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Published in: Brain Structure and Function 3/2021

01-04-2021 | Original Article

Inter-fastigial projections along the roof of the fourth ventricle

Authors: Gabriela B. Gómez-González, Ataúlfo Martínez-Torres

Published in: Brain Structure and Function | Issue 3/2021

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Abstract

The fastigial nucleus (FN) is a bilateral cerebellar integrative center for saccadic and vestibular control associated with non-motor functions such as feeding and cardiovascular regulation. In a previous study, we identified a tract of myelinated axons embedded in the subventricular zone (SVZ) that is located between the ependymal cells that form the dorsal wall of the ventricle and the glia limitans at the roof of the fourth ventricle González-González (Sci Rep 2017, 7:40768). Here, we show that this tract of axons, named subventricular axons or SVa, contains projection neurons that bilaterally interconnect both FNs. The approach consisted of the use of a battery of fluorescent neuronal tracers, transgenic mouse lines, and immunohistofluorescence. Our observations show that the SVa belong to a wide network of GABAergic projection neurons mainly located in the medial and caudal region of the FN. The SVa should be considered a part of a continuum of the cerebellar white matter that follows an alternative pathway through the SVZ, a region closely associated with the physiology of the fourth ventricle. This finding adds to our understanding of the complex organization of the FN; however, the function of the interconnection remains to be elucidated.
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Literature
go back to reference Akerboom J, Calderón NC, Tian L, Wabnig S, Prigge M, Tolö J et al (2013) Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front Mol Neurosci 6:1–29CrossRef Akerboom J, Calderón NC, Tian L, Wabnig S, Prigge M, Tolö J et al (2013) Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front Mol Neurosci 6:1–29CrossRef
go back to reference Alvarez-Morujo AJ, Toranzo D, Blazquez JL, Pelaez B, Sanchez A, Pastor FE et al (1992) The ependymal surface of the fourth ventricle of the rat: a combined scanning and transmission electron microscopic study. Histol Histopathol 7:259–266PubMed Alvarez-Morujo AJ, Toranzo D, Blazquez JL, Pelaez B, Sanchez A, Pastor FE et al (1992) The ependymal surface of the fourth ventricle of the rat: a combined scanning and transmission electron microscopic study. Histol Histopathol 7:259–266PubMed
go back to reference Angaut P, Bowsher D (1970) Ascending projections of the medial cerebellar (fastigial) nucleus: an experimental study in the cat. Brain Res 24:49–68PubMedCrossRef Angaut P, Bowsher D (1970) Ascending projections of the medial cerebellar (fastigial) nucleus: an experimental study in the cat. Brain Res 24:49–68PubMedCrossRef
go back to reference Batton RR, Jayaraman A, Ruggiero D, Carpenter MB (1977) Fastigial efferent projections in the monkey: an autoradiographic study. J Comp Neurol 174:281–305PubMedCrossRef Batton RR, Jayaraman A, Ruggiero D, Carpenter MB (1977) Fastigial efferent projections in the monkey: an autoradiographic study. J Comp Neurol 174:281–305PubMedCrossRef
go back to reference Becerra-González M, Varman Durairaj R, Ostos Valverde A, Gualda EJ, Loza-Alvarez P et al (2020) Response to hypoxic preconditioning of glial cells from the roof of the fourth ventricle. Neuroscience 439:211–229PubMedCrossRef Becerra-González M, Varman Durairaj R, Ostos Valverde A, Gualda EJ, Loza-Alvarez P et al (2020) Response to hypoxic preconditioning of glial cells from the roof of the fourth ventricle. Neuroscience 439:211–229PubMedCrossRef
go back to reference Beitz AJ, Chan-Palay V (1979) A Golgi analysis of neuronal organization in the medial cerebellar nucleus of the rat. Neuroscience 4:47–63PubMedCrossRef Beitz AJ, Chan-Palay V (1979) A Golgi analysis of neuronal organization in the medial cerebellar nucleus of the rat. Neuroscience 4:47–63PubMedCrossRef
go back to reference Benagiano V, Rizzi A, Lorusso L, Flace P, Saccia M, Cagiano R et al (2018) The functional anatomy of the cerebrocerebellar circuit: a review and new concepts. J Comp Neurol 526:769–989PubMedCrossRef Benagiano V, Rizzi A, Lorusso L, Flace P, Saccia M, Cagiano R et al (2018) The functional anatomy of the cerebrocerebellar circuit: a review and new concepts. J Comp Neurol 526:769–989PubMedCrossRef
go back to reference Bentivoglio M, Kuypers HG (1982) Divergent axon collaterals from rat cerebellar nuclei to diencephalon, mesencephalon, medulla oblongata and cervical cord. A fluorescent double retrograde labeling study. Exp Brain Res 46:339–356PubMedCrossRef Bentivoglio M, Kuypers HG (1982) Divergent axon collaterals from rat cerebellar nuclei to diencephalon, mesencephalon, medulla oblongata and cervical cord. A fluorescent double retrograde labeling study. Exp Brain Res 46:339–356PubMedCrossRef
go back to reference Berry M, Ibrahim M, Carlile J, Ruge F, Duncan A, Butt AM (1995) Axon-glial relationships in the anterior medullary velum of the adult rat. J Neurocytol 24:965–983PubMedCrossRef Berry M, Ibrahim M, Carlile J, Ruge F, Duncan A, Butt AM (1995) Axon-glial relationships in the anterior medullary velum of the adult rat. J Neurocytol 24:965–983PubMedCrossRef
go back to reference Berry M, Hunter AS, Duncan A, Lordan J, Kirvell S, Tsang WL et al (1998) Axon-glial relations during regeneration of axons in the adult rat anterior medullary velum. J Neurocytol 27:915–937PubMedCrossRef Berry M, Hunter AS, Duncan A, Lordan J, Kirvell S, Tsang WL et al (1998) Axon-glial relations during regeneration of axons in the adult rat anterior medullary velum. J Neurocytol 27:915–937PubMedCrossRef
go back to reference Brocklehurst G (1969) The development of the human cerebrospinal fluid pathway with particular reference to the roof of the fourth ventricle. J Anat 105:467–475PubMedPubMedCentral Brocklehurst G (1969) The development of the human cerebrospinal fluid pathway with particular reference to the roof of the fourth ventricle. J Anat 105:467–475PubMedPubMedCentral
go back to reference Büttner U, Fuchs AF, Markert-Schwab G, Buckmaster P (1991) Fastigial nucleus activity in the alert monkey during slow eye and head movements. J Neurophysiol 65:1360–1371PubMedCrossRef Büttner U, Fuchs AF, Markert-Schwab G, Buckmaster P (1991) Fastigial nucleus activity in the alert monkey during slow eye and head movements. J Neurophysiol 65:1360–1371PubMedCrossRef
go back to reference Canto CB, Witter L, De Zeeuw CI (2016) Whole-cell properties of cerebellar nuclei neurons in vivo. PLoS ONE 11:1–19CrossRef Canto CB, Witter L, De Zeeuw CI (2016) Whole-cell properties of cerebellar nuclei neurons in vivo. PLoS ONE 11:1–19CrossRef
go back to reference Catapano LA, Magavi SSP, Macklis JD (2002) Neuroanatomical tracing of neuronal projections with fluoro-gold. In: Sanberg PR, Sanchez-Ramos JR (eds) Methods mol biol neural stem cells methods and protocols. Humana Press Inc., Totowa Catapano LA, Magavi SSP, Macklis JD (2002) Neuroanatomical tracing of neuronal projections with fluoro-gold. In: Sanberg PR, Sanchez-Ramos JR (eds) Methods mol biol neural stem cells methods and protocols. Humana Press Inc., Totowa
go back to reference Chaudhry FA, Reimer RJ, Bellocchio EE, Danbolt NC, Osen KK, Edwards RH et al (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 18:9733–9750PubMedPubMedCentralCrossRef Chaudhry FA, Reimer RJ, Bellocchio EE, Danbolt NC, Osen KK, Edwards RH et al (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 18:9733–9750PubMedPubMedCentralCrossRef
go back to reference Falcão AM, Marques F, Novais A, Sousa N, Ja P, Sousa JC (2012) The path from the choroid plexus to the subventricular zone: go with the flow! Front Cell Neurosci 6:34PubMedPubMedCentralCrossRef Falcão AM, Marques F, Novais A, Sousa N, Ja P, Sousa JC (2012) The path from the choroid plexus to the subventricular zone: go with the flow! Front Cell Neurosci 6:34PubMedPubMedCentralCrossRef
go back to reference Golanov EV, Regnier-Golanov AS, Britz GW (2017) Integrity of cerebellar fastigial nucleus intrinsic neurons is critical for the global ischemic preconditioning. Brain Sci 7:10CrossRef Golanov EV, Regnier-Golanov AS, Britz GW (2017) Integrity of cerebellar fastigial nucleus intrinsic neurons is critical for the global ischemic preconditioning. Brain Sci 7:10CrossRef
go back to reference González-González MA, Gómez-González GB, González-Becerra M, Martínez-Torres A (2017) Identification of novel cellular clusters define a specialized area in the cerebellar periventricular zone. Sci Rep 7:40768PubMedPubMedCentralCrossRef González-González MA, Gómez-González GB, González-Becerra M, Martínez-Torres A (2017) Identification of novel cellular clusters define a specialized area in the cerebellar periventricular zone. Sci Rep 7:40768PubMedPubMedCentralCrossRef
go back to reference Grosche J, Kettenmann H, Reichenbach A (2002) Bergmann glial cells form distinct morphological structures to interact with cerebellar neurons. J Neu Res 68:138–149CrossRef Grosche J, Kettenmann H, Reichenbach A (2002) Bergmann glial cells form distinct morphological structures to interact with cerebellar neurons. J Neu Res 68:138–149CrossRef
go back to reference Grzanna R, Moliver ME (1979) The locus coeruleus in the rat: an immunohistochemical delineation. Neuroscience 5:21–40CrossRef Grzanna R, Moliver ME (1979) The locus coeruleus in the rat: an immunohistochemical delineation. Neuroscience 5:21–40CrossRef
go back to reference Helmchen C, Straube A, Buttner U (1994) Saccade-related activity in the fastigial oculomotor region of the macaque monkey during spontaneous eye movements in light and darkness. Exp Brain Res 98:474–482PubMedCrossRef Helmchen C, Straube A, Buttner U (1994) Saccade-related activity in the fastigial oculomotor region of the macaque monkey during spontaneous eye movements in light and darkness. Exp Brain Res 98:474–482PubMedCrossRef
go back to reference Homma Y, Nonaka S, Matsuyama K, Mori S (1995) Fastigiofugal projection to the brainstem nuclei in the cat: an anterograde PHA-L tracing study. Neurosci Res 23:89–102PubMedCrossRef Homma Y, Nonaka S, Matsuyama K, Mori S (1995) Fastigiofugal projection to the brainstem nuclei in the cat: an anterograde PHA-L tracing study. Neurosci Res 23:89–102PubMedCrossRef
go back to reference Husson Z, Rousseau CV, Broll I, Zeilhofer HU, Dieudonné S (2014) Differential GABAergic and glycinergic inputs of inhibitory interneurons and Purkinje cells to principal cells of the cerebellar nuclei. J Neurosci 34:9418–9431PubMedPubMedCentralCrossRef Husson Z, Rousseau CV, Broll I, Zeilhofer HU, Dieudonné S (2014) Differential GABAergic and glycinergic inputs of inhibitory interneurons and Purkinje cells to principal cells of the cerebellar nuclei. J Neurosci 34:9418–9431PubMedPubMedCentralCrossRef
go back to reference Ito M (2012) The Cerebellum: brain for an Implicit Self. Pearson Education Inc, New Jersey Ito M (2012) The Cerebellum: brain for an Implicit Self. Pearson Education Inc, New Jersey
go back to reference Katoh YY, Benedek G (2003) Cerebellar fastigial neurons send bifurcating axons to both the left and right superior colliculus in cats. Brain Res 25:246–249CrossRef Katoh YY, Benedek G (2003) Cerebellar fastigial neurons send bifurcating axons to both the left and right superior colliculus in cats. Brain Res 25:246–249CrossRef
go back to reference Katz LC, Burkhalter A, Dreyer WJ (1984) Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 310:498–500PubMedCrossRef Katz LC, Burkhalter A, Dreyer WJ (1984) Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 310:498–500PubMedCrossRef
go back to reference Kheradmand A, Zee DS (2011) Cerebellum and ocular motor control. Front Neurol 1(2):53 Kheradmand A, Zee DS (2011) Cerebellum and ocular motor control. Front Neurol 1(2):53
go back to reference Köbbert C, Apps R, Bechmann I, Lanciego JL, Mey J, Thanos S (2000) Current concepts in neuroanatomical tracing. Prog Neurobiol 62:327–351PubMedCrossRef Köbbert C, Apps R, Bechmann I, Lanciego JL, Mey J, Thanos S (2000) Current concepts in neuroanatomical tracing. Prog Neurobiol 62:327–351PubMedCrossRef
go back to reference Koziol LF, Budding D, Andreasen N, D’Arrigo S, Bulgheroni S, Imamizu H et al (2014) Consensus paper: The cerebellum’s role in movement and cognition. Cerebellum 13:151–177PubMedPubMedCentralCrossRef Koziol LF, Budding D, Andreasen N, D’Arrigo S, Bulgheroni S, Imamizu H et al (2014) Consensus paper: The cerebellum’s role in movement and cognition. Cerebellum 13:151–177PubMedPubMedCentralCrossRef
go back to reference Larsson M (2017) Pax2 is persistently expressed by GABAergic neurons throughout the adult rat dorsal horn. Neurosci Lett 638:96–101PubMedCrossRef Larsson M (2017) Pax2 is persistently expressed by GABAergic neurons throughout the adult rat dorsal horn. Neurosci Lett 638:96–101PubMedCrossRef
go back to reference Louvi A, Alexandre P, Métin C, Wurst W, Wassef M (2003) The isthmic neuroepithelium is essential for cerebellar midline fusion. Development 130:5319–5330PubMedCrossRef Louvi A, Alexandre P, Métin C, Wurst W, Wassef M (2003) The isthmic neuroepithelium is essential for cerebellar midline fusion. Development 130:5319–5330PubMedCrossRef
go back to reference Maricich SM, Herrup K (1999) Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J Neurobiol 41:281–294PubMedCrossRef Maricich SM, Herrup K (1999) Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J Neurobiol 41:281–294PubMedCrossRef
go back to reference Noda H, Sugita S, Ikeda Y (1990) Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey. J Comp Neurol 302:330–348PubMedCrossRef Noda H, Sugita S, Ikeda Y (1990) Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey. J Comp Neurol 302:330–348PubMedCrossRef
go back to reference Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, Kirchhoff F, Kettenmann H (2001) GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33:72–86PubMedCrossRef Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, Kirchhoff F, Kettenmann H (2001) GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33:72–86PubMedCrossRef
go back to reference Oberdick J, Sillitoe RV (2011) Cerebellar zones: history, development, and function. Cerebellum 10:301–306PubMedCrossRef Oberdick J, Sillitoe RV (2011) Cerebellar zones: history, development, and function. Cerebellum 10:301–306PubMedCrossRef
go back to reference Omori O, Umetani T, Sugioka K (1997) Projections from the subdivisions of the fastigial nucleus to the vestibular complex and the prepositus hypoglossal nucleus in the albino rat: an anterograde tracing study using biocytin. Kobe J Med Sci 43(1):37–54PubMed Omori O, Umetani T, Sugioka K (1997) Projections from the subdivisions of the fastigial nucleus to the vestibular complex and the prepositus hypoglossal nucleus in the albino rat: an anterograde tracing study using biocytin. Kobe J Med Sci 43(1):37–54PubMed
go back to reference Pedroarena KM, Kamphausen S (2008) Glycinergic synaptic currents in the deep cerebellar nuclei. Neuropharmacology 54:784–795PubMedCrossRef Pedroarena KM, Kamphausen S (2008) Glycinergic synaptic currents in the deep cerebellar nuclei. Neuropharmacology 54:784–795PubMedCrossRef
go back to reference Porrero C, Rubio-Garrido P, Avendaño C, Clascá F (2010) Mapping of fluorescent protein-expressing neurons and axon pathways in adult and developing Thy1-eYFP-H transgenic mice. Brain Res 1345:59–72PubMedCrossRef Porrero C, Rubio-Garrido P, Avendaño C, Clascá F (2010) Mapping of fluorescent protein-expressing neurons and axon pathways in adult and developing Thy1-eYFP-H transgenic mice. Brain Res 1345:59–72PubMedCrossRef
go back to reference Rasmussen A (1933) Origin and course of the fasciculus uncinatus (Russell) in the cat, with observations on other fiber tracts arising from the cerebellar nuclei. J Comp Neurol 57:165–197CrossRef Rasmussen A (1933) Origin and course of the fasciculus uncinatus (Russell) in the cat, with observations on other fiber tracts arising from the cerebellar nuclei. J Comp Neurol 57:165–197CrossRef
go back to reference Reyes-Haro D, González-González MA, Pétriz A, Rosas-Arellano A, Kettenmann H, Miledi R et al (2013) γ-Aminobutyric acid-ρ expression in ependymal glial cells of the mouse cerebellum. J Neurosci Res 91:527–534PubMedCrossRef Reyes-Haro D, González-González MA, Pétriz A, Rosas-Arellano A, Kettenmann H, Miledi R et al (2013) γ-Aminobutyric acid-ρ expression in ependymal glial cells of the mouse cerebellum. J Neurosci Res 91:527–534PubMedCrossRef
go back to reference Robinson FR, Straube A, Fuchs AF (1993) Role of the caudal fastigial nucleus in saccade generation. II. Effects of muscimol inactivation. J Neurophysiol 70:1741–1758PubMedCrossRef Robinson FR, Straube A, Fuchs AF (1993) Role of the caudal fastigial nucleus in saccade generation. II. Effects of muscimol inactivation. J Neurophysiol 70:1741–1758PubMedCrossRef
go back to reference Schmued LC, Heimer L (1990) Iontophoretic injection of fluoro-gold and other fluorescent tracers. J Histochem Cytochem 38:721–723PubMedCrossRef Schmued LC, Heimer L (1990) Iontophoretic injection of fluoro-gold and other fluorescent tracers. J Histochem Cytochem 38:721–723PubMedCrossRef
go back to reference Siebold C, Glonti L, Glasauer S, Büttner U (1997) Rostral fastigial nucleus activity in the alert monkey during three-dimensional passive head movements. J Neurophysiol 77:1432–1446PubMedCrossRef Siebold C, Glonti L, Glasauer S, Büttner U (1997) Rostral fastigial nucleus activity in the alert monkey during three-dimensional passive head movements. J Neurophysiol 77:1432–1446PubMedCrossRef
go back to reference Uusisaari M, Knöpfel T (2012) Diversity of neuronal elements and circuitry in the cerebellar nuclei. Cerebellum 11:420–421PubMedCrossRef Uusisaari M, Knöpfel T (2012) Diversity of neuronal elements and circuitry in the cerebellar nuclei. Cerebellum 11:420–421PubMedCrossRef
go back to reference Uusisaari M, Obata K, Knöpfel T (2007) Morphological and electrophysiological properties of GABAergic and non-GABAergic cells in the deep cerebellar nuclei. J Neurophysiol 97(1):901–911PubMedCrossRef Uusisaari M, Obata K, Knöpfel T (2007) Morphological and electrophysiological properties of GABAergic and non-GABAergic cells in the deep cerebellar nuclei. J Neurophysiol 97(1):901–911PubMedCrossRef
go back to reference Vercelli A, Repici M, Garbossa D, Grimaldi A (2000) Recent techniques for tracing pathways in the central nervous system of developing and adult mammals. Brain Res Bull 51(1):11–28PubMedCrossRef Vercelli A, Repici M, Garbossa D, Grimaldi A (2000) Recent techniques for tracing pathways in the central nervous system of developing and adult mammals. Brain Res Bull 51(1):11–28PubMedCrossRef
go back to reference Voogd J (1964) The cerebellum of the cat: Structure and fiber connections. Thesis, Leiden. Assen: van Gorcum. Voogd J (1964) The cerebellum of the cat: Structure and fiber connections. Thesis, Leiden. Assen: van Gorcum.
go back to reference Voogd J (1967) Comparative aspects of the structure and fiber connexions of the mammalian cerebellum. In: Fox CA, Snider RS, Leiden S (eds) Progress in Brain Research: Cerebellum. Elsevier, The Netherlands Voogd J (1967) Comparative aspects of the structure and fiber connexions of the mammalian cerebellum. In: Fox CA, Snider RS, Leiden S (eds) Progress in Brain Research: Cerebellum. Elsevier, The Netherlands
go back to reference Voogd J, Jaarsma D, Marani E (1996) The Cerebellum chemoarchitecture and anatomy. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy. Elsevier, The Netherlands Voogd J, Jaarsma D, Marani E (1996) The Cerebellum chemoarchitecture and anatomy. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy. Elsevier, The Netherlands
go back to reference Voogd J, Shinoda Y, Ruigrok TJH, Sugihara I (2013) Cerebellar nuclei and the inferior olivary nuclei: organization and connections. In: Manto M, Schmahmann JD, Rossi F, Gruol DL, Koibuchi N (eds) Handbook of the cerebellum and cerebellar disorders. Springer, Dordrecht, pp 419–421 Voogd J, Shinoda Y, Ruigrok TJH, Sugihara I (2013) Cerebellar nuclei and the inferior olivary nuclei: organization and connections. In: Manto M, Schmahmann JD, Rossi F, Gruol DL, Koibuchi N (eds) Handbook of the cerebellum and cerebellar disorders. Springer, Dordrecht, pp 419–421
go back to reference Walberg F, Pompeiano O, Westrum LE, Hauglie-Hanssen E (1962) Fastigioreticular fibers in the cat. An experimental study with silver methods. J Comp Neurol 119:187–199PubMedCrossRef Walberg F, Pompeiano O, Westrum LE, Hauglie-Hanssen E (1962) Fastigioreticular fibers in the cat. An experimental study with silver methods. J Comp Neurol 119:187–199PubMedCrossRef
go back to reference Weisheit G, Gliem M, Endl E, Pfeffer PL, Busslinger M, Schilling K (2006) Postnatal development of the murine cerebellar cortex: formation and early dispersal of basket, stellate and Golgi neurons. Eur J Neurosci 24:466–478PubMedCrossRef Weisheit G, Gliem M, Endl E, Pfeffer PL, Busslinger M, Schilling K (2006) Postnatal development of the murine cerebellar cortex: formation and early dispersal of basket, stellate and Golgi neurons. Eur J Neurosci 24:466–478PubMedCrossRef
go back to reference Xu FD, Zhang Z, Frazier DT (2001) Microinjection of acetazolamide into the fastigial nucleus augments respiratory output in the rat. J Appl Physiol 91:2342–2350PubMedCrossRef Xu FD, Zhang Z, Frazier DT (2001) Microinjection of acetazolamide into the fastigial nucleus augments respiratory output in the rat. J Appl Physiol 91:2342–2350PubMedCrossRef
go back to reference Yamada J, Noda H (1987) Afferent and efferent connections of the oculomotor cerebellar vermis in the macaque monkey. J Comp Neurol 265:224–241PubMedCrossRef Yamada J, Noda H (1987) Afferent and efferent connections of the oculomotor cerebellar vermis in the macaque monkey. J Comp Neurol 265:224–241PubMedCrossRef
go back to reference Zhang XY, Wang JJ, Zhu JN (2016) Cerebellar fastigial nucleus: from anatomic construction to physiological functions. Cerebel Ataxias 3:9CrossRef Zhang XY, Wang JJ, Zhu JN (2016) Cerebellar fastigial nucleus: from anatomic construction to physiological functions. Cerebel Ataxias 3:9CrossRef
go back to reference Zhu JN, Yung WH, Kwok-Chong Chow B, Chan YS, Wang JJ (2006) The cerebellar hypothalamic circuits: potential pathways underlying cerebellar involvement in somatic-visceral integration. Brain Res Rev 52:93–106PubMedCrossRef Zhu JN, Yung WH, Kwok-Chong Chow B, Chan YS, Wang JJ (2006) The cerebellar hypothalamic circuits: potential pathways underlying cerebellar involvement in somatic-visceral integration. Brain Res Rev 52:93–106PubMedCrossRef
Metadata
Title
Inter-fastigial projections along the roof of the fourth ventricle
Authors
Gabriela B. Gómez-González
Ataúlfo Martínez-Torres
Publication date
01-04-2021
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 3/2021
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-021-02217-8

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