Substance P Excites Large Aspiny Neurons of the Rat Neostriatum

  • Toshihiko Aosaki
  • Yasuo Kawaguchi
Part of the Advances in Behavioral Biology book series (ABBI, volume 47)

Abstract

Substance P (SP) is widely distributed in the mammalian central nervous system, where it is believed to play important roles as a neurotransmitter/neuromodulator. In the striatum, it has been reported that SP-containing fibers and terminals originate mainly from the striatonigral medium-sized spiny projection neurons (Bolam et al., 1986). Although the striatonigral pathway neurons were found to innervate both the pars reticulata of the substantia nigra (SNr) and the external segment of the globus pallidus (GPe), some of them also innervating the internal segment of the globus pallidus (GPi)/entopeduncular nucleus (EP) (Kawaguchi et al., 1990), in situ hybridization and immunohistochemical studies revealed that the receptor for SP, the NK1 receptor, is expressed only by the medium-sized somatostatinergic and large cholinergic interneurons of the striatum (Kaneko et al., 1993; Shigemoto et al., 1993; Aubry et al., 1994; Parent et al., 1995). How SP, released from the intrastriatal collaterals of the striatonigral medium-sized spiny neurons, affects these interneurons is an important question for the understanding of the function of the striatum, because they may in turn modulate the activities of the spiny projection neurons. However, no physiological evidence of such actions of SP has hitherto been available. Here, we report that SP excites the interneurons mainly by opening non-selective cation channels and discuss its functional significance.

Keywords

Medium Spiny Neuron Cholinergic Interneuron Entopeduncular Nucleus Parafascicular Nucleus Neostriatal Neuron 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Akins, P. T., Surmeier, D. J. and Kitai, S. T., 1990, Muscarinic modulation of a transient K+ conductance in rat neostriatal neurons, Nature 344: 240–242.PubMedCrossRefGoogle Scholar
  2. Alexander, G. E. and Crutcher, M. D., 1990, Functional architecture of basal ganglia circuits: neural substrates of parallel processing, Trends Neurosci. 13(7): 266–271.PubMedCrossRefGoogle Scholar
  3. Aosaki, T., Graybiel, A. M. and Kimura, M, 1994, Effects of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys, Science 265: 412–415.PubMedCrossRefGoogle Scholar
  4. Aosaki, T. and Kawaguchi, Y., 1995, Actions of neuropeptides on large aspiny neurons of rat neostriatum in vitro, Soc. Neurosci. Abstr. 21: 913.Google Scholar
  5. Aubry, J. M., Lundstroem, K., Kawashima, E., Ayala, G., Schulz, P., Bartaunusz, V. and Kiss, J. Z., 1994, NK1 receptor expression by cholinergic interneurons in human striatum, Neuroreport 5: 1597–1600.PubMedCrossRefGoogle Scholar
  6. Bolam, J. P., Ingham, C. A., Izzo, P. N., Levey, A. I., Rye, D. B., Smith, A. D. and Wainer, B. H., 1986, Substance P-containing terminals in synaptic contact with cholinergic neurons in the neostriatum and basal forebrain: a double immunocytochemical study in the rat, Brain Res. 397: 279–289.PubMedCrossRefGoogle Scholar
  7. Calabresi, P., Maj, R., Pisani, A., Mercuri, N. B. and Bernardi, G., 1992, Long-term synaptic depression in the striatum: physiological and pharmacological characterization, J. Neurosci. 12: 4224–4233.PubMedGoogle Scholar
  8. Gerfen, C. R., 1992, The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia, Ann. Rev. Neurosci. 15: 285–320.CrossRefGoogle Scholar
  9. Graybiel, A. M., Aosaki, T., Flaherty, A. W. and Kimura, M., 1994, The basal ganglia and adaptive motor control, Science 265: 1826–1831.PubMedCrossRefGoogle Scholar
  10. Guevara Guzman, R., Kendrick, K. M. and Emson, P. C., 1993, Effect of substance P on acetylcholine and dopamine release in the rat striatum: a microdialysis study, Brain Res 622: 147–154.CrossRefGoogle Scholar
  11. Inoue, K., Nakazawa, K., Inoue, K. and Fujimori, K., 1995, Nonselective cation channels coupled with tachykinin receptors in rat sensory neurons, J. Neurophysiol. 73: 736–742.Google Scholar
  12. Jaeger, D., Kita, H. and Wilson, C. J., 1995, Surround inhibition among projection neurons is weak or nonexistent in the rat neostriatum, J. Neurophysiol. 72: 2555–2558.Google Scholar
  13. Jiang, Z. G. and North, R. A., 1992, Pre-and postsynaptic inhibition by opioids in rat striatum. J. Neurosci. 12:356–361.PubMedGoogle Scholar
  14. Kaneko, T., Shigemoto, R., Nakanishi, S. and Mizuno, N., 1993, Substance Preceptor-immunoreactive neurons in the rat neostriatum are segregated into somatostatinergic and cholinergic aspiny neurons, Brain Res. 631:297–303.PubMedCrossRefGoogle Scholar
  15. Kawaguchi, Y., 1992, Large aspiny cells in the matrix of the rat neostriatum in vitro: physiological identification, relation to the compartments and excitatory postsynaptic currents, J. Neurophysiol. 67: 1669–1682.PubMedGoogle Scholar
  16. Kawaguchi, Y., 1993, Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum, J. Neurosci. 13: 4908–4923.PubMedGoogle Scholar
  17. Kawaguchi, Y., Wilson, C. J. and Emson, P. C., 1990, Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin, J. Neurosci. 10: 3421–3438.PubMedGoogle Scholar
  18. Lapper SR, Bolam JP (1992) Input from prefrontal cortex and the parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat. Neuroscience 51: 533–545.PubMedCrossRefGoogle Scholar
  19. Parent, A., Cicchetti, F. and Beach, T. G., 1995, Striatal neurones displaying substance P (NK1) receptor immunoreactivity in human and non-human primates, Neuroreport 6: 721–724.PubMedCrossRefGoogle Scholar
  20. Shen, K. Z. and North, R. A., 1992, Substance P opens cation channels and closes potassium channels in rat locus coeruleus neurons, Neuroscience, 50: 345–353.PubMedCrossRefGoogle Scholar
  21. Shigemoto, R., Nakaya, Y., Nomura, S., Ogawa-Meguro, R., Ohishi, H., Kaneko, T., Nakanishi, S. and Mizuno, N., 1993, Immunocytochemical localization of rat substance P receptor in the striatum, Neurosci. Lett. 153: 157–160.PubMedCrossRefGoogle Scholar
  22. Wilson, C. J., 1993, The generation of natural firing patterns in neostriatal neurons, in: Progress in brain research, Chemical signalling in the basal ganglia, (G. W. Arbuthnott, P. C. Emson, eds.), Elsevier, Amsterdam, pp. 277–297.CrossRefGoogle Scholar
  23. Wilson, C. J., Chang, H. T. and Kitai, S.T., 1990, Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum, J. Neurosci. 10: 508–519.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1996

Authors and Affiliations

  • Toshihiko Aosaki
    • 1
  • Yasuo Kawaguchi
    • 1
  1. 1.Laboratory for Neural Circuits, Bio-Mimetic Control Research CenterThe Institute of Physical and Chemical Research (RIKEN)Nagoya, Aichi 456Japan

Personalised recommendations