Functional Maps of Neocortical Local Circuitry

This review aims to summarize data obtained with different techniques to provide a functional map of the local circuit connections made by neocortical neurones, a reference for those interested in cortical circuitry and the numerical information required by those wishing to model the circuit. A brief description of the main techniques used to study circuitry is followed by outline descriptions of the major classes of neocortical excitatory and inhibitory neurones and the connections that each layer makes with other cortical and subcortical regions. Maps summarizing the projection patterns of each class of neurone within the local circuit and tables of the properties of these local circuit connections are provided. This review relies primarily on anatomical studies that have identified the classes of neurones and their local and long distance connections and on paired intracellular and whole-cell recordings which have documented the properties of the connections between them. A large number of different types of synaptic connections have been described, but for some there are only a few published examples and for others the details that can only be obtained with paired recordings and dye-filling are lacking. A further complication is provided by the range of species, technical approaches and age groups used in these studies. Wherever possible the range of available data are summarised and compared. To fill some of the more obvious gaps for the less well-documented cases, data obtained with other methods are also summarized.

[1]  J. Tigges,et al.  Subcortical projections, cortical associations, and some intrinsic interlaminar connections of the striate cortex in the squirrel monkey (Saimiri) , 1970, The Journal of comparative neurology.

[2]  J. Lund Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta) , 1973, The Journal of comparative neurology.

[3]  F. Valverde Aspects of cortical organization related to the geometry of neurons with intra-cortical axons , 1976, Journal of neurocytology.

[4]  P. Somogyi A specific ‘axo-axonal’ interneuron in the visual cortex of the rat , 1977, Brain Research.

[5]  J G Parnavelas,et al.  Organization of neurons in the visual cortex, area 17, of the rat. , 1977, Journal of anatomy.

[6]  A. Peters,et al.  The forms of non‐pyramidal neurons in the visual cortex of the rat , 1978, The Journal of comparative neurology.

[7]  E. White,et al.  Thalamocortical synapses involving identified neurons in mouse primary somatosensory cortex: A terminal degeneration and golgi/EM study , 1981, The Journal of comparative neurology.

[8]  E. White,et al.  Quantification of synapses formed with apical dendrites of golgi-impregnated pyramidal cells: Variability in thalamocortical inputs, but consistency in the ratios of asymmetrical to symmetrical synapses , 1981, Neuroscience.

[9]  E. White,et al.  Thalamocortical synapses of pyramidal cells which project from SmI to MsI cortex in the mouse , 1981, The Journal of comparative neurology.

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

[11]  E. White,et al.  A quantitative study of thalamocortical and other synapses involving the apical dendrites of corticothalamic projection cells in mouse SmI cortex , 1982, Journal of neurocytology.

[12]  C. Gilbert Microcircuitry of the visual cortex. , 1983, Annual review of neuroscience.

[13]  T. Wiesel,et al.  Clustered intrinsic connections in cat visual cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Alan Peters,et al.  Cellular components of the cerebral cortex , 1984 .

[15]  T. Wiesel,et al.  Patterns of synaptic input to layer 4 of cat striate cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  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.

[17]  D. Whitteridge,et al.  Innervation of cat visual areas 17 and 18 by physiologically identified X‐ and Y‐ type thalamic afferents. II. Identification of postsynaptic targets by GABA immunocytochemistry and Golgi impregnation , 1985, The Journal of comparative neurology.

[18]  E. White,et al.  Synaptic connections of callosal projection neurons in the vibrissal region of mouse primary motor cortex: An electron microscopic/horseradish peroxidase study , 1986, The Journal of comparative neurology.

[19]  P. Somogyi,et al.  Synaptic connections, axonal and dendritic patterns of neurons immunoreactive for cholecystokinin in the visual cortex of the cat , 1986, Neuroscience.

[20]  E. White,et al.  Quantification of thalamocortical synapses with spiny stellate neurons in layer IV of mouse somatosensory cortex , 1986, The Journal of comparative neurology.

[21]  A. Cowey,et al.  Synaptic relationships of a type of GABA-immunoreactive neuron (clutch cell), spiny stellate cells and lateral geniculate nucleus afferents in layer IVC of the monkey striate cortex , 1986, Neuroscience.

[22]  J. Lund Local circuit neurons of macaque monkey striate cortex: I. Neurons of laminae 4C and 5A , 1987, The Journal of comparative neurology.

[23]  E. White,et al.  Intrinsic circuitry involving the local axon collaterals of corticothalamic projection cells in mouse SmI cortex , 1987, The Journal of comparative neurology.

[24]  L C Katz,et al.  Local circuitry of identified projection neurons in cat visual cortex brain slices , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  B. Schofield,et al.  Dendritic morphology and axon collaterals of corticotectal, corticopontine, and callosal neurons in layer V of primary visual cortex of the hooded rat , 1988, The Journal of comparative neurology.

[26]  J. Lund,et al.  Anatomical organization of macaque monkey striate visual cortex. , 1988, Annual review of neuroscience.

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

[28]  J. Bolz,et al.  Morphological types of projection neurons in layer 5 of cat visual cortex , 1990, The Journal of comparative neurology.

[29]  E. White,et al.  Intrinsic circuitry: Synapses involving the local axon collaterals of corticocortical projection neurons in the mouse primary somatosensory cortex , 1990, The Journal of comparative neurology.

[30]  P. Somogyi,et al.  Synapses, axonal and dendritic patterns of GABA-immunoreactive neurons in human cerebral cortex. , 1990, Brain : a journal of neurology.

[31]  J. Lund,et al.  Heterogeneity of chandelier neurons in monkey neocortex: Corticotropin‐releasing factor‐and parvalbumin‐immunoreactive populations , 1990, The Journal of comparative neurology.

[32]  E. White,et al.  Synapses made by axons of callosal projection neurons in mouse somatosensory cortex: Emphasis on intrinsic connections , 1991, The Journal of comparative neurology.

[33]  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.

[34]  J. Lund,et al.  Local circuit neurons of macaque monkey striate cortex: III. Neurons of laminae 4B, 4A, and 3B , 1997, The Journal of comparative neurology.

[35]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[36]  E. Callaway,et al.  Photostimulation using caged glutamate reveals functional circuitry in living brain slices. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[37]  A. Thomson,et al.  Fluctuations in pyramid-pyramid excitatory postsynaptic potentials modified by presynaptic firing pattern and postsynaptic membrane potential using paired intracellular recordings in rat neocortex , 1993, Neuroscience.

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

[39]  J. B. Levitt,et al.  Topography of pyramidal neuron intrinsic connections in macaque monkey prefrontal cortex (areas 9 and 46) , 1993, The Journal of comparative neurology.

[40]  J. Deuchars,et al.  Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self-facilitation, mediated postsynaptically. , 1993, Journal of neurophysiology.

[41]  Y. Kawaguchi,et al.  Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. , 1993, Journal of neurophysiology.

[42]  Y. Kubota,et al.  Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. , 1993, Journal of neurophysiology.

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

[44]  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.

[45]  J. B. Levitt,et al.  Intrinsic cortical connections in macaque visual area V2: Evidence for interaction between different functional streams , 1994, The Journal of comparative neurology.

[46]  J Deuchars,et al.  Relationships between morphology and physiology of pyramid‐pyramid single axon connections in rat neocortex in vitro. , 1994, The Journal of physiology.

[47]  C. Blakemore,et al.  Pyramidal neurons in layer 5 of the rat visual cortex. I. Correlation among cell morphology, intrinsic electrophysiological properties, and axon targets , 1994, The Journal of comparative neurology.

[48]  J. B. Levitt,et al.  Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: Anatomy of interlaminar projections , 1994, Visual Neuroscience.

[49]  P. Goldman-Rakic,et al.  Intrinsic circuit organization of the major layers and sublayers of the dorsolateral prefrontal cortex in the rhesus monkey , 1995, The Journal of comparative neurology.

[50]  J. Deuchars,et al.  Properties of single axon excitatory postsynaptic potentials elicited in spiny interneurons by action potentials in pyramidal neurons in slices of rat neocortex , 1995, Neuroscience.

[51]  I Fujita,et al.  Intrinsic connections in the macaque inferior temporal cortex , 1996, The Journal of comparative neurology.

[52]  E. Callaway,et al.  Contributions of individual layer 6 pyramidal neurons to local circuitry in macaque primary visual cortex , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  K. Zilles,et al.  Distribution of GABAergic Elements Postsynaptic to Ventroposteromedial Thalamic Projections in Layer IV of Rat Barrel Cortex , 1996, The European journal of neuroscience.

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

[55]  J. Deuchars,et al.  Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. , 1996, The Journal of physiology.

[56]  P. Somogyi,et al.  Effect, number and location of synapses made by single pyramidal cells onto aspiny interneurones of cat visual cortex. , 1997, The Journal of physiology.

[57]  Y. Kubota,et al.  GABAergic cell subtypes and their synaptic connections in rat frontal cortex. , 1997, Cerebral cortex.

[58]  Javier DeFelipe,et al.  Double bouquet cell axons in the human temporal neocortex: relationship to bundles of myelinated axons and colocalization of calretinin and calbindin D-28k immunoreactivities , 1997, Journal of Chemical Neuroanatomy.

[59]  Geniculo-cortical afferents form synaptic contacts with vasoactive intestinal polypeptide (VIP) immunoreactive neurons of the rat visual cortex , 1997, Neuroscience Letters.

[60]  H. Markram A network of tufted layer 5 pyramidal neurons. , 1997, Cerebral cortex.

[61]  K. Zilles,et al.  Interneurons Immunoreactive for Vasoactive Intestinal Polypeptide (VIP) are Extensively Innervated by Parvalbumin‐Containing Boutons in Rat Primary Somatosensory Cortex , 1997, The European journal of neuroscience.

[62]  H. Markram,et al.  Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. , 1997, The Journal of physiology.

[63]  P. Somogyi,et al.  Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. , 1997, The Journal of physiology.

[64]  Paul Leonard Gabbott,et al.  Local‐circuit neurones in the medial prefrontal cortex (areas 25, 32 and 24b) in the rat: Morphology and quantitative distribution , 1997, The Journal of comparative neurology.

[65]  A. Thomson Activity‐dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro , 1997, The Journal of physiology.

[66]  M. Deschenes,et al.  Projections to layer VI of the posteromedial barrel field in the rat: a reappraisal of the role of corticothalamic pathways. , 1998, Cerebral cortex.

[67]  A. Thomson,et al.  Postsynaptic pyramidal target selection by descending layer III pyramidal axons: dual intracellular recordings and biocytin filling in slices of rat neocortex , 1998, Neuroscience.

[68]  H. Markram,et al.  Differential signaling via the same axon of neocortical pyramidal neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[69]  P. Somogyi,et al.  Differentially Interconnected Networks of GABAergic Interneurons in the Visual Cortex of the Cat , 1998, The Journal of Neuroscience.

[70]  Y. Kubota,et al.  Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex , 1998, Neuroscience.

[71]  C. A. Gallagher,et al.  Ascending Projections of Simple and Complex Cells in Layer 6 of the Cat Striate Cortex , 1998, The Journal of Neuroscience.

[72]  E. G. Jones,et al.  Viewpoint: the core and matrix of thalamic organization , 1998, Neuroscience.

[73]  J. Rossier,et al.  Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex , 1998, The European journal of neuroscience.

[74]  Y. Frégnac,et al.  Visual input evokes transient and strong shunting inhibition in visual cortical neurons , 1998, Nature.

[75]  P. Somogyi,et al.  Target-cell-specific facilitation and depression in neocortical circuits , 1998, Nature Neuroscience.

[76]  J J Jack,et al.  Synaptic interactions between smooth and spiny neurones in layer 4 of cat visual cortex in vitro , 1998, The Journal of physiology.

[77]  K. Rockland,et al.  Single axon analysis of pulvinocortical connections to several visual areas in the Macaque , 1999, The Journal of comparative neurology.

[78]  Ken Mackie,et al.  Presynaptically Located CB1 Cannabinoid Receptors Regulate GABA Release from Axon Terminals of Specific Hippocampal Interneurons , 1999, The Journal of Neuroscience.

[79]  J. Lübke,et al.  Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single ‘barrel’ of developing rat somatosensory cortex , 1999, The Journal of physiology.

[80]  K. Martin,et al.  Intracortical excitation of spiny neurons in layer 4 of cat striate cortex in vitro. , 1999, Cerebral cortex.

[81]  B. Sakmann,et al.  Developmental Switch in the Short-Term Modification of Unitary EPSPs Evoked in Layer 2/3 and Layer 5 Pyramidal Neurons of Rat Neocortex , 1999, The Journal of Neuroscience.

[82]  K. Harris,et al.  Slices Have More Synapses than Perfusion-Fixed Hippocampus from both Young and Mature Rats , 1999, The Journal of Neuroscience.

[83]  M. C. Angulo,et al.  Postsynaptic glutamate receptors and integrative properties of fast-spiking interneurons in the rat neocortex. , 1999, Journal of neurophysiology.

[84]  A. Destexhe,et al.  Dual intracellular recordings and computational models of slow inhibitory postsynaptic potentials in rat neocortical and hippocampal slices , 1999, Neuroscience.

[85]  Alex M. Thomson,et al.  Molecular frequency filters at central synapses , 2000, Progress in Neurobiology.

[86]  Alex M Thomson,et al.  Double immunofluorescence, peroxidase labelling and ultrastructural analysis of interneurones following prolonged electrophysiological recordings in vitro , 2000, Journal of Neuroscience Methods.

[87]  R. Yuste,et al.  Optical probing of neuronal circuits with calcium indicators. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[88]  K. Rockland,et al.  Feedback connections from area MT of the squirrel monkey to areas V1 and V2 , 2000, The Journal of comparative neurology.

[89]  B. Sakmann,et al.  The Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex , 2000, The Journal of Neuroscience.

[90]  H. Markram,et al.  Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. , 2000, Science.

[91]  R. Traub,et al.  Neuronal fast oscillations as a target site for psychoactive drugs. , 2000, Pharmacology & therapeutics.

[92]  A. Agmon,et al.  Diverse Types of Interneurons Generate Thalamus-Evoked Feedforward Inhibition in the Mouse Barrel Cortex , 2001, The Journal of Neuroscience.

[93]  J. Rossier,et al.  Kainate Receptors Regulate Unitary IPSCs Elicited in Pyramidal Cells by Fast-Spiking Interneurons in the Neocortex , 2001, The Journal of Neuroscience.

[94]  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.

[95]  R. Kötter,et al.  Layer-Specific Intracolumnar and Transcolumnar Functional Connectivity of Layer V Pyramidal Cells in Rat Barrel Cortex , 2001, The Journal of Neuroscience.

[96]  D. Contreras,et al.  Voltage-Sensitive Dye Imaging of Neocortical Spatiotemporal Dynamics to Afferent Activation Frequency , 2001, The Journal of Neuroscience.

[97]  B. Connors,et al.  Short-term dynamics of thalamocortical and intracortical synapses onto layer 6 neurons in neocortex. , 2002, Journal of neurophysiology.

[98]  H. Markram,et al.  Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. , 2002, Cerebral cortex.

[99]  Yun Wang,et al.  Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. , 2002, Cerebral cortex.

[100]  R. Silver,et al.  Synaptic connections between layer 4 spiny neurone‐ layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column , 2002, The Journal of physiology.

[101]  G. Tamás,et al.  Identified Sources and Targets of Slow Inhibition in the Neocortex , 2003, Science.

[102]  J. Lübke,et al.  Morphometric analysis of the columnar innervation domain of neurons connecting layer 4 and layer 2/3 of juvenile rat barrel cortex. , 2003, Cerebral cortex.

[103]  Alex M Thomson,et al.  Presynaptic frequency filtering in the gamma frequency band; dual intracellular recordings in slices of adult rat and cat neocortex. , 2003, Cerebral cortex.

[104]  M. Whittington,et al.  A Novel Network of Multipolar Bursting Interneurons Generates Theta Frequency Oscillations in Neocortex , 2003, Neuron.

[105]  B. Connors,et al.  Two dynamically distinct inhibitory networks in layer 4 of the neocortex. , 2003, Journal of neurophysiology.

[106]  T. Harkany,et al.  Pyramidal cell communication within local networks in layer 2/3 of rat neocortex , 2003, The Journal of physiology.

[107]  Afia B Ali,et al.  Involvement of post‐synaptic kainate receptors during synaptic transmission between unitary connections in rat neocortex , 2003, The European journal of neuroscience.

[108]  D. Whitteridge,et al.  Synaptic targets of HRP-filled layer III pyramidal cells in the cat striate cortex , 2004, Experimental Brain Research.

[109]  Jochen F. Staiger,et al.  Recurrent axon collaterals of corticothalamic projection neurons in rat primary somatosensory cortex contribute to excitatory and inhibitory feedback-loops , 1996, Anatomy and Embryology.

[110]  H. Markram,et al.  Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat , 2004, The Journal of physiology.

[111]  Takeharu Nagai,et al.  Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity , 2004, Nature Neuroscience.

[112]  I. Reichova,et al.  Somatosensory corticothalamic projections: distinguishing drivers from modulators. , 2004, Journal of neurophysiology.

[113]  R. Douglas,et al.  A Quantitative Map of the Circuit of Cat Primary Visual Cortex , 2004, The Journal of Neuroscience.

[114]  S Murray Sherman,et al.  Differences in projection patterns between large and small corticothalamic terminals , 2004, The Journal of comparative neurology.

[115]  J. Rossier,et al.  Cortical GABA Interneurons in Neurovascular Coupling: Relays for Subcortical Vasoactive Pathways , 2004, The Journal of Neuroscience.

[116]  S. Nelson,et al.  Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation , 2004, Nature Neuroscience.

[117]  J. Zhu,et al.  Chandelier Cells Control Excessive Cortical Excitation: Characteristics of Whisker-Evoked Synaptic Responses of Layer 2/3 Nonpyramidal and Pyramidal Neurons , 2004, The Journal of Neuroscience.

[118]  Henry Markram,et al.  Interneuron Diversity series: Molecular and genetic tools to study GABAergic interneuron diversity and function , 2004, Trends in Neurosciences.

[119]  G. Tamás,et al.  Summation of unitary IPSPs elicited by identified axo-axonic interneurons. , 2004, Cerebral cortex.

[120]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[121]  G. Tamás,et al.  Gap-Junctional Coupling between Neurogliaform Cells and Various Interneuron Types in the Neocortex , 2005, The Journal of Neuroscience.

[122]  E. Callaway,et al.  Excitatory cortical neurons form fine-scale functional networks , 2005, Nature.

[123]  Maria Blatow,et al.  Molecular diversity of neocortical GABAergic interneurones , 2005, The Journal of physiology.

[124]  Rafael Yuste,et al.  Fluorescence microscopy today , 2005, Nature Methods.

[125]  Bert Sakmann,et al.  Monosynaptic Connections between Pairs of Spiny Stellate Cells in Layer 4 and Pyramidal Cells in Layer 5A Indicate That Lemniscal and Paralemniscal Afferent Pathways Converge in the Infragranular Somatosensory Cortex , 2005, The Journal of Neuroscience.

[126]  Sooyoung Chung,et al.  Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex , 2005, Nature.

[127]  G. Tamás,et al.  Lighting the chandelier: new vistas for axo-axonic cells , 2005, Trends in Neurosciences.

[128]  D. Contreras,et al.  Comparison of Responses to Electrical Stimulation and Whisker Deflection Using Two Different Voltage-sensitive Dyes in Mouse Barrel Cortex in Vivo , 2005, The Journal of Membrane Biology.

[129]  Alex M Thomson,et al.  Excitatory connections made by presynaptic cortico-cortical pyramidal cells in layer 6 of the neocortex. , 2005, Cerebral cortex.

[130]  H. Markram,et al.  Neuropeptide and calcium‐binding protein gene expression profiles predict neuronal anatomical type in the juvenile rat , 2005, The Journal of physiology.

[131]  P. Somogyi,et al.  Defined types of cortical interneurone structure space and spike timing in the hippocampus , 2005, The Journal of physiology.

[132]  E. Callaway,et al.  Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity , 2005, Nature Neuroscience.

[133]  R. Yasuda Imaging spatiotemporal dynamics of neuronal signaling using fluorescence resonance energy transfer and fluorescence lifetime imaging microscopy , 2006, Current Opinion in Neurobiology.

[134]  A. Agmon,et al.  Distinct Subtypes of Somatostatin-Containing Neocortical Interneurons Revealed in Transgenic Mice , 2006, The Journal of Neuroscience.

[135]  Rafael Yuste,et al.  Reverse optical probing (ROPING) of neocortical circuits , 2006, Synapse.

[136]  Y. Kawaguchi,et al.  Recurrent Connection Patterns of Corticostriatal Pyramidal Cells in Frontal Cortex , 2006, The Journal of Neuroscience.

[137]  Diego Contreras,et al.  Integration of evoked responses in supragranular cortex studied with optical recordings in vivo. , 2006, Journal of neurophysiology.

[138]  Johannes J. Letzkus,et al.  Cortical feed-forward networks for binding different streams of sensory information , 2006, Nature Neuroscience.

[139]  Alex M Thomson,et al.  Layer 6 cortico-thalamic pyramidal cells preferentially innervate interneurons and generate facilitating EPSPs. , 2006, Cerebral cortex.

[140]  Peter Saggau,et al.  New methods and uses for fast optical scanning , 2006, Current Opinion in Neurobiology.

[141]  Feng Zhang,et al.  Channelrhodopsin-2 and optical control of excitable cells , 2006, Nature Methods.

[142]  H. Markram,et al.  Spontaneous and evoked synaptic rewiring in the neonatal neocortex , 2006, Proceedings of the National Academy of Sciences.

[143]  G. Tamás,et al.  Excitatory Effect of GABAergic Axo-Axonic Cells in Cortical Microcircuits , 2006, Science.

[144]  Karel Svoboda,et al.  Supersensitive Ras activation in dendrites and spines revealed by two-photon fluorescence lifetime imaging , 2006, Nature Neuroscience.

[145]  Thomas K. Berger,et al.  Heterogeneity in the pyramidal network of the medial prefrontal cortex , 2006, Nature Neuroscience.

[146]  Alex M Thomson,et al.  Dynamic properties of excitatory synaptic connections involving layer 4 pyramidal cells in adult rat and cat neocortex. , 2007, Cerebral cortex.

[147]  Ian R. Wickersham,et al.  Monosynaptic Restriction of Transsynaptic Tracing from Single, Genetically Targeted Neurons , 2007, Neuron.

[148]  Yumiko Yoshimura,et al.  Specialized Inhibitory Synaptic Actions Between Nearby Neocortical Pyramidal Neurons , 2007, Science.

[149]  W. C. Hall,et al.  High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice , 2007, Proceedings of the National Academy of Sciences.

[150]  Satoru Kondo,et al.  Neocortical Inhibitory Terminals Innervate Dendritic Spines Targeted by Thalamocortical Afferents , 2007, The Journal of Neuroscience.

[151]  Alex M Thomson,et al.  Binomial parameters differ across neocortical layers and with different classes of connections in adult rat and cat neocortex , 2007, Proceedings of the National Academy of Sciences.

[152]  Hannah Monyer,et al.  Functional Characterization of Intrinsic Cholinergic Interneurons in the Cortex , 2007, The Journal of Neuroscience.

[153]  Benjamin R. Arenkiel,et al.  In Vivo Light-Induced Activation of Neural Circuitry in Transgenic Mice Expressing Channelrhodopsin-2 , 2007, Neuron.

[154]  K. Svoboda,et al.  Channelrhodopsin-2–assisted circuit mapping of long-range callosal projections , 2007, Nature Neuroscience.

[155]  A. Zaitsev,et al.  Electrophysiological differences between neurogliaform cells from monkey and rat prefrontal cortex. , 2007, Journal of neurophysiology.

[156]  H. Markram,et al.  Morphological, Electrophysiological, and Synaptic Properties of Corticocallosal Pyramidal Cells in the Neonatal Rat Neocortex , 2006 .

[157]  Alex M Thomson,et al.  Robust correlations between action potential duration and the properties of synaptic connections in layer 4 interneurones in neocortical slices from juvenile rats and adult rat and cat , 2007, The Journal of physiology.

[158]  E. Boyden,et al.  Multiple-Color Optical Activation, Silencing, and Desynchronization of Neural Activity, with Single-Spike Temporal Resolution , 2007, PloS one.

[159]  Feng Zhang,et al.  Multimodal fast optical interrogation of neural circuitry , 2007, Nature.

[160]  H. Markram,et al.  Disynaptic Inhibition between Neocortical Pyramidal Cells Mediated by Martinotti Cells , 2007, Neuron.

[161]  Massimo Scanziani,et al.  Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex , 2007, Nature Neuroscience.

[162]  Ryohei Yasuda,et al.  Imaging spatiotemporal dynamics of neuronal signaling using fluorescence resonance energy transfer and fluorescence lifetime imaging microscopy , 2007, Current Opinion in Neurobiology.

[163]  R. Kötter,et al.  Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits , 2007, Brain Structure and Function.

[164]  Y. Yanagawa,et al.  Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats. , 2008, Cerebral cortex.

[165]  Moritz Helmstaedter,et al.  Monosynaptic connections between pairs of L5A pyramidal neurons in columns of juvenile rat somatosensory cortex. , 2008, Cerebral cortex.