Functional state of corticostriatal synapses determines their expression of short‐ and long‐term plasticity

Relationships between presynaptic function and short‐ and long‐term plasticity were investigated at adult corticostriatal synapses. Wide variability was observed in the expression of short‐ and long‐term synaptic plasticity. Intracellular records from 47 cells produced 17 examples of LTD (<90% of control), 10 examples of no long‐term change (between 90–110% of control), and 20 examples of LTP (>110% of control). Similar variation existed in paired‐pulse and posttetanic plasticities. The variability expressed in all three forms of plasticity appears to be related, based on correlations found between the paired‐pulse ratio (PPR) and tetanus‐induced short‐ (3 min posttetanus) and long‐term plasticities (16–20 min posttetanus). These data suggest that tetanus‐induced changes in synaptic strength are related to the intrinsic, preconditioned behavior of synapses. Every cell showing paired‐pulse depression also expressed LTD in response to high‐frequency activation of its afferents. Those synapses showing paired‐pulse potentiation tended to express LTP, although exceptions did exist. Similar relationships were found in a parallel analysis of population spikes. PPR also changed in association with the expression of posttetanic and long‐term depression. Greater paired‐pulse potentiation was observed in medial intracellular recordings, but no medial to lateral differences were seen in posttetanic plasticities. Field recordings also showed a medial bias toward paired‐pulse and posttetanic potentiation, but not in long‐term plasticity. Block of postsynaptic L‐type Ca2+ channels with nifedipine eliminated LTD expression, but overall no differences were found between nifedipine and control cells. Synapse 38:271–280, 2000. © 2000 Wiley‐Liss, Inc.

[1]  B. Katz,et al.  The role of calcium in neuromuscular facilitation , 1968, The Journal of physiology.

[2]  L. Squire,et al.  Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. , 1980, Science.

[3]  S. Redman,et al.  Post‐tetanic potentiation and facilitation of synaptic potentials evoked in cat spinal motoneurones. , 1981, The Journal of physiology.

[4]  R. Beninger The role of dopamine in locomotor activity and learning , 1983, Brain Research Reviews.

[5]  J. Bower,et al.  Facilitating and nonfacilitating synapses on pyramidal cells: a correlation between physiology and morphology. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Grzegorz Hess,et al.  Quantal analysis of paired-pulse facilitation in guinea pig hippocampal slices , 1987, Neuroscience Letters.

[7]  J. Joyce,et al.  Quantitative autoradiography of dopamine D2 sites in rat caudate-putamen: Localization to intrinsic neurons and not to neocortical afferents , 1987, Neuroscience.

[8]  A. Mcgeorge,et al.  The organization of the projection from the cerebral cortex to the striatum in the rat , 1989, Neuroscience.

[9]  C. Stevens,et al.  Presynaptic mechanism for long-term potentiation in the hippocampus , 1990, Nature.

[10]  M. Delong,et al.  Primate models of movement disorders of basal ganglia origin , 1990, Trends in Neurosciences.

[11]  R. Tsien,et al.  Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices , 1990, Nature.

[12]  M. Chesselet,et al.  Heterogeneous distribution of dopamine D2 receptor mRNA in the rat striatum: A quantitative analysis with in situ hybridization histochemistry , 1991, The Anatomical record.

[13]  K. Zipser,et al.  Role of residual calcium in synaptic depression and posttetanic potentiation: Fast and slow calcium signaling in nerve terminals , 1991, Neuron.

[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]  R. Malinow,et al.  The probability of transmitter release at a mammalian central synapse , 1993, Nature.

[16]  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.

[17]  Christian Rosenmund,et al.  Nonuniform probability of glutamate release at a hippocampal synapse. , 1993, Science.

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

[19]  R. Zucker,et al.  Residual Ca2 + and short-term synaptic plasticity , 1994, Nature.

[20]  R. Nicoll,et al.  Long-term potentiation: evidence against an increase in transmitter release probability in the CA1 region of the hippocampus. , 1994, Science.

[21]  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.

[22]  D. Johnston,et al.  Changes in paired-pulse facilitation suggest presynaptic involvement in long-term potentiation , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  W. Abraham,et al.  Differential regulation of paired-pulse plasticity following LTP in the dentate gyrus. , 1994, Neuroreport.

[24]  R. Malinow,et al.  LTP: desperately seeking resolution. , 1994, Science.

[25]  Y. Miyashita,et al.  Two distinct glutamatergic synaptic inputs to striatal medium spiny neurones of neonatal rats and paired‐pulse depression. , 1994, The Journal of physiology.

[26]  A. C. Greenwood,et al.  Quantal mechanism of long-term potentiation in hippocampal mossy-fiber synapses. , 1994, Journal of neurophysiology.

[27]  D W Tank,et al.  A quantitative measurement of the dependence of short-term synaptic enhancement on presynaptic residual calcium , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  R. Traystman,et al.  Global incomplete cerebral ischemia produces predominantly cortical neuronal injury. , 1995, Stroke.

[29]  Marc G. Weisskopf,et al.  Presynaptic changes during mossy fibre LTP revealed by NMDA receptor-mediated synaptic responses , 1995, Nature.

[30]  Jon W. Johnson,et al.  Posttetanic potentiation and presynaptically induced long-term potentiation at the mossy fiber synapse in rat hippocampus. , 1995, Journal of neurobiology.

[31]  S. Siegelbaum,et al.  Regulation of hippocampal transmitter release during development and long-term potentiation. , 1995, Science.

[32]  U. Kuhnt,et al.  Changes in paired-pulse facilitation correlate with induction of long-term potentiation in area CA1 of rat hippocampal slices , 1996, Neuroscience.

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

[34]  D. Willingham,et al.  Motor Skills Have Diverse Neural Bases: Spared and Impaired Skill Acquisition in Huntington's Disease , 1996 .

[35]  Jane S. Paulsen,et al.  Dissociations within nondeclarative memory in Huntington's disease. , 1996 .

[36]  I. Divac,et al.  Representation of a single vibrissa in the rat neostriatum: peaks of energy metabolism reveal a distributed functional module , 1996, Neuroscience.

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

[38]  Jennifer A. Mangels,et al.  A Neostriatal Habit Learning System in Humans , 1996, Science.

[39]  D. Carpenter,et al.  Interactions among paired‐pulse facilitation and post‐tetanic and long‐term potentiation in the mossy fiber‐CA3 pathway in rat hippocampus , 1996, Synapse.

[40]  S. Young,et al.  Glutamate-dependent long-term presynaptic changes in corticostriatal excitability , 1996, Neuroscience.

[41]  T. Manabe,et al.  Presynaptic Long-Term Depression at the Hippocampal Mossy Fiber--CA3 Synapse , 1996, Science.

[42]  D. Johnston,et al.  The role of dendritic action potentials and Ca2+ influx in the induction of homosynaptic long-term depression in hippocampal CA1 pyramidal neurons. , 1996, Learning & memory.

[43]  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.

[44]  Molecule Promises a Better Buckyball , 1996 .

[45]  T. Tsumoto,et al.  Quantal analysis suggests presynaptic involvement in expression of neocortical short- and long-term depression. , 1997, Neuroscience.

[46]  D. Lovinger,et al.  Decreased Frequency But Not Amplitude of Quantal Synaptic Responses Associated with Expression of Corticostriatal Long-Term Depression , 1997, The Journal of Neuroscience.

[47]  J. Galen Buckwalter,et al.  Age‐related change in short‐term synaptic plasticity intrinsic to excitatory striatal synapses , 1997, Synapse.

[48]  C. Stevens,et al.  Heterogeneity of Release Probability, Facilitation, and Depletion at Central Synapses , 1997, Neuron.

[49]  D. Lovinger,et al.  Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[50]  T. Schikorski,et al.  Quantitative Ultrastructural Analysis of Hippocampal Excitatory Synapses Materials and Methods Terminology Fixation and Embedding , 2022 .

[51]  T. Sejnowski,et al.  Heterogeneous Release Properties of Visualized Individual Hippocampal Synapses , 1997, Neuron.

[52]  W. Singer,et al.  Relations Between Long‐term Synaptic Modifications and Paired‐pulse Interactions in the Rat Neocortex , 1997, The European journal of neuroscience.

[53]  W. Abraham,et al.  Induction and reversal of long‐term potentiation by repeated high‐frequency stimulation in rat hippocampal slices , 1997, Hippocampus.

[54]  P. Kelly,et al.  Attenuation of paired-pulse facilitation associated with synaptic potentiation mediated by postsynaptic mechanisms. , 1997, Journal of neurophysiology.

[55]  O. Hikosaka,et al.  Differential roles of monkey striatum in learning of sequential hand movement , 1997, Experimental Brain Research.

[56]  S. Charpier,et al.  In vivo activity-dependent plasticity at cortico-striatal connections: evidence for physiological long-term potentiation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[57]  D. Shear,et al.  Comparison of intrastriatal injections of quinolinic acid and 3-nitropropionic acid for use in animal models of Huntington's disease , 1998, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[58]  J. Gabrieli Cognitive neuroscience of human memory. , 1998, Annual review of psychology.

[59]  M. Bunsey,et al.  Differential Effects of Dorsal and Ventral Hippocampal Lesions , 1998, The Journal of Neuroscience.

[60]  M. Jüptner,et al.  A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. , 1998, Brain : a journal of neurology.

[61]  M. Moser,et al.  Functional differentiation in the hippocampus , 1998, Hippocampus.

[62]  K. Reymann,et al.  Interaction between paired-pulse facilitation and long-term potentiation of minimal excitatory postsynaptic potentials in rat hippocampal slices: A patch-clamp study , 1998, Neuroscience.

[63]  O. Hikosaka,et al.  Expectation of reward modulates cognitive signals in the basal ganglia , 1998, Nature Neuroscience.

[64]  S. Sahrmann,et al.  Cognitive and motor functioning in Parkinson disease: subjects with and without questionable dementia. , 1998, Archives of neurology.

[65]  J. Walsh,et al.  Modulation of long-term synaptic plasticity at excitatory striatal synapses , 1999, Neuroscience.

[66]  S. Charpier,et al.  In vivo induction of striatal long-term potentiation by low-frequency stimulation of the cerebral cortex , 1999, Neuroscience.

[67]  C F Stevens,et al.  Quantitative fine-structural analysis of olfactory cortical synapses. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[68]  P. Calabresi,et al.  A Critical Role of the Nitric Oxide/cGMP Pathway in Corticostriatal Long-Term Depression , 1999, The Journal of Neuroscience.