Functional effects of distinct innervation styles of pyramidal cells by fast spiking cortical interneurons

Inhibitory interneurons target precise membrane regions on pyramidal cells, but differences in their functional effects on somata, dendrites and spines remain unclear. We analyzed inhibitory synaptic events induced by cortical, fast-spiking (FS) basket cells which innervate dendritic shafts and spines as well as pyramidal cell somata. Serial electron micrograph (EMg) reconstructions showed that somatic synapses were larger than dendritic contacts. Simulations with precise anatomical and physiological data reveal functional differences between different innervation styles. FS cell soma-targeting synapses initiate a strong, global inhibition, those on shafts inhibit more restricted dendritic zones, while synapses on spines may mediate a strictly local veto. Thus, FS cell synapses of different sizes and sites provide functionally diverse forms of pyramidal cell inhibition. DOI: http://dx.doi.org/10.7554/eLife.07919.001

[1]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[3]  Y. Kubota,et al.  Dependence of GABAergic Synaptic Areas on the Interneuron Type and Target Size , 2000, The Journal of Neuroscience.

[4]  M. Merzenich,et al.  Model of autism: increased ratio of excitation/inhibition in key neural systems , 2003, Genes, brain, and behavior.

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

[6]  N. Spruston,et al.  Synapse Distribution Suggests a Two-Stage Model of Dendritic Integration in CA1 Pyramidal Neurons , 2009, Neuron.

[7]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  R. Angus Silver,et al.  Nanoscale Distribution of Presynaptic Ca2+ Channels and Its Impact on Vesicular Release during Development , 2015, Neuron.

[9]  I. Fleidervish,et al.  How cesium dialysis affects the passive properties of pyramidal neurons: implications for voltage clamp studies of persistent sodium current , 2008 .

[10]  Roberto Araya,et al.  The spine neck filters membrane potentials , 2006, Proceedings of the National Academy of Sciences.

[11]  Nelson Spruston,et al.  Synaptic amplification by dendritic spines enhances input cooperativity , 2012, Nature.

[12]  M. Scanziani,et al.  Equalizing Excitation-Inhibition Ratios across Visual Cortical Neurons , 2014, Nature.

[13]  P. Somogyi,et al.  Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations , 2008, Science.

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

[15]  Mark Farrant,et al.  Differences in Synaptic GABAA Receptor Number Underlie Variation in GABA Mini Amplitude , 1997, Neuron.

[16]  Guosong Liu,et al.  Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites , 2004, Nature Neuroscience.

[17]  T. Freund,et al.  Differences between Somatic and Dendritic Inhibition in the Hippocampus , 1996, Neuron.

[18]  R. Miles,et al.  Noninvasive Measurements of the Membrane Potential and GABAergic Action in Hippocampal Interneurons , 1999, The Journal of Neuroscience.

[19]  Y. Kawaguchi,et al.  Two distinct activity patterns of fast-spiking interneurons during neocortical UP states , 2008, Proceedings of the National Academy of Sciences.

[20]  R. Yuste,et al.  Axo-dendritic overlap and laminar projection can explain interneuron connectivity to pyramidal cells. , 2013, Cerebral cortex.

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

[22]  Elly Nedivi,et al.  Clustered Dynamics of Inhibitory Synapses and Dendritic Spines in the Adult Neocortex , 2012, Neuron.

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

[24]  Tomoki Fukai,et al.  Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements , 2009, Nature Neuroscience.

[25]  Marc Tessier-Lavigne,et al.  Extension of Long Leading Processes and Neuronal Migration in the Mammalian Brain Directed by the Chemoattractant Netrin-1 , 1999, Neuron.

[26]  Attila Losonczy,et al.  Parvalbumin-Positive Basket Cells Differentiate among Hippocampal Pyramidal Cells , 2014, Neuron.

[27]  Thomas M. Morse,et al.  Compartmentalization of GABAergic Inhibition by Dendritic Spines , 2013, Science.

[28]  Masaki Nomura,et al.  Conserved properties of dendritic trees in four cortical interneuron subtypes , 2011, Scientific reports.

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

[30]  A. Marty,et al.  Vesicular Release Statistics and Unitary Postsynaptic Current at Single GABAergic Synapses , 2015, Neuron.

[31]  Norio Matsuki,et al.  Heterogeneity and independency of unitary synaptic outputs from hippocampal CA3 pyramidal cells , 2012, The Journal of physiology.

[32]  Yoshiyuki Kubota,et al.  Untangling GABAergic wiring in the cortical microcircuit , 2014, Current Opinion in Neurobiology.

[33]  D. Whitteridge,et al.  Synaptic connections of intracellularly filled clutch cells: A type of small basket cell in the visual cortex of the cat , 1985, The Journal of comparative neurology.

[34]  Stefan R. Pulver,et al.  Ultra-sensitive fluorescent proteins for imaging neuronal activity , 2013, Nature.

[35]  C. Wilson,et al.  Equilibrium potential of GABA(A) current and implications for rebound burst firing in rat subthalamic neurons in vitro. , 2000, Journal of neurophysiology.

[36]  Y. Kubota,et al.  Highly Differentiated Projection-Specific Cortical Subnetworks , 2011, The Journal of Neuroscience.

[37]  F. Karube,et al.  Selective coexpression of multiple chemical markers defines discrete populations of neocortical GABAergic neurons. , 2011, Cerebral cortex.

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

[39]  Nicholas T. Carnevale,et al.  Electrical Advantages of Dendritic Spines , 2012, PloS one.

[40]  Pico Caroni,et al.  Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning , 2013, Nature.

[41]  Peter Somogyi,et al.  Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites , 1994, Nature.

[42]  Yuchio Yanagawa,et al.  Fast activation of feedforward inhibitory neurons from thalamic input and its relevance to the regulation of spike sequences in the barrel cortex , 2010, The Journal of physiology.

[43]  Y. Ben-Ari,et al.  Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy , 2001, Nature Neuroscience.

[44]  Karl Deisseroth,et al.  Activation of Specific Interneurons Improves V1 Feature Selectivity and Visual Perception , 2012, Nature.

[45]  H. Kasai,et al.  Number and Density of AMPA Receptors in Single Synapses in Immature Cerebellum , 2005, The Journal of Neuroscience.

[46]  T. Yagi.  Role of the Clustered Protocadherins in Promoting Neuronal Diversity and Function , 2015 .

[47]  Masahiko Watanabe,et al.  Release probability of hippocampal glutamatergic terminals scales with the size of the active zone , 2012, Nature Neuroscience.

[48]  Joseph J. Marlin,et al.  GABA-A Receptor Inhibition of Local Calcium Signaling in Spines and Dendrites , 2014, The Journal of Neuroscience.

[49]  J C Fiala,et al.  Reconstruct: a free editor for serial section microscopy , 2005, Journal of microscopy.

[50]  R. Yuste,et al.  Dense Inhibitory Connectivity in Neocortex , 2011, Neuron.

[51]  D. Lewis,et al.  Alterations of Cortical GABA Neurons and Network Oscillations in Schizophrenia , 2010, Current psychiatry reports.

[52]  Terrence J. Sejnowski,et al.  An Efficient Method for Computing Synaptic Conductances Based on a Kinetic Model of Receptor Binding , 1994, Neural Computation.

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

[54]  G. Stuart,et al.  Excitatory Actions of GABA in the Cortex , 2003, Neuron.

[55]  R. Yuste,et al.  Dense, Unspecific Connectivity of Neocortical Parvalbumin-Positive Interneurons: A Canonical Microcircuit for Inhibition? , 2011, The Journal of Neuroscience.

[56]  Idan Segev,et al.  Principles Governing the Operation of Synaptic Inhibition in Dendrites , 2012, Neuron.

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

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

[59]  G. Ellis‐Davies,et al.  Structural basis of long-term potentiation in single dendritic spines , 2004, Nature.

[60]  T. Hirabayashi,et al.  Impaired clustered protocadherin‐α leads to aggregated retinogeniculate terminals and impaired visual acuity in mice , 2015, Journal of neurochemistry.

[61]  P. Caroni,et al.  Early- and Late-Born Parvalbumin Basket Cell Subpopulations Exhibiting Distinct Regulation and Roles in Learning , 2015, Neuron.

[62]  T. Hensch.  Critical period plasticity in local cortical circuits , 2005, Nature Reviews Neuroscience.

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

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

[65]  Y. Dan,et al.  An arithmetic rule for spatial summation of excitatory and inhibitory inputs in pyramidal neurons , 2009, Proceedings of the National Academy of Sciences.

[66]  A. Polsky,et al.  Synaptic Integration in Tuft Dendrites of Layer 5 Pyramidal Neurons: A New Unifying Principle , 2009, Science.

[67]  G. Knott,et al.  Formation of Dendritic Spines with GABAergic Synapses Induced by Whisker Stimulation in Adult Mice , 2002, Neuron.

[68]  M. Bartos,et al.  Impaired fast-spiking interneuron function in a genetic mouse model of depression , 2015, eLife.