The glutamate‐enriched cortical and thalamic input to neurons in the subthalamic nucleus of the rat: Convergence with GABA‐positive terminals

Neurons of the subthalamic nucleus play a key role in the normal physiology and the pathophysiology of the basal ganglia. In order to understand better how the activity of subthalamic neurons and hence the output of the basal ganglia are controlled, we have reexamined the topography and examined in detail the synaptology and neurochemical nature of the two major excitatory projections to the subthalamic nucleus, that from the cortex and from the parafascicular nucleus of the thalamus. The approach was to use anterograde neuronal tracing and postembedding immunocytochemistry for amino acid transmitters.

[1]  H. Kita,et al.  Electrical membrane properties of rat subthalamic neurons in an in vitro slice preparation , 1987, Brain Research.

[2]  A. Reiner,et al.  Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies , 1992, Journal of Neuroscience Methods.

[3]  P. Somogyi,et al.  Antisera to gamma-aminobutyric acid. I. Production and characterization using a new model system. , 1985, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[4]  Y. Smith,et al.  Topographical and Synaptic Organization of the GABA‐Containing Pallidosubthalamic Projection in the Rat , 1990, The European journal of neuroscience.

[5]  M. Mouroux,et al.  Evidence that the parafascicular projection to the subthalamic nucleus is glutamatergic. , 1993, Neuroreport.

[6]  R. Hassler,et al.  Effect of frontal cortex ablation on striatal glutamic acid level in rat , 1977, Brain Research.

[7]  T. Hattori,et al.  Single subthalamic nucleus neurons project to both the globus pallidus and substantia nigra in rat , 1980, The Journal of comparative neurology.

[8]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[9]  C. Hammond,et al.  Intracellular labelling of rat subthalamic neurones with horseradish peroxidase: Computer analysis of dendrites and characterization of axon arborization , 1983, Neuroscience.

[10]  André Parent,et al.  Neurons of the subthalamic nucleus in primates display glutamate but not GABA immunoreactivity , 1988, Brain Research.

[11]  A. Parent,et al.  Efferent projections of the subthalamic nucleus in the squirrel monkey as studied by the PHA‐L anterograde tracing method , 1990, The Journal of comparative neurology.

[12]  V. I. Novoselov,et al.  The release of labeledl-glutamic acid from rat neostriatum In vivo following stimulation of frontal cortex , 1980, Neuroscience.

[13]  R. Weinberg,et al.  Antibodies to glutamate and aspartate recognize non-endogenous ligands for excitatory amino acid receptors , 1990, Brain Research.

[14]  H. Kita,et al.  Efferent projections of the subthalamic nucleus in the rat: Light and electron microscopic analysis with the PHA‐L method , 1987, The Journal of comparative neurology.

[15]  N. Canteras,et al.  Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat , 1990, Brain Research.

[16]  Y. Smith,et al.  The striatum and the globus pallidus send convergent synaptic inputs onto single cells in the entopeduncular nucleus of the rat: A double anterograde labelling study combined with postembedding immunocytochemistry for GABA , 1992, The Journal of comparative neurology.

[17]  H. Bergman,et al.  Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. , 1990, Science.

[18]  A. D. Smith,et al.  Descending Projections from the Substantia Nigra and Retrorubral Field to the Medullary and Pontomedullary Reticular Formation , 1991, The European journal of neuroscience.

[19]  R. Weinberg,et al.  Glutamate in thalamic fibers terminating in layer IV of primary sensory cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  Y. Smith,et al.  Convergence of synaptic terminals from the striatum and the globus pallidus onto single neurones in the substantia nigra and the entopeduncular nucleus. , 1993, Progress in brain research.

[21]  I. Mitchell,et al.  A 2-deoxyglucose study of the effects of dopamine agonists on the parkinsonian primate brain. Implications for the neural mechanisms that mediate dopamine agonist-induced dyskinesia. , 1992, Brain : a journal of neurology.

[22]  J. Bolam,et al.  Convergent Synaptic Input From the Neostriatum and the Subthalamus Onto Identified Nigrothalamic Neurons in the Rat , 1994, The European journal of neuroscience.

[23]  M. Delong,et al.  Altered Tonic Activity of Neurons in the Globus Pallidus and Subthalamic Nucleus in the Primate MPTP Model of Parkinsonism , 1987 .

[24]  J. Bolam,et al.  Neurons projecting from the entopeduncular nucleus to the thalamus receive convergent synaptic inputs from the subthalamic nucleus and the neostriatum in the rat , 1994, Brain Research.

[25]  S. Haber,et al.  Organization of the output of the ventral striatopallidal system in the rat: Ventral pallidal efferents , 1993, Neuroscience.

[26]  H. Bergman,et al.  The primate subthalamic nucleus. I. Functional properties in intact animals. , 1994, Journal of neurophysiology.

[27]  M R DeLong,et al.  The primate subthalamic nucleus. III. Changes in motor behavior and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of parkinsonism. , 1994, Journal of neurophysiology.

[28]  Y. Smith,et al.  Convergence of synaptic inputs from the striatum and the globus pallidus onto identified nigrocollicular cells in the rat: A double anterograde labelling study , 1991, Neuroscience.

[29]  R. M. Beckstead.  The thalamostriatal projection in the cat , 1984, The Journal of comparative neurology.

[30]  T. Hattori,et al.  Confirmation of thalamosubthalamic projections by electron microscopic autoradiography , 1983, Brain Research.

[31]  A. Crossman,et al.  Primate models of dyskinesia: The experimental approach to the study of basal ganglia-related involuntary movement disorders , 1987, Neuroscience.

[32]  P. Somogyi,et al.  Quantification of immunogold labelling reveals enrichment of glutamate in mossy and parallel fibre terminals in cat cerebellum , 1986, Neuroscience.

[33]  H. Kita,et al.  Intracellular study of rat entopeduncular nucleus neurons in an in vitro slice preparation: response to subthalamic stimulation , 1991, Brain Research.

[34]  M. King,et al.  Biocytin: a versatile anterograde neuroanatomical tract-tracing alternative , 1989, Brain Research.

[35]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[36]  P. Somogyi,et al.  The Journal of Histochemistry and Cytochemistry Copyright Iii. Demonstration of Gaba in Golgi-impregnated Neurons and in Conventional Electron Microscopic Sections of Cat Striate Cortex' , 2022 .

[37]  J. Deniau,et al.  Cortical inputs to the subthalamus: intracellular analysis , 1981, Brain Research.

[38]  O. Ottersen,et al.  Terminals of subthalamonigral fibres are enriched with glutamate-like immunoreactivity: An electron microscopic, immunogold analysis in the cat , 1993, Journal of Chemical Neuroanatomy.

[39]  Okihide Hikosaka,et al.  Visual and oculomotor functions of monkey subthalamic nucleus. , 1992 .

[40]  R. Weinberg,et al.  Techniques to optimize post-embedding single and double staining for amino acid neurotransmitters. , 1992, Journal of Histochemistry and Cytochemistry.

[41]  K. Usunoff,et al.  Corticosubthalamic projection in the cat: an electron microscopic study , 1979, Brain Research.

[42]  H. Kita,et al.  Responses of rat substantia nigra pars reticulata units to cortical stimulation , 1992, Neuroscience Letters.

[43]  I. Divac,et al.  Biochemical evidence for glutamate as neurotransmitter in corticostriatal and corticothalamic fibres in rat brain , 1981, Neuroscience.

[44]  R. Wurtz,et al.  Modification of saccadic eye movements by GABA-related substances. II. Effects of muscimol in monkey substantia nigra pars reticulata. , 1985, Journal of neurophysiology.

[45]  T. Hattori,et al.  Direct projections from the centre median‐parafascicular complex to the subthalamic nucleus in the cat and rat , 1983, The Journal of comparative neurology.

[46]  Jean Féger,et al.  The Effects of Activation or Inhibition of the Subthalamic Nucleus on the Metabolic and Electrophysiological Activities Within the Pallidal Complex and Substantia Nigra in the Rat , 1991, The European journal of neuroscience.

[47]  P. Robledo,et al.  Excitatory influence of rat subthalamic nucleus to substantia nigra pars reticulata and the pallidal complex: electrophysiological data , 1990, Brain Research.

[48]  M. Sambrook,et al.  Experimental hemichorea/hemiballismus in the monkey. Studies on the intracerebral site of action in a drug-induced dyskinesia. , 1984, Brain : a journal of neurology.

[49]  H. Kita,et al.  The morphology of intracellularly labeled rat subthalamic neurons: A light microscopic analysis , 1983, The Journal of comparative neurology.

[50]  M. Bevan,et al.  The projections from the parafascicular thalamic nucleus to the subthalamic nucleus and the striatum arise from separate neuronal populations: A comparison with the corticostriatal and corticosubthalamic efferents in a retrograde fluorescent double-labelling study , 1994, Neuroscience.

[51]  B Bioulac,et al.  Reversal of Rigidity and Improvement in Motor Performance by Subthalamic High‐frequency Stimulation in MPTP‐treated Monkeys , 1993, The European journal of neuroscience.

[52]  I. Divac,et al.  High affinity uptake of glutamate in terminals of corticostriatal axons , 1977, Nature.

[53]  J. Penney,et al.  The functional anatomy of basal ganglia disorders , 1989, Trends in Neurosciences.

[54]  E. Scarnati,et al.  Pharmacological study of the cortical-induced excitation of subthalamic nucleus neurons in the rat: Evidence for amino acids as putative neurotransmitters , 1987, Neuroscience.

[55]  T. Aziz,et al.  Lesion of the subthalamic nucleus for the alleviation of 1‐methyl‐4‐phenyl‐1,2,3,6‐tetrahydropyridine (MPTP)‐induced parkinsonism in the primate , 1991, Movement disorders : official journal of the Movement Disorder Society.

[56]  S Afsharpour,et al.  Topographical projections of the cerebral cortex to the subthalamic nucleus , 1985, The Journal of comparative neurology.

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

[58]  F. Conti,et al.  Characterization of antisera to glutamate and aspartate. , 1988, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[59]  R. Weinberg,et al.  Amino acid immunocytochemistry of primary afferent terminals in the rat dorsal horn , 1994, The Journal of comparative neurology.

[60]  P. Petrusz,et al.  Molecular requirements for haften binding to antibodies against glutamate and aspartate , 1992, Neuroscience.

[61]  L. Tremblay,et al.  Responses of pallidal neurons to striatal stimulation in intact waking monkeys , 1989, Brain Research.

[62]  H. Groenewegen,et al.  Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat , 1990, The Journal of comparative neurology.

[63]  Hugh J. Spencer.  Antagonism of cortical excitation of striatal neurons by glutamic acid diethyl ester: Evidence for glutamic acid as an excitatory transmitter in the rat striatum , 1976, Brain Research.

[64]  M. Kudo,et al.  Ultrastructural analyses of afferent terminals in the subthalamic nucleus of the cat with a combined degeneration and horseradish peroxidase tracing method , 1987, The Journal of comparative neurology.

[65]  P. Somogyi,et al.  Antisera to gamma-aminobutyric acid. II. Immunocytochemical application to the central nervous system. , 1985, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.