the mediodorsal nucleus of the thalamus , 1998, Progress in Neurobiology.

[110]  G. Buzsáki,et al.  Gamma Oscillations in the Entorhinal Cortex of the Freely Behaving Rat , 1998, The Journal of Neuroscience.

[111]  L. Squire,et al.  Encapsulation of Implicit and Explicit Memory in Sequence Learning , 1998, Journal of Cognitive Neuroscience.

[112]  Martin Deschênes,et al.  The organization of corticothalamic projections: reciprocity versus parity , 1998, Brain Research Reviews.

[113]  E. G. Jones,et al.  A new view of specific and nonspecific thalamocortical connections. , 1998, Advances in neurology.

[114]  Jones Eg A new view of specific and nonspecific thalamocortical connections. , 1998 .

[115]  T. Freund,et al.  Enkephalin‐containing interneurons are specialized to innervate other interneurons in the hippocampal CA1 region of the rat and guinea‐pig , 1998, The European journal of neuroscience.

[116]  P. V. Rayudu,et al.  Increased NMDA current and spine density in mice lacking the NMDA receptor subunit NR3A , 1998, Nature.

[117]  P J Reber,et al.  Cortical areas supporting category learning identified using functional MRI. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[118]  Prof. Dr. Dr. Valentino Braitenberg,et al.  Cortex: Statistics and Geometry of Neuronal Connectivity , 1998, Springer Berlin Heidelberg.

[119]  M. Sarter,et al.  Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents , 1999, Neuroscience.

[120]  D. Contreras,et al.  Cortically-induced coherence of a thalamic-generated oscillation , 1999, Neuroscience.

[121]  E. G. Jones,et al.  Predominance of corticothalamic synaptic inputs to thalamic reticular nucleus neurons in the rat , 1999, The Journal of comparative neurology.

[122]  T. Freund,et al.  Total Number and Ratio of Excitatory and Inhibitory Synapses Converging onto Single Interneurons of Different Types in the CA1 Area of the Rat Hippocampus , 1999, The Journal of Neuroscience.

[123]  C. Koch,et al.  Encoding of visual information by LGN bursts. , 1999, Journal of neurophysiology.

[124]  B. Connors,et al.  Intrinsic firing patterns and whisker-evoked synaptic responses of neurons in the rat barrel cortex. , 1999, Journal of neurophysiology.

[125]  C. Bartheld Systematic bias in an “unbiased” neuronal counting technique , 1999 .

[126]  R. Reep,et al.  Topographic organization of the striatal and thalamic connections of rat medial agranular cortex , 1999, Brain Research.

[127]  G. Recanzone,et al.  Frequency and intensity response properties of single neurons in the auditory cortex of the behaving macaque monkey. , 2000, Journal of neurophysiology.

[128]  R. Linke,et al.  Convergent and complementary projections of the caudal paralaminar thalamic nuclei to rat temporal and insular cortex. , 2000, Cerebral cortex.

[129]  Keiji Tanaka,et al.  Connections between Anterior Inferotemporal Cortex and Superior Temporal Sulcus Regions in the Macaque Monkey , 2000, The Journal of Neuroscience.

[130]  W. Singer,et al.  Interhemispheric asymmetries of the modular structure in human temporal cortex. , 2000, Science.

[131]  M S Gazzaniga Regional Differences in Cortical Organization , 2000, Science.

[132]  J. Magee,et al.  Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons , 2000, Nature Neuroscience.

[133]  J. Winer,et al.  Auditory thalamocortical projections in the cat: Laminar and areal patterns of input , 2000, The Journal of comparative neurology.

[134]  J. Donoghue,et al.  Learning-induced LTP in neocortex. , 2000, Science.

[135]  J. Magee Dendritic integration of excitatory synaptic input , 2000, Nature Reviews Neuroscience.

[136]  G Lynch,et al.  Origins and Distribution of Cholinergically Induced β Rhythms in Hippocampal Slices , 2000, The Journal of Neuroscience.

[137]  C. Bartheld Comparison of 2-D and 3-D counting: the need for calibration and common sense , 2001, Trends in Neurosciences.

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

[139]  Mark F. Bear,et al.  Long-Term Potentiation of Thalamocortical Transmission in the Adult Visual Cortex In Vivo , 2001, The Journal of Neuroscience.

[140]  Patricia K. Kuhl,et al.  Language/Culture/Mind/Brain , 2001, Annals of the New York Academy of Sciences.

[141]  B Sakmann,et al.  AMPA Receptor Channels with Long-Lasting Desensitization in Bipolar Interneurons Contribute to Synaptic Depression in a Novel Feedback Circuit in Layer 2/3 of Rat Neocortex , 2001, The Journal of Neuroscience.

[142]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[143]  Katsuei Shibuki,et al.  Sequence dependence of post‐tetanic potentiation after sequential heterosynaptic stimulation in the rat auditory cortex , 2001, The Journal of physiology.

[144]  L. Cauller,et al.  Corticocortical and thalamocortical projections to layer I of the frontal neocortex in rats , 2001, Brain Research.

[145]  S. Sherman Tonic and burst firing: dual modes of thalamocortical relay , 2001, Trends in Neurosciences.

[146]  J. Bullier,et al.  Cortical mapping of gamma oscillations in areas V1 and V4 of the macaque monkey , 2001, Visual Neuroscience.

[147]  J. Kaas,et al.  Areal and callosal connections in the somatosensory cortex of the star-nosed mole. , 2001, Somatosensory & motor research.

[148]  S. Raghavachari,et al.  Distinct patterns of brain oscillations underlie two basic parameters of human maze learning. , 2001, Journal of neurophysiology.

[149]  W. Singer,et al.  Rapid feature selective neuronal synchronization through correlated latency shifting , 2001, Nature Neuroscience.

[150]  K. Rockland,et al.  Parvalbumin positive dendrites co-localize with apical dendritic bundles in rat retrosplenial cortex , 2002, Neuroreport.

[151]  [Structure of the cerebral cortex. Intrinsic organization and comparative analysis of the neocortex]. , 2002, Revista de neurologia.

[152]  Richard Granger,et al.  Identification of Diagnostic Evoked Response Potential Segments in Alzheimer's Disease , 2002, Experimental Neurology.

[153]  H. Swadlow,et al.  Activation of a Cortical Column by a Thalamocortical Impulse , 2002, The Journal of Neuroscience.

[154]  Jiankun Cui,et al.  Temporal and regional expression of NMDA receptor subunit NR3A in the mammalian brain , 2002, The Journal of comparative neurology.

[155]  K. Rockland,et al.  The pyramidal cell of the sensorimotor cortex of the macaque monkey: phenotypic variation. , 2002, Cerebral cortex.

[156]  K. Rockland Visual cortical organization at the single axon level: a beginning , 2002, Neuroscience Research.

[157]  H. Markram,et al.  Stereotypy in neocortical microcircuits , 2002, Trends in Neurosciences.

[158]  A. Graybiel,et al.  Shifts in striatal responsivity evoked by chronic stimulation of dopamine and glutamate systems. , 2002, Brain : a journal of neurology.

[159]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

[160]  Christoph E Schreiner,et al.  Functional architecture of auditory cortex , 2002, Current Opinion in Neurobiology.

[161]  Günther Palm,et al.  Scene segmentation by spike synchronization in reciprocally connected visual areas. I. Local effects of cortical feedback , 2002, Biological Cybernetics.

[162]  Richard Granger,et al.  Olfactory cortex as a model for telencephalic processing , 2002 .

[163]  Henry Kennedy,et al.  Early specification of the hierarchical organization of visual cortical areas in the macaque monkey. , 2002, Cerebral cortex.

[164]  J. Movshon,et al.  The Timing of Response Onset and Offset in Macaque Visual Neurons , 2002, The Journal of Neuroscience.

[165]  O. D. Creutzfeldt,et al.  Representation of complex visual stimuli in the brain , 1978, Naturwissenschaften.

[166]  E. G. Jones,et al.  The distribution of intrinsic cortical axons in area 3b of cat primary somatosensory cortex , 2004, Experimental Brain Research.

[167]  L. M. Kitzes,et al.  Intrinsic inter- and intralaminar connections and their relationship to the tonotopic map in cat primary auditory cortex , 2004, Experimental Brain Research.

[168]  S. Grossberg,et al.  Adaptive pattern classification and universal recoding: I. Parallel development and coding of neural feature detectors , 1976, Biological Cybernetics.

[169]  Stephen Grossberg,et al.  Adaptive pattern classification and universal recoding: II. Feedback, expectation, olfaction, illusions , 1976, Biological Cybernetics.

[170]  K. Shibuki,et al.  Long-term potentiation of supragranular pyramidal outputs in the rat auditory cortex , 1996, Experimental Brain Research.

[171]  Richard Granger,et al.  Computation of frequency-to-spatial transform by olfactory bulb glomeruli , 2004, Biological Cybernetics.

[172]  D. Mumford On the computational architecture of the neocortex , 2004, Biological Cybernetics.

[173]  M. Scheel Topographic organization of the auditory thalamocortical system in the albino rat , 2004, Anatomy and Embryology.

[174]  Terrence J. Sejnowski,et al.  Inhibition synchronizes sparsely connected cortical neurons within and between columns in realistic network models , 1996, Journal of Computational Neuroscience.

[175]  D. Glahn,et al.  Magnetic resonance findings in bipolar disorder. , 2005, The Psychiatric clinics of North America.