In vivo activity-dependent plasticity at cortico-striatal connections: evidence for physiological long-term potentiation.

The purpose of the present study was to investigate in vivo the activity-dependent plasticity of glutamatergic cortico-striatal synapses. Electrical stimuli were applied in the facial motor cortex and intracellular recordings were performed in the ipsilateral striatal projection field of this cortical area. Recorded cells exhibited the typical intrinsic membrane properties of striatal output neurons and were identified morphologically as medium spiny type I neurons. Subthreshold cortical tetanization produced either short-term posttetanic potentiation or short-term depression of cortically-evoked excitatory postsynaptic potentials. When coupled with a postsynaptic depolarization leading the membrane potential to a suprathreshold level, the tetanus induced long-term potentiation (LTP) of cortico-striatal synaptic transmission. Induction of striatal LTP was prevented by intracellular injection of a calcium chelator suggesting that this synaptic plasticity involves an increase of postsynaptic free calcium concentration. Contrasting with previous in vitro studies our findings demonstrate that LTP constitutes the normal form of use-dependent plasticity at cortico-striatal synapses. Since excitation of striatal neurons produces a disinhibition of premotor networks, LTP at excitatory striatal inputs should favor the initiation of movements and therefore could be critical for the functions of basal ganglia in motor learning.

[1]  R. Hall,et al.  Organization of motor and somatosensory neocortex in the albino rat , 1974 .

[2]  P. Schwartzkroin,et al.  Long-lasting facilitation of a synaptic potential following tetanization in thein vitro hippocampal slice , 1975, Brain Research.

[3]  B. McNaughton,et al.  Synaptic enhancement in fascia dentata: Cooperativity among coactive afferents , 1978, Brain Research.

[4]  S. T. Kitai,et al.  A Golgi study of rat neostriatal neurons: Light microscopic analysis , 1982, The Journal of comparative neurology.

[5]  G. Lynch,et al.  Intracellular injections of EGTA block induction of hippocampal long-term potentiation , 1983, Nature.

[6]  P. Herrling Pharmacology of the corticocaudate excitatory postsynaptic potential in the cat: Evidence for its mediation by quisqualateor kainate-receptors , 1985, Neuroscience.

[7]  Charles J. Wilson Postsynaptic potentials evoked in spiny neostriatal projection neurons by stimulation of ipsilateral and contralateral neocortex , 1986, Brain Research.

[8]  Richard F. Thompson The neurobiology of learning and memory. , 1986, Science.

[9]  P. Stanzione,et al.  Excitatory amino acids in synaptic excitation of rat striatal neurones in vitro. , 1988, The Journal of physiology.

[10]  J. Deniau,et al.  Disinhibition as a basic process in the expression of striatal functions , 1990, Trends in Neurosciences.

[11]  G Bernardi,et al.  Synaptic and intrinsic control of membrane excitability of neostriatal neurons. I. An in vivo analysis. , 1990, Journal of neurophysiology.

[12]  R. North,et al.  Membrane properties and synaptic responses of rat striatal neurones in vitro. , 1991, The Journal of physiology.

[13]  P. Calabresi,et al.  Long‐term Potentiation in the Striatum is Unmasked by Removing the Voltage‐dependent Magnesium Block of NMDA Receptor Channels , 1992, The European journal of neuroscience.

[14]  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.

[15]  Dimitri M. Kullmann,et al.  Ca2+ Entry via postsynaptic voltage-sensitive Ca2+ channels can transiently potentiate excitatory synaptic transmission in the hippocampus , 1992, Neuron.

[16]  R. Malenka,et al.  Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus , 1992, Neuron.

[17]  D. Lovinger,et al.  Short- and long-term synaptic depression in rat neostriatum. , 1993, Journal of neurophysiology.

[18]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[19]  R. Nicoll,et al.  NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms , 1993, Trends in Neurosciences.

[20]  J. Walsh,et al.  Synaptic activation of N-methyl-d-aspartate receptors induces short-term potentiation at excitatory synapses in the striatum of the rat , 1993, Neuroscience.

[21]  J. Walsh Depression of excitatory synaptic input in rat striatal neurons , 1993, Brain Research.

[22]  P. Calabresi,et al.  Post-receptor mechanisms underlying striatal long-term depression , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  A. Grace,et al.  Identification and characterization of striatal cell subtypes using in vivo intracellular recording in rats. I. Basic physiology and response to corticostriatal fiber stimulation , 1994, Synapse.

[24]  A. Graybiel Building action repertoires: memory and learning functions of the basal ganglia , 1995, Current Opinion in Neurobiology.

[25]  S Laroche,et al.  Stimulation at 1-5 Hz does not produce long-term depression or depotentiation in the hippocampus of the adult rat in vivo. , 1995, Journal of neurophysiology.

[26]  Joel L. Davis,et al.  Adaptive Critics and the Basal Ganglia , 1995 .

[27]  J. Wickens,et al.  Dopamine reverses the depression of rat corticostriatal synapses which normally follows high-frequency stimulation of cortex In vitro , 1996, Neuroscience.

[28]  P. Calabresi,et al.  The corticostriatal projection: from synaptic plasticity to dysfunctions of the basal ganglia , 1996, Trends in Neurosciences.

[29]  S. Charpier,et al.  The lamellar organization of the rat substantia nigra pars reticulata: Segregated patterns of striatal afferents and relationship to the topography of corticostriatal projections , 1996, Neuroscience.

[30]  H. Kita Glutamatergic and gabaergic postsynaptic responses of striatal spiny neurons to intrastriatal and cortical stimulation recorded in slice preparations , 1996, Neuroscience.