Temporal Dynamics of Parvalbumin-Expressing Axo-axonic and Basket Cells in the Rat Medial Prefrontal Cortex In Vivo

Axo-axonic interneurons, innervating exclusively axon initial segments, and parvalbumin-expressing basket interneurons, targeting somata, dendrites, and spines of pyramidal cells, have been proposed to control neuronal activity in prefrontal circuits. We recorded the spike-timing of identified neurons in the prelimbic cortex of anesthetized rats, and show that axo-axonic cells increase their firing during tail pinch-induced brain state-activation. In addition, axo-axonic cells differ from other GABAergic parvalbumin-expressing cells in their spike timing during DOWN- to UP-state transitions of slow oscillations and in their coupling to gamma and spindle oscillations. The distinct firing dynamics and synaptic targets of axo-axonic and other parvalbumin-expressing cells provide differential contributions to the temporal organization of prefrontal networks.

[1]  E. Callaway,et al.  Erratum: Orthogonal micro-organization of orientation and spatial frequency in primate primary visual cortex , 2013, Nature Neuroscience.

[2]  A. Losonczy,et al.  Regulation of neuronal input transformations by tunable dendritic inhibition , 2012, Nature Neuroscience.

[3]  M. Carandini,et al.  Parvalbumin-Expressing Interneurons Linearly Transform Cortical Responses to Visual Stimuli , 2012, Neuron.

[4]  Thomas Klausberger,et al.  Terminal Field and Firing Selectivity of Cholecystokinin-Expressing Interneurons in the Hippocampal CA3 Area , 2011, The Journal of Neuroscience.

[5]  R. Yuste,et al.  State-Dependent Function of Neocortical Chandelier Cells , 2011, The Journal of Neuroscience.

[6]  M. Morales,et al.  Mesocorticolimbic Glutamatergic Pathway , 2011, The Journal of Neuroscience.

[7]  O. Marín,et al.  Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling , 2010, Nature.

[8]  T. Klausberger,et al.  Distinct Firing Patterns of Identified Basket and Dendrite-Targeting Interneurons in the Prefrontal Cortex during Hippocampal Theta and Local Spindle Oscillations , 2009, The Journal of Neuroscience.

[9]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

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

[11]  John R. Huguenard,et al.  Thalamic synchrony and dynamic regulation of global forebrain oscillations , 2007, Trends in Neurosciences.

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

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

[14]  P. Jonas,et al.  Shunting Inhibition Improves Robustness of Gamma Oscillations in Hippocampal Interneuron Networks by Homogenizing Firing Rates , 2006, Neuron.

[15]  D. Lewis,et al.  Cortical inhibitory neurons and schizophrenia , 2005, Nature Reviews Neuroscience.

[16]  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.

[17]  R. Yuste,et al.  Attractor dynamics of network UP states in the neocortex , 2003, Nature.

[18]  P. Goldman-Rakic,et al.  Dopamine Modulation of Perisomatic and Peridendritic Inhibition in Prefrontal Cortex , 2003, The Journal of Neuroscience.

[19]  M. Steriade,et al.  Neuronal Plasticity in Thalamocortical Networks during Sleep and Waking Oscillations , 2003, Neuron.

[20]  P. Somogyi,et al.  Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons , 2000, Nature Neuroscience.

[21]  Y. Kawaguchi,et al.  Noradrenergic Excitation and Inhibition of GABAergic Cell Types in Rat Frontal Cortex , 1998, The Journal of Neuroscience.

[22]  J. Csicsvari,et al.  Reliability and State Dependence of Pyramidal Cell–Interneuron Synapses in the Hippocampus an Ensemble Approach in the Behaving Rat , 1998, Neuron.

[23]  D. Pinault,et al.  A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin , 1996, Journal of Neuroscience Methods.

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

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

[26]  M. Arbib,et al.  Conceptual models of neural organization. , 1974, Neurosciences Research Program bulletin.

[27]  Peter Somogyi,et al.  Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis , 2009, Nature Neuroscience.

[28]  G. Buzsáki.  Rhythms of the brain , 2006 .

[29]  Abbreviated title: Rhythmically discharging units Address all correspondence to: , 2022 .