Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Substantia nigra stimulation evoked antidromic responses in rat neostriatum

  • 45 Accesses

  • 20 Citations

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.

This is a preview of subscription content, log in to check access.

References

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

  2. 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

  3. 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

  4. 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

  5. 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

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

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

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

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

  10. 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

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

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

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

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

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

  16. 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

  17. 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

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

  19. 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

  20. 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

  21. 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

  22. 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

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

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

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

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

  27. 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

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

  29. 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

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

  31. 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

  32. 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

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

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

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

  36. 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

  37. 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

  38. 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

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

  40. 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

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

  42. 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

  43. 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

  44. 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

  45. 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

  46. 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

Download references

Author information

Correspondence to L. J. Ryan.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

Key words

  • Substantia nigra
  • Neostriatum
  • Antidromic responses