Developmental control of spike-timing-dependent plasticity by tonic GABAergic signaling in striatum

Activity-dependent long-term potentiation (LTP) and depression (LTD) of synaptic strength underlie multiple forms of learning and memory. Spike-timing-dependent plasticity (STDP) has been described as a Hebbian synaptic learning rule that could account for experience-dependent changes in neural networks, but little is known about whether and how STDP evolves during development. We previously showed that GABAergic signaling governs STDP polarity and thus operates as a Hebbian/anti-Hebbian switch in the striatum. Although GABAergic networks are subject to important developmental maturation, it remains unclear whether STDP is developmentally shaped by GABAergic signaling. Here, we investigated whether STDP rules are developmentally regulated at corticostriatal synapses in the dorsolateral striatum. We found that striatal STDP displays unidirectional plasticity (Hebbian tLTD) in young rats (P7-10) whereas STDP is bidirectional and anti-Hebbian in juvenile (P20-25) and adult (P60-90) rats. We also provide evidence that the appearance of tonic (extrasynaptic) GABAergic signaling from the juvenile stage is a crucial factor in shaping STDP rules during development, establishing bidirectional anti-Hebbian STDP in the adult striatum. Thus, developmental maturation of GABAergic signaling tightly drives the polarity of striatal plasticity.

[1]  F. Conti,et al.  GABA transporters in the mammalian cerebral cortex: localization, development and pathological implications , 2004, Brain Research Reviews.

[2]  P. J. Sjöström,et al.  Dendritic excitability and synaptic plasticity. , 2008, Physiological reviews.

[3]  P. Jonas,et al.  Symmetric spike timing-dependent plasticity at CA3–CA3 synapses optimizes storage and recall in autoassociative networks , 2016, Nature Communications.

[4]  S. Kirischuk,et al.  GABA transporter 1 tunes GABAergic synaptic transmission at output neurons of the mouse neostriatum , 2008, The Journal of physiology.

[5]  Yihui Cui,et al.  Distinct coincidence detectors govern the corticostriatal spike timing‐dependent plasticity , 2010, The Journal of physiology.

[6]  Laurent Venance,et al.  Spike-Timing Dependent Plasticity in the Striatum , 2010, Front. Syn. Neurosci..

[7]  Rodney C. Samaco,et al.  GABAergic dysfunction mediates autism-like stereotypies and Rett syndrome phenotypes , 2010, Nature.

[8]  Kristen K. Ade,et al.  Dopamine Modulation of GABA Tonic Conductance in Striatal Output Neurons , 2009, The Journal of Neuroscience.

[9]  F. Kimura,et al.  Developmental Switch in Spike Timing-Dependent Plasticity at Layers 4–2/3 in the Rodent Barrel Cortex , 2012, The Journal of Neuroscience.

[10]  M. Farrant,et al.  Variations on an inhibitory theme: phasic and tonic activation of GABAA receptors , 2005, Nature Reviews Neuroscience.

[11]  N. Nelson,et al.  Molecular characterization of four pharmacologically distinct gamma-aminobutyric acid transporters in mouse brain [corrected]. , 1993, The Journal of biological chemistry.

[12]  David Attwell,et al.  Multiple modes of GABAergic inhibition of rat cerebellar granule cells , 2003, The Journal of physiology.

[13]  I. Módy,et al.  Developmental regulation and neuroprotective effects of striatal tonic GABAA currents , 2010, Neuroscience.

[14]  A. Zador,et al.  Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex , 2003, Nature.

[15]  L. Venance,et al.  Astrocytes gate Hebbian synaptic plasticity in the striatum , 2016, Nature Communications.

[16]  I. Módy,et al.  Activation of GABAA Receptors: Views from Outside the Synaptic Cleft , 2007, Neuron.

[17]  R. Pearce,et al.  Etomidate Impairs Long-Term Potentiation In Vitro by Targeting α5-Subunit Containing GABAA Receptors on Nonpyramidal Cells , 2015, The Journal of Neuroscience.

[18]  D. Feldman.  The Spike-Timing Dependence of Plasticity , 2012, Neuron.

[19]  J. A. Peters,et al.  Subunit‐dependent interaction of the general anaesthetic etomidate with the γ‐aminobutyric acid type A receptor , 1997, British journal of pharmacology.

[20]  D. Contreras,et al.  Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation , 2006, The Journal of Neuroscience.

[21]  Takao K Hensch,et al.  Balancing plasticity/stability across brain development. , 2013, Progress in brain research.

[22]  S. Panzeri,et al.  Excitatory GABAergic effects in striatal projection neurons. , 2006, Journal of neurophysiology.

[23]  Joshua L. Plotkin,et al.  Development of striatal fast-spiking GABAergic interneurons. , 2007, Progress in brain research.

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

[25]  J. Partridge,et al.  Distinct roles of synaptic and extrasynaptic GABAAreceptors in striatal inhibition dynamics , 2013, Front. Neural Circuits.

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

[27]  S. Moss,et al.  Functional regulation of GABAA receptors in nervous system pathologies , 2012, Current Opinion in Neurobiology.

[28]  F. Fujiyama,et al.  A single-neuron tracing study of arkypallidal and prototypic neurons in healthy rats , 2015, Brain Structure and Function.

[29]  J. Glowinski,et al.  Bidirectional Activity-Dependent Plasticity at Corticostriatal Synapses , 2005, The Journal of Neuroscience.

[30]  Henrike Planert,et al.  Target Selectivity of Feedforward Inhibition by Striatal Fast-Spiking Interneurons , 2013, The Journal of Neuroscience.

[31]  R. Khazipov,et al.  GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. , 2007, Physiological reviews.

[32]  Charles J. Wilson,et al.  Comparison of IPSCs Evoked by Spiny and Fast-Spiking Neurons in the Neostriatum , 2004, The Journal of Neuroscience.

[33]  R. Froemke,et al.  Oxytocin Enables Maternal Behavior by Balancing Cortical Inhibition , 2015, Nature.

[34]  J. Kerr,et al.  Dopamine Receptor Activation Is Required for Corticostriatal Spike-Timing-Dependent Plasticity , 2008, The Journal of Neuroscience.

[35]  Anatol C. Kreitzer,et al.  Striatal microcircuitry and movement disorders , 2012, Trends in Neurosciences.

[36]  I. Módy,et al.  Extrasynaptic GABAA Receptors: Their Function in the CNS and Implications for Disease , 2012, Neuron.

[37]  P. Greengard,et al.  Dichotomous Dopaminergic Control of Striatal Synaptic Plasticity , 2008, Science.

[38]  Patrick D. Roberts,et al.  Computational Consequences of Temporally Asymmetric Learning Rules: II. Sensory Image Cancellation , 2000, Journal of Computational Neuroscience.

[39]  R. Malenka,et al.  Synaptic Plasticity: Multiple Forms, Functions, and Mechanisms , 2008, Neuropsychopharmacology.

[40]  Laurent Venance,et al.  Electrical and chemical transmission between striatal GABAergic output neurones in rat brain slices , 2004, The Journal of physiology.

[41]  G. Silberberg,et al.  Local and afferent synaptic pathways in the striatal microcircuitry , 2015, Current Opinion in Neurobiology.

[42]  A. Fukuda,et al.  Pathophysiological power of improper tonic GABAA conductances in mature and immature models , 2013, Front. Neural Circuits.

[43]  Charles J. Wilson,et al.  Feedforward and feedback inhibition in neostriatal GABAergic spiny neurons , 2008, Brain Research Reviews.

[44]  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.

[45]  Jeanette Hellgren Kotaleski,et al.  GABAergic Circuits Control Spike-Timing-Dependent Plasticity , 2013, The Journal of Neuroscience.

[46]  P. J. Sjöström,et al.  A Cooperative Switch Determines the Sign of Synaptic Plasticity in Distal Dendrites of Neocortical Pyramidal Neurons , 2006, Neuron.

[47]  Sadegh Nabavi,et al.  Engineering a memory with LTD and LTP , 2014, Nature.

[48]  W Wisden,et al.  The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  S. Vicini,et al.  GABAA Receptor β3 Subunit Expression Regulates Tonic Current in Developing Striatopallidal Medium Spiny Neurons , 2011, Front. Cell. Neurosci..

[50]  Istvan Mody,et al.  Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. , 2002, Journal of neurophysiology.

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

[52]  P. Whiting,et al.  Pharmacological characterization of a novel cell line expressing human α4β3δ GABAA receptors , 2002 .

[53]  B. D. Bennett,et al.  Synaptic input and output of parvalbumin-immunoreactive neurons in the neostriatum of the rat , 1994, Neuroscience.

[54]  M. Farrant,et al.  Whole‐cell and single‐channel currents activated by GABA and glycine in granule cells of the rat cerebellum. , 1995, The Journal of physiology.

[55]  P. Calabresi,et al.  Direct and indirect pathways of basal ganglia: a critical reappraisal , 2014, Nature Neuroscience.

[56]  Masahiko Watanabe,et al.  Developmental Switch in Spike Timing-Dependent Plasticity and Cannabinoid-Dependent Reorganization of the Thalamocortical Projection in the Barrel Cortex , 2016, The Journal of Neuroscience.

[57]  O. Paulsen,et al.  Development of dendritic tonic GABAergic inhibition regulates excitability and plasticity in CA1 pyramidal neurons. , 2014, Journal of neurophysiology.

[58]  D. Kullmann,et al.  GABA uptake regulates cortical excitability via cell type–specific tonic inhibition , 2003, Nature Neuroscience.

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

[60]  Johannes J. Letzkus,et al.  Dendritic Synapse Location and Neocortical Spike-Timing-Dependent Plasticity , 2010, Front. Syn. Neurosci..

[61]  Kristen K. Ade,et al.  Differential Tonic GABA Conductances in Striatal Medium Spiny Neurons , 2008, The Journal of Neuroscience.

[62]  L. Trussell,et al.  Coactivation of Pre- and Postsynaptic Signaling Mechanisms Determines Cell-Specific Spike-Timing-Dependent Plasticity , 2007, Neuron.

[63]  A. Schousboe,et al.  PHOSPHATE ACTIVATED GLUTAMINASE ACTIVITY AND GLUTAMINE UPTAKE IN PRIMARY CULTURES OF ASTROCYTES , 1979, Journal of neurochemistry.

[64]  Laurent Venance,et al.  Contribution of astrocytic glutamate and GABA uptake to corticostriatal information processing , 2011, The Journal of physiology.