L2/3 interneuron groups defined by multiparameter analysis of axonal projection, dendritic geometry, and electrical excitability.

For a detailed description of the circuitry of cortical columns at the level of single neurons, it is essential to define the identities of the cell types that constitute these columns. For interneurons (INs), we described 4 "types of axonal projection patterns" in layer 2/3 (L2/3) with reference to the outlines of a cortical column (Helmstaedter et al. 2008a). In addition we quantified the dendritic geometry and electrical excitability of 3 types of the L2/3 INs: "local," "lateral," and "translaminar" inhibitors (Helmstaedter et al. 2008b). Here, we used an iterated cluster analysis (iCA) that combines axonal projection patterns with dendritic geometry and electrical excitability parameters to identify "groups" of INs, from a sample of 39 cells. The iCA defined 9 groups of INs. We propose a hierarchical scheme for identifying L2/3 INs. First, L2/3 INs can be classified as 4 types of axonal projections. Second, L2/3 INs can be subclassified as 9 groups with a high within-group similarity of dendritic, axonal, and electrical parameters. This scheme of identifying L2/3 INs may help to quantitatively describe inhibitory effects on sensory stimulus representations in L2/3 of cortical columns.

[1]  E. G. Jones,et al.  Varieties and distribution of non‐pyramidal cells in the somatic sensory cortex of the squirrel monkey , 1975, The Journal of comparative neurology.

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

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

[4]  B. Connors,et al.  Thalamocortical responses of mouse somatosensory (barrel) cortexin vitro , 1991, Neuroscience.

[5]  I. Divac.  Cortical circuits: Synaptic organization of the cerebral cortex. Structure, function and theory by Edward L. White, Birkäuser, 1989. Sw. fr. 88.00 (xvi + 223 pages) ISBN 3 7643 3402 9 , 1990, Trends in Neurosciences.

[6]  D. Lewis,et al.  Cluster analysis-based physiological classification and morphological properties of inhibitory neurons in layers 2-3 of monkey dorsolateral prefrontal cortex. , 2005, Journal of neurophysiology.

[7]  G. Miyoshi,et al.  Physiologically Distinct Temporal Cohorts of Cortical Interneurons Arise from Telencephalic Olig2-Expressing Precursors , 2007, The Journal of Neuroscience.

[8]  Moritz Helmstaedter,et al.  The relation between dendritic geometry, electrical excitability, and axonal projections of L2/3 interneurons in rat barrel cortex. , 2009, Cerebral cortex.

[9]  R. R. Sturrock,et al.  Problems of the Keimbahn: New Work on Mammalian Germ Cell Lineage , 1985 .

[10]  S. R. Cajal.  Textura del Sistema Nervioso del Hombre y de los Vertebrados, 1899–1904 , 2019 .

[11]  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.

[12]  I. Ferrer,et al.  Non-pyramidal neurons of layers I-III in the dog's cerebral cortex (parietal lobe). A Golgi survey. , 1987, Acta anatomica.

[13]  S. Nelson,et al.  Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. , 2007, Journal of neurophysiology.

[14]  Cpj de Kock,et al.  Reconstruction of an average cortical column in silico , 2007, Brain Research Reviews.

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

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

[17]  Jose-Manuel Alonso,et al.  Functionally distinct inhibitory neurons at the first stage of visual cortical processing , 2003, Nature Neuroscience.

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

[19]  H. Dodt,et al.  Visualizing unstained neurons in living brain slices by infrared DIC-videomicroscopy , 1990, Brain Research.

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

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

[22]  P. Somogyi,et al.  Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat , 1983, Neuroscience.

[23]  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.

[24]  B. Sakmann,et al.  Neuronal correlates of local, lateral, and translaminar inhibition with reference to cortical columns. , 2009, Cerebral cortex.

[25]  Karel Svoboda,et al.  Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs , 2004, Nature Neuroscience.

[26]  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.

[27]  Moritz Helmstaedter,et al.  Efficient Recruitment of Layer 2/3 Interneurons by Layer 4 Input in Single Columns of Rat Somatosensory Cortex , 2008, The Journal of Neuroscience.

[28]  M. Marín‐padilla.  Origin of the pericellular baskets of the pyramidal cells of the human motor cortex: a Golgi study. , 1969, Brain research.

[29]  J. Rossier,et al.  Classification of fusiform neocortical interneurons based on unsupervised clustering. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  B. Sakmann,et al.  Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy , 1993, Pflügers Archiv.

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

[32]  J. Szentágothai.  Synaptology of the Visual Cortex , 1973 .

[33]  R. Douglas,et al.  Mapping the Matrix: The Ways of Neocortex , 2007, Neuron.

[34]  P. Somogyi,et al.  Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat's visual cortex , 1986, Neuroscience.

[35]  C. Beaulieu,et al.  Numerical data on neocortical neurons in adult rat, with special reference to the GABA population , 1993, Brain Research.

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

[37]  J F Fulton,et al.  Physiology of the Nervous System , 1939, Science.

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

[39]  M. Marín‐padilla.  Double origin of the pericellular baskets of the pyramidal cells of the human motor cortex: a Golgi study. , 1969, Brain research.

[40]  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.

[41]  M. Sanders.  Handbook of Sensory Physiology , 1975 .

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

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

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

[45]  Kevin L. Briggman,et al.  Towards neural circuit reconstruction with volume electron microscopy techniques , 2006, Current Opinion in Neurobiology.