Skip to main content

Advertisement

SpringerLink
Log in

Effects of pallidal neurotensin on haloperidol-induced parkinsonian catalepsy: behavioral and electrophysiological studies

苍白球神经降压素对氟哌啶醇所致帕金森病僵直症状的影响: 行为学和电生理学研究

  • Original Article
  • Published:
Neuroscience Bulletin Aims and scope Submit manuscript

Abstract

Objective

The globus pallidus plays a critical role in movement regulation. Previous studies have indicated that the globus pallidus receives neurotensinergic innervation from the striatum, and systemic administration of a neurotensin analog could produce antiparkinsonian effects. The present study aimed to investigate the effects of pallidal neurotensin on haloperidol-induced parkinsonian symptoms.

Methods

Behavioral experiments and electrophysiological recordings were performed in the present study.

Results

Bilateral infusions of neurotensin into the globus pallidus reversed haloperidolinduced parkinsonian catalepsy in rats. Electrophysiological recordings showed that microinjection of neurotensin induced excitation of pallidal neurons in the presence of systemic haloperidol administration. The neurotensin type-1 receptor antagonist SR48692 blocked both the behavioral and the electrophysiological effects induced by neurotensin.

Conclusion

Activation of pallidal neurotensin receptors may be involved in neurotensin-induced antiparkinsonian effects.

摘要

目的

苍白球在机体运动功能调节中发挥重要作用。 形态学研究证实苍白球接受来自纹状体的神经降压素能纤维支配。 有研究报道全身给予神经降压素类似物可诱导产生抗帕金森病效应。 本研究旨在探讨苍白球神经降压素对氟哌啶醇所致的帕金森病僵直症状的影响。

方法

用行为学实验检测大鼠的帕金森病僵直症状, 用电生理学实验方法记录苍白球神经元的自发放频率。

结果

双侧苍白球微量注射神经降压素可以缓解氟哌啶醇所致的帕金森病僵直症状。 在氟哌啶醇条件下, 微量注射神经降压素可以兴奋苍白球神经元。 选择性神经降压素1 型受体拮抗剂SR48692可以拮抗神经降压素所致的行为学和电生理学效应。

结论

上述结果提示, 神经降压素的抗帕金森病作用可能与苍白球神经降压素受体的激活有关。

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Mounayar S, Boulet S, Tandé D, Jan C, Pessiglione M, Hirsch EC, et al. A new model to study compensatory mechanisms in MPTP-treated monkeys exhibiting recovery. Brain 2007, 130: 2898–2914.

    Article  PubMed  Google Scholar 

  2. Bolam JP, Hanley JJ, Booth PAC, Bevan MD. Synaptic organisation of the basal ganglia. J Anat 2000, 196: 527–542.

    Article  PubMed  CAS  Google Scholar 

  3. Smith Y, Bevan MD, Shink E, Bolam JP. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 1998, 86: 353–387.

    Article  PubMed  CAS  Google Scholar 

  4. Kita H. Responses of globus pallidus neurons to cortical stimulation: intracellular study in the rat. Brain Res 1992, 589: 84–90.

    Article  PubMed  CAS  Google Scholar 

  5. Kita H, Kitai ST. Intracellular study of rat globus pallidus neurons: membrane properties and responses to neostriatal, subthalamic and nigral stimulation. Brain Res 1991, 564: 296–305.

    Article  PubMed  CAS  Google Scholar 

  6. Parent A, Hazrati LN. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Brain Res Rev 1995, 20: 128–154.

    Article  PubMed  CAS  Google Scholar 

  7. Kita H, Kita T. Number, origins, and chemical types of rat pallidostriatal projection neurons. J Comp Neurol 2001, 437: 438–448.

    Article  PubMed  CAS  Google Scholar 

  8. Parent A, Sato F, Wu Y, Gauthier J, Levesque M, Parent M. Organization of the basal ganglia: the importance of axonal collateralization. Trends Neurosci 2000, 23: S20–S27.

    Article  PubMed  CAS  Google Scholar 

  9. El-Deredy W, Branston NM, Samuel M, Schrag A, Rothwell JC, Thomas DG, et al. Firing patterns of pallidal cells in parkinsonian patients correlate with their pre-pallidotomy clinical scores. Neuroreport 2000, 11: 3413–3418.

    Article  PubMed  CAS  Google Scholar 

  10. Soares J, Kliem MA, Betarbet R, Greenamyre JT, Yamamoto B, Wichmann T. Role of external pallidal segment in primate parkinsonism: comparison of the effects of 1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine-induced parkinsonism and lesions of the external pallidal segment. J Neurosci 2004, 24: 6417–6426.

    Article  PubMed  CAS  Google Scholar 

  11. Starr PA, Rau GM, Davis V, Marks WJ Jr., Ostrem JL, Simmons D, et al. Spontaneous pallidal neuronal activity in human dystonia: comparison with Parkinson’s disease and normal macaque. J Neurophysiol 2005, 93: 3165–3176.

    Article  PubMed  Google Scholar 

  12. Bergman H, Feingold A, Nini A, Raz A, Slovin H, Abeles M, et al. Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci 1998, 21: 32–38.

    Article  PubMed  CAS  Google Scholar 

  13. Magnin M, Morel A, Jeanmonod D. Single-unit analysis of the pallidum, thalamus and subthalamic nucleus in parkinsonian patients. Neuroscience 2000, 96: 549–564.

    Article  PubMed  CAS  Google Scholar 

  14. Raz A, Vaadia E, Bergman H. Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine vervet model of parkinsonism. J Neurosci 2000, 20: 8559–8571.

    PubMed  CAS  Google Scholar 

  15. Wichmann T, Soares J. Neuronal firing before and after burst discharges in the monkey basal ganglia is predictably patterned in the normal state and altered in parkinsonism. J Neurophysiol 2006, 95: 2120–2133.

    Article  PubMed  CAS  Google Scholar 

  16. Carraway R, Leeman SE. The isolation of a new hypotensive peptide, neurotensin, from bovine hypothalami. J Biol Chem 1973, 248: 6854–6861.

    PubMed  CAS  Google Scholar 

  17. Mendez M, Souaze F, Nagano M, Kelly PA, Rostene W, Forgez P. High affinity neurotensin receptor mRNA distribution in rat brain and peripheral tissues. Analysis by quantitative RT-PCR. J Mol Neurosci 1997, 9: 93–102.

    Article  PubMed  CAS  Google Scholar 

  18. Tyler-McMahon BM, Boules M, Richelson E. Neurotensin: peptide for the next millennium. Regul Pept 2000, 93: 125–136.

    Article  PubMed  CAS  Google Scholar 

  19. Vincent JP. Neurotensin receptors: binding properties, transduction pathways, and structure. Cell Mol Neurobiol 1995, 15: 501–512.

    Article  PubMed  CAS  Google Scholar 

  20. Chalon P, Vita N, Kaghad M, Guillemot M, Bonnin J. Molecular cloning of a levocabastine-sensitive neurotensin binding site. FEBS Lett 1996, 386: 91–94.

    Article  PubMed  CAS  Google Scholar 

  21. Mazella J, Zsurger N, Navarro V, Chabry J, Kaghad M, Caput D. The 100-kDa neurotensin receptor is gp95/sortilin, a non-G-protein-coupled receptor. J Biol Chem 1998, 273: 26273–26276.

    Article  PubMed  CAS  Google Scholar 

  22. Tanaka K, Masu M, Nakanishi S. Structure and functional expression of the cloned rat neurotensin receptor. Neuron 1990, 4: 847–854.

    Article  PubMed  CAS  Google Scholar 

  23. Fassio A, Evans G, Grisshammer R, Bolam JP, Mimmack M, Emson PC. Distribution of the neurotensin receptor NTS1 in the rat CNS studied using an amino-terminal directed antibody. Neuropharmacology 2000, 39: 1430–1442.

    Article  PubMed  CAS  Google Scholar 

  24. Sarret P, Perron A, Stroh T, Beaudet A. Immunohistochemical distribution of NTS2 neurotensin receptors in the rat central nervous system. J Comp Neurol 2003, 461: 520–538.

    Article  PubMed  CAS  Google Scholar 

  25. Martorana A, Martella G, D’Angelo V, Fusco FR, Spadoni F, Bernardi G, et al. Neurotensin effects on N-type calcium currents among rat pallidal neurons: an electrophysiological and immunohistochemical study. Synapse 2006, 60: 371–383.

    Article  PubMed  CAS  Google Scholar 

  26. Chinaglia G, Probst A, Palacios JM. Neurotensin receptors in Parkinson’s disease and progressive supranuclear palsy: an autoradiographic study in basal ganglia. Neuroscience 1990, 39: 351–360.

    Article  PubMed  CAS  Google Scholar 

  27. Fernandez A, de Ceballos ML, Jenner P, Marsden CD. Neurotensin, substance P, delta and mu opioid receptors are decreased in basal ganglia of Parkinson’s disease patients. Neuroscience 1994, 61: 73–79.

    Article  PubMed  CAS  Google Scholar 

  28. Boules M, Warrington L, Fauq A, McCormick D, Richelson E. Antiparkinson-like effects of a novel neurotensin analog in unilaterally 6-hydroxydopamine lesioned rats. Eur J Pharmacol 2001, 428: 227–233.

    Article  PubMed  CAS  Google Scholar 

  29. Schmidt WJ, Mayerhofer A, Meyer A, Kovar KA. Ecstasy counteracts catalepsy in rats, an anti-parkinsonian effect? Neurosci Lett 2002, 330: 251–254.

    Article  PubMed  CAS  Google Scholar 

  30. Chen L, Yung KK, Yung WH. Neurotensin depolarizes globus pallidus neurons in rats via neurotensin type-1 receptor. Neuroscience 2004, 125: 853–859.

    Article  PubMed  CAS  Google Scholar 

  31. Xue Y, Chen L, Cui QL, Xie JX, Yung WH. Electrophysiological and behavioral effects of neurotensin in rat globus pallidus: an in vivo study. Exp Neurol 2007, 205: 108–115.

    Article  PubMed  CAS  Google Scholar 

  32. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. New York: Academic Press, 1986.

    Google Scholar 

  33. Querejeta E, Oviedo-Chavez A, Araujo-Alvarez JM, Quinones-Cardenas AR, Delgado A. In vivo effects of local activation and blockade of 5-HT1B receptors on globus pallidus neuronal spiking. Brain Res 2005, 1043: 186–194.

    Article  PubMed  CAS  Google Scholar 

  34. Kelland MD, Soltis RP, Anderson LA, Bergstrom DA, Walters JR. In vivo characterization of two cell types in the rat globus pallidus which have opposite responses to dopamine receptor stimulation: comparison of electrophysiological properties and responses to apomorphine, dizocilpine, and ketamine anesthesia. Synapse 1995, 20: 338–350.

    Article  PubMed  CAS  Google Scholar 

  35. Ruskin DN, Rawji SS, Walters JR. Effects of full D1 dopamine receptor agonists on firing rates in the globus pallidus and substantia nigra pars compacta in vivo: tests for D1 receptor selectivity and comparisons to the partial agonist SKF 38393. J Pharmacol Exp Ther 1998, 286: 272–281.

    PubMed  CAS  Google Scholar 

  36. Zahm DS, Heimer L. Ventral striatopallidal parts of the basal ganglia in the rat: I. Neurochemical compartmentation as reflected by the distributions of neurotensin and substance P immunoreactivity. J Comp Neurol 1988, 272: 516–535.

    Article  PubMed  CAS  Google Scholar 

  37. Fernandez A, Jenner P, Marsden CD, De Ceballos ML. Characterization of neurotensin-like immunoreactivity in human basal ganglia: increased neurotensin levels in substantia nigra in Parkinson’s disease. Peptides 1995, 16: 339–346.

    Article  PubMed  CAS  Google Scholar 

  38. Martorana A, Fusco FR, D’Angelo V, Sancesario G, Bernardi G. Enkephalin, neurotensin, and substance P immunoreactivite neurones of the rat GP following 6-hydroxydopamine lesion of the substantia nigra. Exp Neurol 2003, 183: 311–319.

    Article  PubMed  CAS  Google Scholar 

  39. DeLong MR. Primate models of movement disorders of basal ganglia origin. Trends Neurosci 1990, 13: 281–285.

    Article  PubMed  CAS  Google Scholar 

  40. Lorenc-Koci E, Wolfarth S, Ossowska K. Haloperidol-increased muscle tone in rats as a model of parkinsonian rigidity. Exp Brain Res 1996, 109: 268–276.

    Article  PubMed  CAS  Google Scholar 

  41. Marino MJ, Valenti O, Conn PJ. Glutamate receptors and Parkinson’s disease. Drugs Aging 2003, 20: 377–397.

    Article  PubMed  CAS  Google Scholar 

  42. Xue Y, Bai B, Yung WH, Chen L. Electrophysiological effects of neurotensin on globus pallidus neurons of 6-hydroxydopaminelesioned rats. Neurosignals 2009, 17: 153–161.

    Article  PubMed  CAS  Google Scholar 

  43. Kasckow J, Nemeroff CB. The neurobiology of neurotensin: focus on neurotensin-dopamine interactions. Regul Pept 1991, 36: 153–164.

    Article  PubMed  CAS  Google Scholar 

  44. Dana C, Vial M, Leonard K, Beauregard A, Kitabgi P, Vincent JP. Electron microscopic localization of neurotensin binding sites in the midbrain tegmentum of the rat. I. Ventral tegmental area and the interfascicular nucleus. J Neurosci 1989, 9: 2247–2257.

    PubMed  CAS  Google Scholar 

  45. Tanji H, Araki T, Fujihara K, Nagasawa H, Itoyama Y. Alteration of neurotensin receptors in MPTP-treated mice. Peptides 1999, 20: 803–807.

    Article  PubMed  CAS  Google Scholar 

  46. Boudin H, Pe’laprat D, Roste’ne W, Pickel VM, Beaudet A. Correlative ultrastructural distribution of neurotensin receptor proteins and binding sites in the rat substantia nigra. J Neurosci 1998, 18: 8473–8484.

    PubMed  CAS  Google Scholar 

  47. Drumheller AD, Gagné MA, St-Pierre S, Jolicoeur FB. Effects of neurotensin on regional brain concentrations of dopamine, serotonin and their main metabolites. Neuropeptides 1990, 15: 169–178.

    Article  PubMed  CAS  Google Scholar 

  48. Napier TC, Gay DA, Hulebak KL, Breese GR. Behavioral and biochemical assessment of time-related changes in globus pallidus and striatal dopamine induced by intranigrally administered neurotensin. Peptides 1985, 6: 1057–1068.

    Article  PubMed  CAS  Google Scholar 

  49. Ikegami M, Ichitani Y, Takahashi T, Iwasaki T. Compensatory increase in extracellular dopamine in the nucleus accumbens of adult rats with neonatal 6-hydroxydopamine treatment. Nihon Shinkei Seishin Yakurigaku Zasshi 2006, 26: 111–117.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology, Qingdao University, Qingdao, 266071, China

    Yan Xue  (薛雁) & Lei Chen  (陈蕾)

Authors
  1. Yan Xue  (薛雁)
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lei Chen  (陈蕾)
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lei Chen  (陈蕾).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xue, Y., Chen, L. Effects of pallidal neurotensin on haloperidol-induced parkinsonian catalepsy: behavioral and electrophysiological studies. Neurosci. Bull. 26, 345–354 (2010). https://doi.org/10.1007/s12264-010-0518-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12264-010-0518-y

Keywords

关键词

Search

Navigation