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Erschienen in: Brain Structure and Function 9/2016

07.12.2015 | Short Communication

A single-neuron tracing study of arkypallidal and prototypic neurons in healthy rats

verfasst von: Fumino Fujiyama, Takashi Nakano, Wakoto Matsuda, Takahiro Furuta, Jun Udagawa, Takeshi Kaneko

Erschienen in: Brain Structure and Function | Ausgabe 9/2016

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Abstract

The external globus pallidus (GP) is known as a relay nucleus of the indirect pathway of the basal ganglia. Recent studies in dopamine-depleted and healthy rats indicate that the GP comprises two main types of pallidofugal neurons: the so-called “prototypic” and “arkypallidal” neurons. However, the reconstruction of complete arkypallidal neurons in healthy rats has not been reported. Here we visualized the entire axonal arborization of four single arkypallidal neurons and six single prototypic neurons in rat brain using labeling with a viral vector expressing membrane-targeted green fluorescent protein and examined the distribution of axon boutons in the target nuclei. Results revealed that not only the arkypallidal neurons but nearly all of the prototypic neurons projected to the striatum with numerous axon varicosities. Thus, the striatum is a major target nucleus for pallidal neurons. Arkypallidal and prototypic GP neurons located in the calbindin-positive and calbindin-negative regions mainly projected to the corresponding positive and negative regions in the striatum. Because the GP and striatum calbindin staining patterns reflect the topographic organization of the striatopallidal projection, the striatal neurons in the sensorimotor and associative regions constitute the reciprocal connection with the GP neurons in the corresponding regions.
Literatur
Zurück zum Zitat Abdi A, Mallet N, Mohamed FY, Sharott A, Dodson PD, Nakamura KC, Suri S, Avery SV, Larvin JT, Garas FN, Garas SN, Vinciati F, Morin S, Bezard E, Baufreton J, Magill PJ (2015) Prototypic and arkypallidal neurons in the dopamine-intact external globus pallidus. J Neurosci 35:6667–6688CrossRefPubMedPubMedCentral Abdi A, Mallet N, Mohamed FY, Sharott A, Dodson PD, Nakamura KC, Suri S, Avery SV, Larvin JT, Garas FN, Garas SN, Vinciati F, Morin S, Bezard E, Baufreton J, Magill PJ (2015) Prototypic and arkypallidal neurons in the dopamine-intact external globus pallidus. J Neurosci 35:6667–6688CrossRefPubMedPubMedCentral
Zurück zum Zitat Baufreton J, Kirkham E, Atherton JF, Menard A, Magill PJ, Bolam JP, Bevan MD (2009) Sparse but selective and potent synaptic transmission from the globus pallidus to the subthalamic nucleus. J Neurophysiol 102:532–545CrossRefPubMedPubMedCentral Baufreton J, Kirkham E, Atherton JF, Menard A, Magill PJ, Bolam JP, Bevan MD (2009) Sparse but selective and potent synaptic transmission from the globus pallidus to the subthalamic nucleus. J Neurophysiol 102:532–545CrossRefPubMedPubMedCentral
Zurück zum Zitat Bevan MD, Booth PA, Eaton SA, 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 PA, Eaton SA, 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
Zurück zum Zitat Bevan MD, Magill PJ, Terman D, Bolam JP, Wilson CJ (2002) Move to the rhythm: oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci 25:525–531CrossRefPubMed Bevan MD, Magill PJ, Terman D, Bolam JP, Wilson CJ (2002) Move to the rhythm: oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci 25:525–531CrossRefPubMed
Zurück zum Zitat Dodson PD, Larvin JT, Duffell JM, Garas FN, Doig NM, Kessaris N, Duguid IC, Bogacz R, Butt SJB, Magill PJ (2015) Distinct developmental origins manifest in the specialized encoding of movement by adult neurons of the external globus pallidus. Neuron 86:501–513CrossRefPubMedPubMedCentral Dodson PD, Larvin JT, Duffell JM, Garas FN, Doig NM, Kessaris N, Duguid IC, Bogacz R, Butt SJB, Magill PJ (2015) Distinct developmental origins manifest in the specialized encoding of movement by adult neurons of the external globus pallidus. Neuron 86:501–513CrossRefPubMedPubMedCentral
Zurück zum Zitat Flandin P, Kimura S, Rubenstein JLR (2010) The Progenitor zone of the ventral medial ganglionic eminence requires Nk2-1 to generate most of the globus pallidus but few neocortical interneurons. J Neurosci 30:2812–2823CrossRefPubMedPubMedCentral Flandin P, Kimura S, Rubenstein JLR (2010) The Progenitor zone of the ventral medial ganglionic eminence requires Nk2-1 to generate most of the globus pallidus but few neocortical interneurons. J Neurosci 30:2812–2823CrossRefPubMedPubMedCentral
Zurück zum Zitat Fujiyama F, Sohn J, Nakano T, Furuta T, Nakamura KC, Matsuda W, Kaneko T (2011) Exclusive and common targets of neostriatofugal projections of rat striosome neurons: a single neuron-tracing study using a viral vector. Eur J Neurosci 33:668–677CrossRefPubMed Fujiyama F, Sohn J, Nakano T, Furuta T, Nakamura KC, Matsuda W, Kaneko T (2011) Exclusive and common targets of neostriatofugal projections of rat striosome neurons: a single neuron-tracing study using a viral vector. Eur J Neurosci 33:668–677CrossRefPubMed
Zurück zum Zitat Furuta T, Tomioka R, Taki K, Nakamura K, Tamamaki N, Kaneko T (2001) In vivo transduction of central neurons using recombinant Sindbis virus: Golgi-like labeling of dendrites and axons with membrane-targeted fluorescent proteins. J Histochem Cytochem 49:1497–1508CrossRefPubMed Furuta T, Tomioka R, Taki K, Nakamura K, Tamamaki N, Kaneko T (2001) In vivo transduction of central neurons using recombinant Sindbis virus: Golgi-like labeling of dendrites and axons with membrane-targeted fluorescent proteins. J Histochem Cytochem 49:1497–1508CrossRefPubMed
Zurück zum Zitat Gerfen CR (1985) The neostriatal mosaic. I. Compartmental organization of projections from the striatum to the substantia nigra in the rat. J Comp Neurol 236:454–476CrossRefPubMed Gerfen CR (1985) The neostriatal mosaic. I. Compartmental organization of projections from the striatum to the substantia nigra in the rat. J Comp Neurol 236:454–476CrossRefPubMed
Zurück zum Zitat Gittis AH, Berke JD, Bevan MD, Chan CS, Mallet N, Morrow MM, Schmidt R (2014) New roles for the external globus pallidus in basal ganglia circuits and behavior. J Neurosci 34:15178–15183CrossRefPubMedPubMedCentral Gittis AH, Berke JD, Bevan MD, Chan CS, Mallet N, Morrow MM, Schmidt R (2014) New roles for the external globus pallidus in basal ganglia circuits and behavior. J Neurosci 34:15178–15183CrossRefPubMedPubMedCentral
Zurück zum Zitat Hontanilla B, Parent A, Giménez-Amaya JM (1997) Parvalbumin and calbindin D-28k in the entopeduncular nucleus, subthalamic nucleus, and substantia nigra of the rat as revealed by double-immunohistochemical methods. Synapse 25:359–367CrossRefPubMed Hontanilla B, Parent A, Giménez-Amaya JM (1997) Parvalbumin and calbindin D-28k in the entopeduncular nucleus, subthalamic nucleus, and substantia nigra of the rat as revealed by double-immunohistochemical methods. Synapse 25:359–367CrossRefPubMed
Zurück zum Zitat Hoover BR, Marshall JF (2002) Further characterization of preproenkephalin mRNA-containing cells in the rodent globus pallidus. Neuroscience 111:111–125CrossRefPubMed Hoover BR, Marshall JF (2002) Further characterization of preproenkephalin mRNA-containing cells in the rodent globus pallidus. Neuroscience 111:111–125CrossRefPubMed
Zurück zum Zitat Kaneko T, Caria MA, Asanuma H (1994) Information processing within the motor cortex. II. Intracortical connections between neurons receiving somatosensory cortical input and motor output neurons of the cortex. J Comp Neurol 345:172–184CrossRefPubMed Kaneko T, Caria MA, Asanuma H (1994) Information processing within the motor cortex. II. Intracortical connections between neurons receiving somatosensory cortical input and motor output neurons of the cortex. J Comp Neurol 345:172–184CrossRefPubMed
Zurück zum Zitat Kita H, Kita T (2001) Number, origins, and chemical types of rat pallidostriatal projection neurons. J Comp Neurol 437:438–448CrossRefPubMed Kita H, Kita T (2001) Number, origins, and chemical types of rat pallidostriatal projection neurons. J Comp Neurol 437:438–448CrossRefPubMed
Zurück zum Zitat Kita H, Kitai ST (1994) The morphology of globus pallidus projection neurons in the rat: an intracellular staining study. Brain Res 636:308–319CrossRefPubMed Kita H, Kitai ST (1994) The morphology of globus pallidus projection neurons in the rat: an intracellular staining study. Brain Res 636:308–319CrossRefPubMed
Zurück zum Zitat Koshimizu Y, Fujiyama F, Nakamura KC, Furuta T, Kaneko T (2013) Quantitative analysis of axon bouton distribution of subthalamic nucleus neurons in the rat by single neuron visualization with a viral vector. J Comp Neurol 521:2125–2146CrossRefPubMed Koshimizu Y, Fujiyama F, Nakamura KC, Furuta T, Kaneko T (2013) Quantitative analysis of axon bouton distribution of subthalamic nucleus neurons in the rat by single neuron visualization with a viral vector. J Comp Neurol 521:2125–2146CrossRefPubMed
Zurück zum Zitat Kuramoto E, Furuta T, Nakamura KC, Unzai T, Hioki H, Kaneko T (2009) Two types of thalamocortical projections from the motor thalamic nuclei of the rat: a single neuron-tracing study using viral vectors. Cereb Cortex 19:2065–2077CrossRefPubMed Kuramoto E, Furuta T, Nakamura KC, Unzai T, Hioki H, Kaneko T (2009) Two types of thalamocortical projections from the motor thalamic nuclei of the rat: a single neuron-tracing study using viral vectors. Cereb Cortex 19:2065–2077CrossRefPubMed
Zurück zum Zitat Mallet N, Micklem BR, Henny P, Brown MT, Williams C, Bolam JP, Nakamura KC, Magill PJ (2012) Dichotomous organization of the external globus pallidus. Neuron 74:1075–1086CrossRefPubMedPubMedCentral Mallet N, Micklem BR, Henny P, Brown MT, Williams C, Bolam JP, Nakamura KC, Magill PJ (2012) Dichotomous organization of the external globus pallidus. Neuron 74:1075–1086CrossRefPubMedPubMedCentral
Zurück zum Zitat Mastro KJ, Bouchard RS, Holt HAK, Gittis AH (2014) Transgenic mouse lines subdivide external segment of the globus pallidus (GPe) neurons and reveal distinct GPe output pathways. J Neurosci 34:2087–2099CrossRefPubMedPubMedCentral Mastro KJ, Bouchard RS, Holt HAK, Gittis AH (2014) Transgenic mouse lines subdivide external segment of the globus pallidus (GPe) neurons and reveal distinct GPe output pathways. J Neurosci 34:2087–2099CrossRefPubMedPubMedCentral
Zurück zum Zitat Matsuda W, Furuta T, Nakamura KC, Hioki H, Fujiyama F, Arai R, Kaneko T (2009) Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. J Neurosci 29:444–453CrossRefPubMed Matsuda W, Furuta T, Nakamura KC, Hioki H, Fujiyama F, Arai R, Kaneko T (2009) Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. J Neurosci 29:444–453CrossRefPubMed
Zurück zum Zitat Nambu A, Linás R (1994) Electrophysiology of globus pallidus neurons in vitro. J Neurophysiol 72:1127–1139PubMed Nambu A, Linás R (1994) Electrophysiology of globus pallidus neurons in vitro. J Neurophysiol 72:1127–1139PubMed
Zurück zum Zitat Nambu A, Linás R (1997) Morphology of globus pallidus neurons; its correlation with electrophysiology in guinea pig brain slices. J Comp Neurol 377:85–94CrossRefPubMed Nambu A, Linás R (1997) Morphology of globus pallidus neurons; its correlation with electrophysiology in guinea pig brain slices. J Comp Neurol 377:85–94CrossRefPubMed
Zurück zum Zitat Ohno S, Kuramoto E, Furuta T, Hioki H, Tanaka YR, Fujiyama F, Sonomura T, Uemura M, Sugiyama K, Kaneko T (2012) A morphological analysis of thalamocortical axon fibers of rat posterior thalamic nuclei: a single neuron tracing study with viral vectors. Cereb Cortex 22:2840–2857CrossRefPubMed Ohno S, Kuramoto E, Furuta T, Hioki H, Tanaka YR, Fujiyama F, Sonomura T, Uemura M, Sugiyama K, Kaneko T (2012) A morphological analysis of thalamocortical axon fibers of rat posterior thalamic nuclei: a single neuron tracing study with viral vectors. Cereb Cortex 22:2840–2857CrossRefPubMed
Zurück zum Zitat Prensa I, Parent A (2001) The nigrostriatal pathway in the rat: a single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J Neurosci 21:7247–7260PubMed Prensa I, Parent A (2001) The nigrostriatal pathway in the rat: a single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J Neurosci 21:7247–7260PubMed
Zurück zum Zitat Rajakumar N, Rushlow W, Naus CC, Elisevich K, Flumerfelt BA (1994) Neurochemical compartmentalization of the globus pallidus in the rat: an immunocytochemical study of calcium-binding proteins. J Comp Neurol 346:337–348CrossRefPubMed Rajakumar N, Rushlow W, Naus CC, Elisevich K, Flumerfelt BA (1994) Neurochemical compartmentalization of the globus pallidus in the rat: an immunocytochemical study of calcium-binding proteins. J Comp Neurol 346:337–348CrossRefPubMed
Zurück zum Zitat Sadek AR, Magill PJ, Bolam JP (2007) A single-cell analysis of intrinsic connectivity in the rat globus pallidus. J Neurosci 27:6352–6362CrossRefPubMed Sadek AR, Magill PJ, Bolam JP (2007) A single-cell analysis of intrinsic connectivity in the rat globus pallidus. J Neurosci 27:6352–6362CrossRefPubMed
Zurück zum Zitat Sato F, Lavallée P, Lévesque M, Parent A (2000) Single-axon tracing study of neurons of the external segment of the globus pallidus in primate. J Comp Neurol 417:17–31CrossRefPubMed Sato F, Lavallée P, Lévesque M, Parent A (2000) Single-axon tracing study of neurons of the external segment of the globus pallidus in primate. J Comp Neurol 417:17–31CrossRefPubMed
Zurück zum Zitat Smith Y, Bevan MD, Shink E, Bolam JP (1998) Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86:353–387CrossRefPubMed Smith Y, Bevan MD, Shink E, Bolam JP (1998) Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86:353–387CrossRefPubMed
Zurück zum Zitat Stephenson-Jones M, Samuelsson E, Ericsson J, Robertson B, Grillner S (2011) Evolutionary conservation of the basal ganglia as a common vertebrate mechanism for action selection. Curr Biol 21:1081–1091CrossRefPubMed Stephenson-Jones M, Samuelsson E, Ericsson J, Robertson B, Grillner S (2011) Evolutionary conservation of the basal ganglia as a common vertebrate mechanism for action selection. Curr Biol 21:1081–1091CrossRefPubMed
Metadaten
Titel
A single-neuron tracing study of arkypallidal and prototypic neurons in healthy rats
verfasst von
Fumino Fujiyama
Takashi Nakano
Wakoto Matsuda
Takahiro Furuta
Jun Udagawa
Takeshi Kaneko
Publikationsdatum
07.12.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 9/2016
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-015-1152-2

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