Skip to main content
Top
Published in: Brain Structure and Function 9/2017

01-12-2017 | Original Article

Substance P effects exclusively on prototypic neurons in mouse globus pallidus

Authors: Kazuko Mizutani, Susumu Takahashi, Shinichiro Okamoto, Fuyuki Karube, Fumino Fujiyama

Published in: Brain Structure and Function | Issue 9/2017

Login to get access

Abstract

Previous studies have suggested that the neurokinin-1 receptor (NK-1R) expressing neurons in the globus pallidus (GP) receive substance P (SP), presumably released by axon collaterals of striatal direct neurons. However, the effect of SP on the GP remains unclear. In this study, we identified that the SP-responsive cells comprise a highly specific cell type in the GP with regard to immunofluorescence, electrophysiology, and projection properties. Morphologically, NK-1R-immunoreactive neurons occasionally co-expressed parvalbumin (PV) and/or Lim-homeobox 6 (Lhx6), but not Forkhead box protein P2 (FoxP2), which is mainly expressed by arkypallidal neurons. Retrograde tracing experiments also showed that some of GP neurons projecting to the subthalamic nucleus (namely prototypic neurons) expressed NK-1R as well as Lhx6 and/or PV, but not FoxP2. In vitro electrophysiological study revealed that, among 48 GP neurons, the SP agonist induced inward current in 21 neurons. The response was prevented by bath application of the NK-1R antagonist. Based on the firing properties, 92 recorded GP neurons were classified into three distinct types, i.e., CL1, 2, and 3. Interestingly, all the SP-responsive neurons were found to be in CL2 and CL3 types, but not in CL1. Moreover, active and passive membrane properties of the neurons in those clusters and immunofluorescent identification suggested that CL1 and CL2/3 could be considered as arkypallidal and prototypic neurons, respectively. Therefore, SP-responsive neurons were one of the populations of prototypic neurons based on both anatomical and electrophysiological results. Altogether, the striatal direct pathway neurons could affect the indirect pathway in the way of prototypic neurons, via the action of SP to NK-1R.
Appendix
Available only for authorised users
Literature
go back to reference Aosaki T, Kawaguchi Y (1996) Actions of substance P on rat neostriatal neurons in vitro. J Neurosci 16:5141–5153PubMed Aosaki T, Kawaguchi Y (1996) Actions of substance P on rat neostriatal neurons in vitro. J Neurosci 16:5141–5153PubMed
go back to reference Bevan MD, Booth P, Eaton S, Bolam JP (1998) Selective innervation of neostriatal interneurons by a subclass of neuron in the globus pallidus of the rat. J Neurosci 18:9438–9452PubMed Bevan MD, Booth P, Eaton S, Bolam JP (1998) Selective innervation of neostriatal interneurons by a subclass of neuron in the globus pallidus of the rat. J Neurosci 18:9438–9452PubMed
go back to reference Furuta T, Koyano K, Tomioka R et al (2004) GABAergic basal forebrain neurons that express receptor for neurokinin B and send axons to the cerebral cortex. J Comp Neurol 473:43–58. doi:10.1002/cne.20087 CrossRefPubMed Furuta T, Koyano K, Tomioka R et al (2004) GABAergic basal forebrain neurons that express receptor for neurokinin B and send axons to the cerebral cortex. J Comp Neurol 473:43–58. doi:10.​1002/​cne.​20087 CrossRefPubMed
go back to reference Futami T, Hatanaka Y, Matsushita K, Furuya S (1998) Expression of substance P receptor in the substantia nigra. Mol Brain Res 54:183–198CrossRefPubMed Futami T, Hatanaka Y, Matsushita K, Furuya S (1998) Expression of substance P receptor in the substantia nigra. Mol Brain Res 54:183–198CrossRefPubMed
go back to reference Gomez-Gallego M, Fernandez-Villalba E, Fernandez-Barreiro A, Herrero MT (2007) Changes in the neuronal activity in the pedunculopontine nucleus in chronic MPTP-treated primates: an in situ hybridization study of cytochrome oxidase subunit I, choline acetyl transferase and substance P mRNA expression. J Neural Transm 114:319–326. doi:10.1007/s00702-006-0547-x CrossRefPubMed Gomez-Gallego M, Fernandez-Villalba E, Fernandez-Barreiro A, Herrero MT (2007) Changes in the neuronal activity in the pedunculopontine nucleus in chronic MPTP-treated primates: an in situ hybridization study of cytochrome oxidase subunit I, choline acetyl transferase and substance P mRNA expression. J Neural Transm 114:319–326. doi:10.​1007/​s00702-006-0547-x CrossRefPubMed
go back to reference Nambu A, Llinás R (1994) Electrophysiology of globus pallidus neurons in vitro. J Neurophysiol 72:1127–1139PubMed Nambu A, Llinás R (1994) Electrophysiology of globus pallidus neurons in vitro. J Neurophysiol 72:1127–1139PubMed
go back to reference Obeso J, Rodríguez-Oroz MC, Benitez-Temino B et al (2008) Functional organization of the basal ganglia: therapeutic implications for Parkinson’s disease. Mov Disord 23(Suppl 3):S548–S559. doi:10.1002/mds.22062 CrossRefPubMed Obeso J, Rodríguez-Oroz MC, Benitez-Temino B et al (2008) Functional organization of the basal ganglia: therapeutic implications for Parkinson’s disease. Mov Disord 23(Suppl 3):S548–S559. doi:10.​1002/​mds.​22062 CrossRefPubMed
go back to reference Paxinos G, Franklin KB (2013) The mouse brain in stereotaxic coordinates, 4th edn. Elsevier, Amsterdam Paxinos G, Franklin KB (2013) The mouse brain in stereotaxic coordinates, 4th edn. Elsevier, Amsterdam
go back to reference Quirion R, Shults CW, Moody TW, Pert CB, Chase TN, O’Donohue TL (1983) Autoradiographic distribution of substance P receptors in rat central nervous system. Nature 303:714–716. doi:10.1038/303714a0 CrossRefPubMed Quirion R, Shults CW, Moody TW, Pert CB, Chase TN, O’Donohue TL (1983) Autoradiographic distribution of substance P receptors in rat central nervous system. Nature 303:714–716. doi:10.​1038/​303714a0 CrossRefPubMed
go back to reference Role LW (1984) Substance P modulation of acetylcholine-induced currents in embryonic chicken sympathetic and ciliary ganglion neurons. Proc Natl Acad Sci USA 81:2924–2928CrossRefPubMedPubMedCentral Role LW (1984) Substance P modulation of acetylcholine-induced currents in embryonic chicken sympathetic and ciliary ganglion neurons. Proc Natl Acad Sci USA 81:2924–2928CrossRefPubMedPubMedCentral
go back to reference Sosulina L, Strippel C, Romo-Parra H et al (2015) Substance P excites GABAergic neurons in the mouse central amygdala through neurokinin 1 receptor activation. J Neurophysiol. doi:10.1152/jn.00883.2014 Sosulina L, Strippel C, Romo-Parra H et al (2015) Substance P excites GABAergic neurons in the mouse central amygdala through neurokinin 1 receptor activation. J Neurophysiol. doi:10.​1152/​jn.​00883.​2014
go back to reference Ward JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58:236–244CrossRef Ward JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58:236–244CrossRef
go back to reference Whitty CJ, Walker PD, Goebel DJ, Poosch MS, Bannon MJ (1995) Quantitation, cellular localization and regulation of neurokinin receptor gene expression within the rat substantia nigra. Neurosci 64:419–425. doi:10.1016/0306-4522(94)00373-D CrossRef Whitty CJ, Walker PD, Goebel DJ, Poosch MS, Bannon MJ (1995) Quantitation, cellular localization and regulation of neurokinin receptor gene expression within the rat substantia nigra. Neurosci 64:419–425. doi:10.​1016/​0306-4522(94)00373-D CrossRef
Metadata
Title
Substance P effects exclusively on prototypic neurons in mouse globus pallidus
Authors
Kazuko Mizutani
Susumu Takahashi
Shinichiro Okamoto
Fuyuki Karube
Fumino Fujiyama
Publication date
01-12-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 9/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1453-8

Other articles of this Issue 9/2017

Brain Structure and Function 9/2017 Go to the issue