The relation between dendritic geometry, electrical excitability, and axonal projections of L2/3 interneurons in rat barrel cortex.

Interneurons in layer 2/3 (L2/3) of the somatosensory cortex show 4 types of axonal projection patterns with reference to the laminae and borders of columns in rat barrel cortex (Helmstaedter et al. 2008a). Here, we analyzed the dendritic geometry and electrical excitability of these interneurons. First, dendritic polarity, measured based on the insertion points of primary dendrites on the soma surface, yielded a continuous one-dimensional measure without a clustering of dendritic polarity types. Secondly, we analyzed polar and vertical distributions of dendritic length. A cluster analysis allowed the definition of 7 types of dendritic arborization. Thirdly, when dendritic polarity was related to the intrinsic electrical excitability we found that the ratio of frequency adaptation in trains of action potentials (APs) evoked by current injection was correlated with the number of primary dendrites. Numerical simulations of spiking patterns in L2/3 interneurons suggested that the number of primary dendrites could account for up to 50% of this correlation. Fourthly, dendritic arborization was not correlated with axonal projection, and axonal projection types could not be predicted by electrical excitability parameters. We conclude that 1) dendritic polarity is correlated to intrinsic electrical excitability, and 2) the axonal projection pattern represents an independent classifier of interneurons.

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

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

[3]  T. Sejnowski,et al.  [Letters to nature] , 1996, Nature.

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

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

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

[7]  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.

[8]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

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

[10]  Richard Miles,et al.  Interneuron Diversity series: Fast in, fast out – temporal and spatial signal processing in hippocampal interneurons , 2004, Trends in Neurosciences.

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

[12]  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.

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

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

[15]  Chris J. McBain,et al.  Interneurons unbound , 2001, Nature Reviews Neuroscience.

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

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

[18]  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.

[19]  W. Rall.  Branching dendritic trees and motoneuron membrane resistivity. , 1959, Experimental neurology.

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

[21]  John R. Huguenard,et al.  Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids , 2004, Nature.

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

[23]  Nicholas T. Carnevale,et al.  The NEURON Simulation Environment , 1997, Neural Computation.

[24]  Miles A Whittington,et al.  Interneuron Diversity series: Inhibitory interneurons and network oscillations in vitro , 2003, Trends in Neurosciences.

[25]  Moritz Helmstaedter,et al.  L2/3 interneuron groups defined by multiparameter analysis of axonal projection, dendritic geometry, and electrical excitability. , 2009, Cerebral cortex.

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

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

[28]  Maria V. Sanchez-Vives,et al.  Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. , 2003, Journal of neurophysiology.

[29]  F. Karube,et al.  Axon Branching and Synaptic Bouton Phenotypes in GABAergic Nonpyramidal Cell Subtypes , 2004, The Journal of Neuroscience.

[30]  J. Lübke,et al.  Columnar Organization of Dendrites and Axons of Single and Synaptically Coupled Excitatory Spiny Neurons in Layer 4 of the Rat Barrel Cortex , 2000, The Journal of Neuroscience.

[31]  Randy M Bruno,et al.  Subcolumnar dendritic and axonal organization of spiny stellate and star pyramid neurons within a barrel in rat somatosensory cortex. , 2008, Cerebral cortex.

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

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

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

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

[36]  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.

[37]  A. Zaitsev,et al.  Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral prefrontal cortex. , 2005, Cerebral cortex.

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

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

[40]  Andreas T. Schaefer,et al.  Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern. , 2003, Journal of neurophysiology.

[41]  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.

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

[43]  J. H. Ward.  Hierarchical Grouping to Optimize an Objective Function , 1963 .

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

[45]  B. Sakmann,et al.  Cortex Is Driven by Weak but Synchronously Active Thalamocortical Synapses , 2006, Science.

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

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

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

[49]  勇一 作村,et al.  Biophysics of Computation , 2001 .

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

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

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

[53]  A. Burkhalter,et al.  Three distinct families of GABAergic neurons in rat visual cortex. , 1997, Cerebral cortex.

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

[55]  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.

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

[57]  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.

[58]  R. Foehring,et al.  Correlation of physiologically and morphologically identified neuronal types in human association cortex in vitro. , 1991, Journal of neurophysiology.

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