Response to Comment on “Principles of connectivity among morphologically defined cell types in adult neocortex”

The critique of Barth et al. centers on three points: (i) the completeness of our study is overstated; (ii) the connectivity matrix we describe is biased by technical limitations of our brain-slicing and multipatching methods; and (iii) our cell classification scheme is arbitrary and we have simply renamed previously identified interneuron types. We address these criticisms in our Response.

[1]  N. Tamamaki,et al.  Long-Range GABAergic Connections Distributed throughout the Neocortex and their Possible Function , 2010, Front. Neurosci..

[2]  Quanxin Wang,et al.  Multiple Distinct Subtypes of GABAergic Neurons in Mouse Visual Cortex Identified by Triple Immunostaining , 2007, Frontiers in neuroanatomy.

[3]  S. Hestrin,et al.  Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Kevin L. Briggman,et al.  Wiring specificity in the direction-selectivity circuit of the retina , 2011, Nature.

[5]  B. Connors,et al.  A network of electrically coupled interneurons drives synchronized inhibition in neocortex , 2000, Nature Neuroscience.

[6]  S. Nelson,et al.  A Resource of Cre Driver Lines for Genetic Targeting of GABAergic Neurons in Cerebral Cortex , 2011, Neuron.

[7]  Bernardo Rudy,et al.  Channelrhodopsin-assisted patching: in vivo recording of genetically and morphologically identified neurons throughout the brain. , 2014, Cell reports.

[8]  Y. Kubota,et al.  Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  S. Hestrin,et al.  Morphology and Physiology of Cortical Neurons in Layer I , 1996, The Journal of Neuroscience.

[10]  George H. Denfield,et al.  Pupil Fluctuations Track Fast Switching of Cortical States during Quiet Wakefulness , 2014, Neuron.

[11]  Alexander S. Ecker,et al.  Principles of connectivity among morphologically defined cell types in adult neocortex , 2015, Science.

[12]  Xiaolong Jiang,et al.  The organization of two new cortical interneuronal circuits , 2013, Nature Neuroscience.

[13]  Hannah Monyer,et al.  GABAergic Interneurons Shape the Functional Maturation of the Cortex , 2013, Neuron.

[14]  Trevor Hastie,et al.  Regularization Paths for Generalized Linear Models via Coordinate Descent. , 2010, Journal of statistical software.

[15]  C. McBain,et al.  Neurogliaform cells dynamically regulate somatosensory integration via synapse-specific modulation , 2012, Nature Neuroscience.

[16]  Daniel R. Berger,et al.  The Fuzzy Logic of Network Connectivity in Mouse Visual Thalamus , 2016, Cell.

[17]  Athanasia G. Palasantza,et al.  Electrophysiological, transcriptomic and morphologic profiling of single neurons using Patch-seq , 2015, Nature Biotechnology.

[18]  Ken Mackie,et al.  Endocannabinoid Signaling in Rat Somatosensory Cortex: Laminar Differences and Involvement of Specific Interneuron Types , 2005, The Journal of Neuroscience.

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

[20]  G. Fishell,et al.  Interneuron cell types are fit to function , 2014, Nature.

[21]  G. Shepherd,et al.  Geometric and functional organization of cortical circuits , 2005, Nature Neuroscience.

[22]  Kristina J. Nielsen,et al.  Targeting Single Neuronal Networks for Gene Expression and Cell Labeling In Vivo , 2010, Neuron.

[23]  Thomas K. Berger,et al.  A synaptic organizing principle for cortical neuronal groups , 2011, Proceedings of the National Academy of Sciences.

[24]  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.

[25]  Alex S. Ferecskó,et al.  The fractions of short- and long-range connections in the visual cortex , 2009, Proceedings of the National Academy of Sciences.

[26]  Sonja M. Wojcik,et al.  A Shared Vesicular Carrier Allows Synaptic Corelease of GABA and Glycine , 2006, Neuron.

[27]  Jochen F. Staiger,et al.  Characterizing VIP Neurons in the Barrel Cortex of VIPcre/tdTomato Mice Reveals Layer-Specific Differences , 2015, Cerebral cortex.

[28]  Arne V. Blackman,et al.  Target-Specific Expression of Presynaptic NMDA Receptors in Neocortical Microcircuits , 2012, Neuron.

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

[30]  Rafael Yuste,et al.  Comment on “Principles of connectivity among morphologically defined cell types in adult neocortex” , 2016, Science.

[31]  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.

[32]  Edward M. Callaway,et al.  Laminar Specificity of Functional Input to Distinct Types of Inhibitory Cortical Neurons , 2009, The Journal of Neuroscience.

[33]  Dina R. Dajani,et al.  Local brain connectivity across development in autism spectrum disorder: A cross‐sectional investigation , 2016, Autism research : official journal of the International Society for Autism Research.

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

[35]  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.

[36]  D. Prince,et al.  Heterogeneous actions of serotonin on interneurons in rat visual cortex. , 2003, Journal of neurophysiology.

[37]  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.

[38]  Rafael Yuste,et al.  Persistently Active, Pacemaker-Like Neurons in Neocortex , 2007, Front. Neurosci..

[39]  Csaba Varga,et al.  HUMAN AND , 2022 .

[40]  A. Bacci,et al.  The neuronal identity bias behind neocortical GABAergic plasticity , 2015, Trends in Neurosciences.

[41]  Karel Svoboda,et al.  A platform for brain-wide imaging and reconstruction of individual neurons , 2016, eLife.

[42]  F. Fujiyama,et al.  Demonstration of long‐range GABAergic connections distributed throughout the mouse neocortex , 2005, The European journal of neuroscience.

[43]  Dirk Feldmeyer,et al.  Electrophysiological and morphological characterization of neuronal microcircuits in acute brain slices using paired patch-clamp recordings. , 2015, Journal of visualized experiments : JoVE.

[44]  Y. Kawaguchi,et al.  Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex , 2002, Journal of neurocytology.

[45]  Xiaolong Jiang,et al.  Canonical Organization of Layer 1 Neuron-Led Cortical Inhibitory and Disinhibitory Interneuronal Circuits. , 2015, Cerebral cortex.

[46]  Emery N. Brown,et al.  The BRAIN Initiative: developing technology to catalyse neuroscience discovery , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[47]  R. Yuste,et al.  Correlation between axonal morphologies and synaptic input kinetics of interneurons from mouse visual cortex. , 2007, Cerebral cortex.

[48]  M. Scanziani,et al.  Inhibition of Inhibition in Visual Cortex: The Logic of Connections Between Molecularly Distinct Interneurons , 2013, Nature Neuroscience.

[49]  G. Fishell,et al.  The Largest Group of Superficial Neocortical GABAergic Interneurons Expresses Ionotropic Serotonin Receptors , 2010, The Journal of Neuroscience.

[50]  Arno C. Schmitt,et al.  Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A , 2011, Proceedings of the National Academy of Sciences.

[51]  Charles Rattray,et al.  Themes and variations , 2007, Architectural Research Quarterly.

[52]  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.

[53]  Yuchio Yanagawa,et al.  Local Connections of Layer 5 GABAergic Interneurons to Corticospinal Neurons , 2011, Front. Neural Circuits.

[54]  G. Fishell,et al.  A disinhibitory circuit mediates motor integration in the somatosensory cortex , 2013, Nature Neuroscience.

[55]  Charles J. Wilson,et al.  An inhibitory corticostriatal pathway , 2016, eLife.

[56]  Andreas T Schaefer,et al.  Transfection via whole-cell recording in vivo: bridging single-cell physiology, genetics and connectomics , 2011, Nature Neuroscience.

[57]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

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

[59]  Simon J. Mitchell,et al.  Direct measurement of somatic voltage clamp errors in central neurons , 2008, Nature Neuroscience.

[60]  Hysell V. Oviedo,et al.  Long-term Cre-mediated retrograde tagging of neurons using a novel recombinant pseudorabies virus , 2014, Front. Neuroanat..

[61]  Brett J. Graham,et al.  Anatomy and function of an excitatory network in the visual cortex , 2016, Nature.

[62]  R. Rosenfeld.  Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[63]  A. Reyes,et al.  Spatial Profile of Excitatory and Inhibitory Synaptic Connectivity in Mouse Primary Auditory Cortex , 2012, The Journal of Neuroscience.

[64]  L. Luo,et al.  Comprehensive Maps of Drosophila Higher Olfactory Centers: Spatially Segregated Fruit and Pheromone Representation , 2007, Cell.

[65]  B. Connors,et al.  Two networks of electrically coupled inhibitory neurons in neocortex , 1999, Nature.

[66]  Ariel Agmon,et al.  Not all that glitters is gold: off-target recombination in the somatostatin–IRES-Cre mouse line labels a subset of fast-spiking interneurons , 2013, Front. Neural Circuits.

[67]  M. Brecht,et al.  Spiking Irregularity and Frequency Modulate the Behavioral Report of Single-Neuron Stimulation , 2014, Neuron.

[68]  Ivan Cohen,et al.  Diversity and overlap of parvalbumin and somatostatin expressing interneurons in mouse presubiculum , 2015, Front. Neural Circuits.

[69]  Theofanis Karayannis,et al.  Sensory inputs control the integration of neurogliaform interneurons into cortical circuits , 2015, Nature Neuroscience.

[70]  Z. J. Huang,et al.  Development of GABA innervation in the cerebral and cerebellar cortices , 2007, Nature Reviews Neuroscience.

[71]  Joshua I. Sanders,et al.  Cortical interneurons that specialize in disinhibitory control , 2013, Nature.

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

[73]  N. Seidah,et al.  Regulation by gastric acid of the processing of progastrin‐derived peptides in rat antral mucosa , 1997, The Journal of physiology.

[74]  E. P. Gardner,et al.  Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex , 2008, Nature Reviews Neuroscience.

[75]  M. C. Angulo,et al.  Molecular and Physiological Diversity of Cortical Nonpyramidal Cells , 1997, The Journal of Neuroscience.

[76]  Christian Wozny,et al.  Specificity of Synaptic Connectivity between Layer 1 Inhibitory Interneurons and Layer 2/3 Pyramidal Neurons in the Rat Neocortex , 2011, Cerebral cortex.

[77]  R. Nicoll,et al.  Loss of Inhibitory Neuron AMPA Receptors Contributes to Ataxia and Epilepsy in Stargazer Mice , 2008, The Journal of Neuroscience.

[78]  C. Petersen,et al.  The Excitatory Neuronal Network of the C2 Barrel Column in Mouse Primary Somatosensory Cortex , 2009, Neuron.

[79]  L. Gliksman,et al.  A CROSS-SECTIONAL INVESTIGATION , 1989 .

[80]  Concha Bielza,et al.  New insights into the classification and nomenclature of cortical GABAergic interneurons , 2013, Nature Reviews Neuroscience.