https://doi.org/10.4081/ejh.2022.3370

Postnatal development of thalamic reticular nucleus projections to the anterior thalamic nuclei in rats

Vol. 66 No. 2 (2022)
Submitted: 14 December 2021
Accepted: 26 February 2022
Published: 24 March 2022
Thalamic reticular nucleus, parvalbumin, axon terminal, development, anterior thalamic nucleus, rat
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Authors

Hitoshi Fujita
Department of Neuroanatomy, Graduate School of Medicine, Yokohama City University, Yokohama, Japan.
Kosuke Imura
imurako@yokohama-cu.ac.jp
https://orcid.org/0000-0002-0368-7069
Department of Neuroanatomy, Graduate School of Medicine, Yokohama City University, Yokohama, Japan.
Masahito Takiguchi
Department of Neuroanatomy, Graduate School of Medicine, Yokohama City University, Yokohama, Japan.
Kengo Funakoshi
Department of Neuroanatomy, Graduate School of Medicine, Yokohama City University, Yokohama, Japan.

The thalamic reticular nucleus (TRN) projects inhibitory signals to the thalamus, thereby controlling thalamocortical connections. Few studies have examined the development of TRN projections to the anterior thalamic nuclei with regard to axon course and the axon terminal distributions. In the present study, we used parvalbumin (PV) immunostaining to investigate inhibitory projections from the TRN to the thalamus in postnatal (P) 2- to 5-week-old rats (P14–35). The distribution of PV-positive (+) nerve fibers and nerve terminals markedly differed among the anterior thalamic nuclei at P14. Small, beaded nerve terminals were more distributed throughout the anterodorsal nucleus (AD) than in the anteroventral nucleus (AV) and anteromedial nucleus (AM). PV+ fibers traveling from the TRN to the AD were observed in the AV and AM. Nodular nerve terminals, spindle or en passant terminals, were identified on the axons passing through the AV and AM. At P21, axon bundles traveling without nodular terminals were observed, and nerve terminals were distributed throughout the AV and AM similar to the AD. At P28 and P35, the nerve terminals were evenly distributed throughout each nucleus. In addition, DiI tracer injections into the retrosplenial cortex revealed retrogradely-labeled projection neurons in the 3 nuclei at P14. At P14, the AD received abundant projections from the TRN and then projected to the retrosplenial cortex. The AV and AM seem to receive projections with distinct nodular nerve terminals from the TRN and project to the retrosplenial cortex. The projections from TRN to the AV and AM with nodular nerve terminals at P14 are probably developmental-period specific. In comparison, the TRN projections to the AD at P14 might be related to the development of spatial navigation as part of the head orientation system.

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Citations

Crossref
Scopus
Google Scholar
Europe PMC
Jones EG. Thalamic circuitry and thalamocortical synchrony. Phil Trans R Soc Lond B 2002;357:1659-73. DOI: https://doi.org/10.1098/rstb.2002.1168
Takata N. Thalamic reticular nucleus in the thalamocortical loop. Neurosci Res 2020;156:32-40. DOI: https://doi.org/10.1016/j.neures.2019.12.004
Battaglia G, Lizier C, Colacitti C, Princivalle A, Spreafico R. A reticuloreticular commissural pathway in the rat thalamus. J Comp Neurol 1994;347:127-38. DOI: https://doi.org/10.1002/cne.903470110
Arcelli P, Frassoni C, Regondi CM, De Biasi S, Spreafico R. GABAergic neurons in mammalian thalamus: a marker of thalamic complexity? Brain Res Bull 1997;42:27-37. DOI: https://doi.org/10.1016/S0361-9230(96)00107-4
Sherman SM. Interneurons and triadic circuitry of the thalamus. Trends Neurosci 2004;27:670-5. DOI: https://doi.org/10.1016/j.tins.2004.08.003
Murata Y, Colonnese MT. Thalamic inhibitory circuits and network activity development. Brain Res 2019; 706:13-23. DOI: https://doi.org/10.1016/j.brainres.2018.10.024
Celio MR. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience1990;135:375-475. DOI: https://doi.org/10.1016/0306-4522(90)90091-H
Arai R, Jacobowitz DM, Deura S. Distribution of calretinin, calbindin-D28k, and parvalbumin in the rat thalamus. Brain Res Bull 1994;33:595–614. DOI: https://doi.org/10.1016/0361-9230(94)90086-8
Frassoni C, Bentivoglio M, Spreafico R, Sánchez MP, Puelles L, Fairen A. Postnatal development of calbindin and parvalbumin immunoreactivity in the thalamus of the rat. Develop Brain Res 1991;58:243-9. DOI: https://doi.org/10.1016/0165-3806(91)90011-7
Seto-oshima A, Aoki E, Semba R, Emson PC, Heizmann CW. Parvalbumin immunoreactivity in the reticular thalamic nucleus of developing rats. Acta Histochem Cytochem 1989;22:331-40. DOI: https://doi.org/10.1267/ahc.22.331
Amadeo A, Ortino B, Frassoni C. Parvalbumin and GABA in the developing somatosensory thalamus of the rat: an immunocytochemical ultrastructural correlation. Anat Embryol (Berl) 2001;203:109-19. DOI: https://doi.org/10.1007/s004290000143
Yoder RM, Clark BJ, Taube JS. Origins of landmark encoding in the brain. Trends Neurosci 2011;34:561-71. DOI: https://doi.org/10.1016/j.tins.2011.08.004
Tan HM, Bassett JP, O'Keefe J, Cacucci F, Wills TJ. The development of the head direction system before eye opening in the rat. Curr Biol 2015;25:479-83. DOI: https://doi.org/10.1016/j.cub.2014.12.030
Perry BAL, Mitchell AS. Considering the evidence for anterior and laterodorsal thalamic nuclei as higher order relays to cortex. Front Mol Neurosci 2019;12:167. DOI: https://doi.org/10.3389/fnmol.2019.00167
Liu XB, Coble J, van Luijtelaar G, Jones EG. Reticular nucleus-specific changes in alpha3 subunit protein at GABA synapses in genetically epilepsy-prone rats. Proc Natl Acad Sci USA 2007;104:12512-7. DOI: https://doi.org/10.1073/pnas.0705320104
Oda S, Funato H, Sato F, Adachi-Akahane S, Ito M, Takase K, Kuroda M. A subset of thalamocortical projections to the retrosplenial cortex possesses two vesicular glutamate transporter isoforms, VGluT1 and VGluT2, in axon terminals and somata. J Comp Neurol 2014;522:2089-106. DOI: https://doi.org/10.1002/cne.23519
Burette AC, Strehler EE, Weinberg RJ. "Fast" plasma membrane calcium pump PMCA2a concentrates in GABAergic terminals in the adult rat brain. J Comp Neurol 2009 512:500-13. DOI: https://doi.org/10.1002/cne.21909
Bartheld CSV, Cunningham DE, Rubel EW. Neuronal tracing with DiI: decalcification, cryosectioning, and photoconversion for light and electron microscopic analysis. J Histochem Cytochem 1990;38:725-33. DOI: https://doi.org/10.1177/38.5.2185313
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012;9:676-82. DOI: https://doi.org/10.1038/nmeth.2019
Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 2nd ed. Academic Press; 1986.
Zakowski W, Bogus-Nowakowska K, Robak A. Embryonic and postnatal development of calcium-binding proteins immunoreactivity in the anterior thalamus of the guinea pig. J Chem Neuroanat 2013;53:25-32. DOI: https://doi.org/10.1016/j.jchemneu.2013.09.005
Zakowski W. Neurochemistry of the anterior thalamic nuclei. Mol Neurobiol 2017;54:5248-63. DOI: https://doi.org/10.1007/s12035-016-0077-y
Biasi SD, Amadeo A, Arcelli P, Frassoni C, Spreafico R. Postnatal development of GABA-immunoreactive terminals in the reticular and ventrobasal nuclei of the rat thalamus: a light and electron microscopic study. Neuroscience 1997;76:503-16. DOI: https://doi.org/10.1016/S0306-4522(96)00376-4
Miró-Bernié N, Ichinohe N, Pérez-Clausell J, Rockland KS. Zinc-rich transient vertical modules in the rat retrosplenial cortex during postnatal development. Neuroscience 2006;138:523-35. DOI: https://doi.org/10.1016/j.neuroscience.2005.11.049
Bassett JP, Wills TJ, Cacucci F. Self-organized attractor dynamics in the developing head direction circuit. Curr Biol 2018;28:609-15. DOI: https://doi.org/10.1016/j.cub.2018.01.010
Ahmed AK, Guison NG, Yamadori T. A retrograde fluorescent-labeling study of direct relationship between the limbic (anterodorsal and anteroventral thalamic nuclei) and the visual system in the albino rat. Brain Res 1996;729:119-23. DOI: https://doi.org/10.1016/0006-8993(96)00283-1
Shibata H. Topographic organization of subcortical projections to the anterior thalamic nuclei in the rat. J Comp Neurol 1992;322:117-27. DOI: https://doi.org/10.1002/cne.903230110
Bassett J, Tullman ML, Taube JS. Lesions of the tegmentomammillary circuit in the head direction system disrupt the head direction signal in the anterior thalamus. J Neurosci 2007;27:7564-77. DOI: https://doi.org/10.1523/JNEUROSCI.0268-07.2007
Alpeeva EV, Makarenko IG. Perinatal development of the mammillothalamic tract and innervation of the anterior thalamic nuclei. Brain Res 2009;1248:1-13. DOI: https://doi.org/10.1016/j.brainres.2008.10.060

Ethics Approval

This study is approved under the guidelines of the official Japanese regulations for research on animals in the Yokohama City University (approval NO. F-A-16-064)

Supporting Agencies

Fundamental Research Funding of Yokohama City University

How to Cite

Fujita, H., Imura, K., Takiguchi, M., & Funakoshi, K. (2022). Postnatal development of thalamic reticular nucleus projections to the anterior thalamic nuclei in rats. European Journal of Histochemistry, 66(2). https://doi.org/10.4081/ejh.2022.3370
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