Enhanced high‐frequency membrane potential fluctuations control spike output in striatal fast‐spiking interneurones in vivo

Non‐technical summary  Rhythmic activity patterns are a common theme throughout neuroscience. However, it is still poorly understood how network functions are modulated by fast oscillatory inputs from distant brain regions. In this respect, the striatum is particularly interesting as almost all neuronal activity is driven by long‐range inputs. We find that the three main classes of neurones in the striatum show very distinct oscillatory activity patterns in specific frequency ranges. In particular, we show that fast‐spiking interneurones are highly sensitive to fast fluctuating synaptic inputs in the intact brain. This sensitivity was probably due to a combination of faster dynamics of synaptic inputs and intrinsic amplification of high‐frequency signals. In contrast, projection neurones and other interneurones lacking these mechanisms were insensitive to fast oscillatory input patterns. These results suggest that transmission of fast cortical oscillatory inputs modulates information processing in the striatum via engagement of fast‐spiking interneurones.

[1]  J. Berke,et al.  Fast oscillations in cortical‐striatal networks switch frequency following rewarding events and stimulant drugs , 2009, The European journal of neuroscience.

[2]  K. Blackwell,et al.  Gap Junctions between Striatal Fast-Spiking Interneurons Regulate Spiking Activity and Synchronization as a Function of Cortical Activity , 2009, The Journal of Neuroscience.

[3]  D. James Surmeier,et al.  Thalamic Gating of Corticostriatal Signaling by Cholinergic Interneurons , 2010, Neuron.

[4]  Pierre Yger,et al.  Network-State Modulation of Power-Law Frequency-Scaling in Visual Cortical Neurons , 2009, PLoS Comput. Biol..

[5]  J. Mayhew,et al.  How Visual Stimuli Activate Dopaminergic Neurons at Short Latency , 2005, Science.

[6]  Jeffery R Wickens,et al.  Inhibitory interactions between spiny projection neurons in the rat striatum. , 2002, Journal of neurophysiology.

[7]  P. Redgrave,et al.  Cortico-Striatal Spike-Timing Dependent Plasticity After Activation of Subcortical Pathways , 2010, Front. Syn. Neurosci..

[8]  P. O’Donnell,et al.  Turning off cortical ensembles stops striatal Up states and elicits phase perturbations in cortical and striatal slow oscillations in rat in vivo , 2006, The Journal of physiology.

[9]  Henrike Planert,et al.  Dynamics of Synaptic Transmission between Fast-Spiking Interneurons and Striatal Projection Neurons of the Direct and Indirect Pathways , 2010, The Journal of Neuroscience.

[10]  Jean-Michel Deniau,et al.  Cell‐specific spike‐timing‐dependent plasticity in GABAergic and cholinergic interneurons in corticostriatal rat brain slices , 2008, The Journal of physiology.

[11]  J. Tepper,et al.  Heterogeneity and Diversity of Striatal GABAergic Interneurons , 2010, Front. Neuroanat..

[12]  K. Horikawa,et al.  A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates , 1988, Journal of Neuroscience Methods.

[13]  Anatol C. Kreitzer,et al.  Distinct Roles of GABAergic Interneurons in the Regulation of Striatal Output Pathways , 2010, The Journal of Neuroscience.

[14]  D. Plenz,et al.  Up and Down States in Striatal Medium Spiny Neurons Simultaneously Recorded with Spontaneous Activity in Fast-Spiking Interneurons Studied in Cortex–Striatum–Substantia Nigra Organotypic Cultures , 1998, The Journal of Neuroscience.

[15]  Xiao-Jing Wang Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[16]  Enrico Bracci,et al.  Dopamine excites fast-spiking interneurons in the striatum. , 2002, Journal of neurophysiology.

[17]  David Golomb,et al.  Mechanisms of Firing Patterns in Fast-Spiking Cortical Interneurons , 2007, PLoS Comput. Biol..

[18]  William R. Softky,et al.  Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. , 1996, Journal of neurophysiology.

[19]  A. Engel,et al.  Different Subtypes of Striatal Neurons Are Selectively Modulated by Cortical Oscillations , 2009, The Journal of Neuroscience.

[20]  S. Anderson,et al.  The origin and specification of cortical interneurons , 2006, Nature Reviews Neuroscience.

[21]  C. H. Vanderwolf,et al.  Superior colliculus stimulation enhances neocortical serotonin release and electrocorticographic activation in the urethane-anesthetized rat , 2003, Brain Research.

[22]  H. Kita,et al.  Interneurons in the rat striatum: relationships between parvalbumin neurons and cholinergic neurons , 1992, Brain Research.

[23]  J. Wickens,et al.  Differences in striatal spiny neuron action potentials between the spontaneously hypertensive and Wistar-Kyoto rat strains , 2007, Neuroscience.

[24]  Alexander B. Wiltschko,et al.  Selective Activation of Striatal Fast-Spiking Interneurons during Choice Execution , 2010, Neuron.

[25]  S. Charpier,et al.  Relationship between EEG potentials and intracellular activity of striatal and cortico-striatal neurons: an in vivo study under different anesthetics. , 2001, Cerebral cortex.

[26]  Adriano B. L. Tort,et al.  Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task , 2008, Proceedings of the National Academy of Sciences.

[27]  H. T. Chang,et al.  Disfacilitation and long-lasting inhibition of neostriatal neurons in the rat , 2004, Experimental Brain Research.

[28]  Aaron J Gruber,et al.  Cortically activated interneurons shape spatial aspects of cortico-accumbens processing. , 2009, Journal of neurophysiology.

[29]  Kuei Yuan Tseng,et al.  Cortical Slow Oscillatory Activity Is Reflected in the Membrane Potential and Spike Trains of Striatal Neurons in Rats with Chronic Nigrostriatal Lesions , 2001, The Journal of Neuroscience.

[30]  Enrico Bracci,et al.  Voltage‐dependent membrane potential oscillations of rat striatal fast‐spiking interneurons , 2003, The Journal of physiology.

[31]  Hans R. Gelderblom,et al.  Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition , 2001 .

[32]  Y. Yarom,et al.  Resonance, oscillation and the intrinsic frequency preferences of neurons , 2000, Trends in Neurosciences.

[33]  J. Reynolds,et al.  Visual-Induced Excitation Leads to Firing Pauses in Striatal Cholinergic Interneurons , 2011, The Journal of Neuroscience.

[34]  D. Paré,et al.  Coherent gamma oscillations couple the amygdala and striatum during learning , 2009, Nature Neuroscience.

[35]  P. Calabresi,et al.  Long-term synaptic depression in the striatum: physiological and pharmacological characterization , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  Stéphane Charpier,et al.  Feedforward Inhibition of Projection Neurons by Fast-Spiking GABA Interneurons in the Rat Striatum In Vivo , 2005, The Journal of Neuroscience.

[37]  Peter Jonas,et al.  Distinct nonuniform cable properties optimize rapid and efficient activation of fast-spiking GABAergic interneurons , 2009, Proceedings of the National Academy of Sciences.

[38]  F. G. Pike,et al.  Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents , 2000, The Journal of physiology.

[39]  J. Wickens,et al.  Substantia nigra dopamine regulates synaptic plasticity and membrane potential fluctuations in the rat neostriatum, in vivo , 2000, Neuroscience.

[40]  J. Tepper,et al.  Inhibitory control of neostriatal projection neurons by GABAergic interneurons , 1999, Nature Neuroscience.

[41]  J. Wickens,et al.  Short-Latency Activation of Striatal Spiny Neurons via Subcortical Visual Pathways , 2009, The Journal of Neuroscience.

[42]  J. Deniau,et al.  Synaptic Convergence of Motor and Somatosensory Cortical Afferents onto GABAergic Interneurons in the Rat Striatum , 2002, Journal of Neuroscience.

[43]  A. Aertsen,et al.  Gating of signal propagation in spiking neural networks by balanced and correlated excitation and inhibition , 2010 .

[44]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[45]  Y. Kawaguchi,et al.  Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  Michael Rudolph,et al.  Extracting Information from the Power Spectrum of Synaptic Noise , 2004, Journal of Computational Neuroscience.

[47]  J. Berke Uncoordinated Firing Rate Changes of Striatal Fast-Spiking Interneurons during Behavioral Task Performance , 2008, The Journal of Neuroscience.

[48]  E. Bracci,et al.  Serotonin excites fast-spiking interneurons in the striatum , 2009, The European journal of neuroscience.

[49]  D. Oorschot Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: A stereological study using the cavalieri and optical disector methods , 1996, The Journal of comparative neurology.