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Substantia nigra stimulation evoked antidromic responses in rat neostriatum

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Summary

Electrical stimulation of the substantia nigra of rats elicits a burst of small amplitude waves with a latency of 4–6 ms that may last for 10–15 ms throughout much of the neostriatum. Frontal cortex stimulation also elicits a burst response, which can occlude the substantia nigra response. The substantia nigra evoked burst response was still present after chronic neocortical ablation or thalamic transection or both treatments combined. The response corresponds to the first sharp negative wave of the substantia nigra evoked neostriatal field potential. Single substantia nigra evoked action potentials were recorded in neostriatum with a mean latency of 9.8 ms, ranging from 4–22 ms. These action potentials were considered to be antidromic because 1) they were occluded during appropriate collision intervals by orthodromic action potentials elicited by frontal cortex stimulation. Subthreshold frontal cortex conditioning stimulation did not alter the threshold for activation from substantia nigra. The refractory period for the axon was at least as long as that for the soma and ranged between 0.8–2.0 ms. The antidromic responses failed to follow low frequency stimulation (< 40 Hz for 3000 ms). This failure occurred in the axon between substantia nigra and globus pallidus. The burst response and first sharp negative wave of the field potential probably represent the antidromic activation of the ubiquitous and densely packed medium spiny neostriatal projection neurons. These responses 1) occur at the same latency, 2) respond in the same manner to twin pulse and repetitive stimulation and 3) are occluded by frontal cortex stimulation in the same manner as antidromic action potentials.

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References

  • Barker JL, Crayton JW, Nicoll RA (1971) Antidromic and orthodromic responses of paraventricular and supraoptic neurosecretory cells. Brain Res 33: 353–366

    Google Scholar 

  • Bolam JP, Powell JF, Totterdell S, Smith AD (1981) The proportion of neurons in the rat neostriatum that project to the substantia nigra demonstrated using horseradish peroxidase conjugated with wheatgerm agglutinin. Brain Res 220: 339–343

    Google Scholar 

  • Bolam JP, Somogyi P, Takagi H, Fodor I, Smith AD (1983) Localization of substance P-like immunoreactivity in neurons and nerve terminals in the neostriatum of the rat: a correlated light and electron microscopic study. J Neurocytol 12: 325–344

    Google Scholar 

  • Bunney BS, Aghajanian GK (1976) The precise localization of nigral afferents in the rat as determined by a retrograde tracing technique. Brain Res 117: 423–435

    Google Scholar 

  • Chang HT, Wilson CJ, Kitai ST (1981) Single neostriatal efferent axons in the globus pallidus: a light and electron microscopic study. Science 213: 915–918

    Google Scholar 

  • Collingridge GL, James TA, MacLeod NK (1980) Antidromic latency variations of nigral compacta neurons. Experientia 36: 970–971

    Google Scholar 

  • Davies J, Tongroach P (1978) Neuropharmacological studies on the nigro-striatal and raphé-striatal system in the rat. Eur J Pharmacol 51: 91–100

    Google Scholar 

  • Deniau JM, Feger J, de Guyader C (1976) Striatal evoked inhibition of identified nigro-thalamic neurons. Brain Res 104: 152–156

    Google Scholar 

  • Feltz P, Albe-Fessard D (1972) A study of an ascending nigrocaudate pathway. Electroenceph Clin Neurophysiol 33: 179–193

    Google Scholar 

  • Feltz P, De Champlain J (1972) Persistence of caudate unitary responses to nigral stimulation after destruction and functional impairment of striatal dopaminergic terminals. Brain Res 43: 595–600

    Google Scholar 

  • Feltz P, MacKenzie JS (1969) Properties of caudate unitary responses to repetitive nigral stimulation. Brain Res 13: 612–616

    Google Scholar 

  • Frigyesi TL, Purpura DP (1967) Electrophysiological analysis of reciprocal caudato-nigra relations. Brain Res 6: 440–456

    Google Scholar 

  • Fuller JH, Schlag JD (1976) Determination of antidromic excitation by the collision test; problems of interpretation. Brain Res 112: 283–298

    Google Scholar 

  • Fuller DRG, Hull CD, Buchwald NA (1975) Intracellular responses of caudate output neurons to orthodromic stimulation. Brain Res 96: 337–341

    Google Scholar 

  • Gerfen CR (1984) The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems. Nature 311: 461–464

    Google Scholar 

  • Graybiel AM, Ragsdale CW, Moon Edley S (1979) Compartments in the striatum of the cat observed by retrograde cell labelling. Exp Brain Res 34: 189–195

    Google Scholar 

  • Grofova I (1975) The identification of striatal and pallidal neurons projecting to substantia nigra. An experimental study by means of retrograde axonal transport of horseradish peroxidase. Brain Res 91: 286–291

    Google Scholar 

  • Grofova I (1979) Types of striatonigral neurons labeled by retrograde transport of horseradish peroxidase. Appl Neurophysiol 42: 25–28

    Google Scholar 

  • Groves PM, Fenster GA, Tepper JM, Nakamura S, Young SJ (1982) Changes in dopaminergic terminal excitability induced by apomorphine and haloperidol. Brain Res 221: 425–431

    Google Scholar 

  • Groves PM (1983) A theory of the functional organization of the neostriatum and the neostriatal control of voluntary movement. Brain Res Rev 5: 109–132

    Google Scholar 

  • Jessel TM, Emson PC, Paxinos G, Cuello A (1978) Topographical projections of substance P and GABA pathways in the striato and pallido-nigral system: a biochemical and immunohistochemical study. Brain Res 152: 487–498

    Google Scholar 

  • Kemp JM, Powell TPS (1971) The structure of the caudate nucleus of the cat: light and electron microscopy. Philos Trans R Soc Lond B 262: 413–427

    Google Scholar 

  • Kitai ST, Kocsis JD (1979) The caudate projection neurons in cat. Appl Neurophysiol 42: 29–30

    Google Scholar 

  • Kitai ST, Wagner A, Precht W, Ohno T (1975) Nigro-caudate and caudato-nigral relationship: an electrophysiological study. Brain Res 85: 44–48

    Google Scholar 

  • Kocsis JD, Kitai ST (1977) Dual excitatory inputs to caudate spiny neurons from substantia nigra stimulation. Brain Res 138: 271–283

    Google Scholar 

  • Kocsis JD, VanderMaelen CP (1979) A supernormal period in central axons following single cell stimulation. Exp Brain Res 36: 381–386

    Google Scholar 

  • Konig JFR, Klippel RA (1963) The rat brain, a stereotaxic atlas of the lower forebrain and lower parts of the brain stem. Williams and Wilkins, Baltimore MD

    Google Scholar 

  • Lehmann K, Andreas K (1979) Pharmakologische Beeinflussung von ausgelosten Caudatus-Potentialen. Acta Biol Med Germ 38: 1323–1330

    Google Scholar 

  • Lighthall JW, Kitai ST (1983) A short duration GABAergic inhibition in identified neostriatal medium spiny neurons: in vitro slice study. Brain Res Bull 11: 103–110

    Google Scholar 

  • Lighthall JW, Park MR, Kitai ST (1981) Inhibition in slices of rat neostriatum. Brain Res 212: 182–187

    Google Scholar 

  • Liles SL (1974) Single-unit-responses of caudate neurons to stimulation of frontal cortex, substantia nigra and entopeduncular nucleus in cats. J Neurophysiol 37: 254–265

    Google Scholar 

  • Matsuda Y, Jinnai K (1980) Afferent inputs to caudate output neurons as monitored by antidromic spike invasion of the cell soma. Brain Res 188: 560–565

    Google Scholar 

  • Mercer LF, Remley NR (1978) Combined solution of ketamine and chloral hydrate as an anesthetic. Physiol Behav 20: 495–496

    Google Scholar 

  • Park MR, Lighthall JW, Kitai ST (1980) Recurrent inhibition in the rat neostriatum. Brain Res 194: 359–369

    Google Scholar 

  • Pazo JH (1977) Substantia nigra and somatosensory evoked responses in the caudate nucleus. Acta Physiol Latinoam 27: 333–338

    Google Scholar 

  • Preston RJ, Bishop GA, Kitai ST (1980) Medium spiny neuron projection from the rat neostriatum: an intracellular horseradish peroxidase study. Brain Res 183: 253–263

    Google Scholar 

  • Quiron R, Dam T-V (1985) Multiple tachykinin receptors in guinea pig brain. High densities of substance K (neurokinin A) binding sites in the substantia nigra. Neuropeptides 6: 191–204

    Google Scholar 

  • Ribak CE, Vaughn JE, Roberts E (1979) The GABA neurons and their own axon terminals in rat corpus striatum as demonstrated by GAD immunocytochemistry. J Comp Neurol 187: 261–284

    Google Scholar 

  • Richardson TL, Miller JJ, McLennan H (1977) Mechanisms of excitation and inhibition in the nigrostriatal system. Brain Res 127: 219–234

    Google Scholar 

  • Somogyi P, Bolam JP, Smith AD (1981) Monosynaptic cortical input and local axon collateral of identified striatonigral neurons. A light and electron microscopic study using the Golgi-peroxidase transport-degeneration procedure. J Comp Neurol 195: 567–584

    Google Scholar 

  • Swadlow HA (1982) Antidromic activation: measuring the refractory period at the site of axonal stimulation. Exp Neurol 75: 514–519

    Google Scholar 

  • Tepper JM, Nakamura S, Young SJ, Groves PM (1984) Autoreceptor-mediated changes in dopaminergic terminal excitability: effects of striatal drug infusions. Brain Res 309: 317–333

    Google Scholar 

  • Wagner A, Dupelj M, Lee KC (1977) The effects of drugs on the field potential in the caudate nucleus following nigra stimulation. Acta Neurochirurgica Suppl 24: 191–198

    Google Scholar 

  • Wilson CJ, Groves PM (1980) Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intracellular injection of horseradish peroxidase. J Comp Neurol 194: 599–615

    Google Scholar 

  • Wilson CJ, Chang HT, Kitai ST (1982) Origins of postsynaptic potentials evoked in identied rat neostriatal neurons by stimulation in substantia nigra. Exp Brain Res 45: 157–167

    Google Scholar 

  • Yeoman RR, Rigor BM, Dafny N (1981) Altered caudate nucleus field potentials following sustained stimulation to different substantia nigra regions. Int J Neurosci 13: 103–111

    Google Scholar 

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Ryan, L.J., Young, S.J. & Groves, P.M. Substantia nigra stimulation evoked antidromic responses in rat neostriatum. Exp Brain Res 63, 449–460 (1986). https://doi.org/10.1007/BF00237469

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  • DOI: https://doi.org/10.1007/BF00237469

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