The metabotropic glutamate receptor subtype 1 regulates development and maintenance of lemniscal synaptic connectivity in the somatosensory thalamus

English version

Autoři: Madoka Narushima ^aff001; Yuki Yagasaki ^aff001; Yuichi Takeuchi ^aff001; Atsu Aiba ^aff002; Mariko Miyata ^aff001
Působiště autorů: Division of Neurophysiology, Department of Physiology, School of Medicine, Tokyo Women's Medical University, Shinjuku-ku, Tokyo, Japan ^aff001; Laboratory of Animal Resources, Center for Disease Biology and Integrated Medicine, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo, Japan ^aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0226820

Souhrn

The metabotropic glutamate receptor subtype 1 (mGluR1) is a major subtype of group I mGluRs, which contributes to the development and plasticity of synapses in the brain. In the sensory thalamus, the thalamocortical neuron receives sensory afferents and massive feedback input from corticothalamic (CT) fibers. Notably, mGluR1 is more concentrated in CT synapses in the sensory thalamus. In the visual thalamus, mGluR1 maintains mature afferent synaptic connectivity. However, it is unknown whether mGluR1 contributes to strengthening of immature synapses or weakening of excess synapses during development and whether mGluR1 at CT synapses heterosynaptically regulates the development or refinement of afferent synapses. Here we investigated the effects of knocking out the gene encoding mGluR1 or pharmacologically blocking cortical activity on the development and maintenance of lemniscal synapses, i.e., the somatosensory afferent synapses, in the ventral posteromedial somatosensory thalamus. mGluR1-knockout (KO) mice exhibited delayed developmental strengthening as well as incomplete elimination and remodeling after maturation of lemniscal synapses. Similar to the phenotypes exhibited by mGluR1-KO mice, pharmacological blockade of somatosensory cortical activity from P12 or P21 for 1 week in wild-type mice perturbed elimination or maintenance of lemniscal synapses, respectively. The same manipulation in mGluR1-KO mice failed to induce additional abnormalities in lemniscal synaptic connectivity. These results suggest that activation of mGluR1, driven by CT input, regulates multiple stages of the development of lemniscal synapses, including strengthening, refinement, and maintenance in the somatosensory thalamus.

Klíčová slova:

Neurons – Nerve fibers – Electrophysiology – Synapses – Chi square tests – Muscle electrophysiology – Thalamus – Thalamic nuclei

Zdroje

1. Espinosa JS, Stryker MP. Development and plasticity of the primary visual cortex. Neuron. 2012;75(2):230–49. doi: 10.1016/j.neuron.2012.06.009 22841309; PubMed Central PMCID: PMC3612584.

2. Moreno-Juan V, Filipchuk A, Anton-Bolanos N, Mezzera C, Gezelius H, Andres B, et al. Prenatal thalamic waves regulate cortical area size prior to sensory processing. Nat Commun. 2017;8:14172. doi: 10.1038/ncomms14172 28155854; PubMed Central PMCID: PMC5296753.

3. Erzurumlu RS, Gaspar P. Development and critical period plasticity of the barrel cortex. Eur J Neurosci. 2012;35(10):1540–53. doi: 10.1111/j.1460-9568.2012.08075.x 22607000; PubMed Central PMCID: PMC3359866.

4. Vitali I, Jabaudon D. Synaptic biology of barrel cortex circuit assembly. Semin Cell Dev Biol. 2014;35:156–64. doi: 10.1016/j.semcdb.2014.07.009 25080022.

5. Li H, Crair MC. How do barrels form in somatosensory cortex? Ann N Y Acad Sci. 2011;1225:119–29. doi: 10.1111/j.1749-6632.2011.06024.x 21534999; PubMed Central PMCID: PMC4700879.

6. Assali A, Gaspar P, Rebsam A. Activity dependent mechanisms of visual map formation—from retinal waves to molecular regulators. Semin Cell Dev Biol. 2014;35:136–46. doi: 10.1016/j.semcdb.2014.08.008 25152335.

7. Wang H, Zhang ZW. A critical window for experience-dependent plasticity at whisker sensory relay synapse in the thalamus. J Neurosci. 2008;28(50):13621–8. doi: 10.1523/JNEUROSCI.4785-08.2008 19074025; PubMed Central PMCID: PMC6671758.

8. Pan L, Yang J, Yang Q, Wang X, Zhu L, Liu Y, et al. A critical period for the rapid modification of synaptic properties at the VPm relay synapse. Front Mol Neurosci. 2017;10:238. doi: 10.3389/fnmol.2017.00238 28790892; PubMed Central PMCID: PMC5525376.

9. Dilger EK, Krahe TE, Morhardt DR, Seabrook TA, Shin HS, Guido W. Absence of plateau potentials in dLGN cells leads to a breakdown in retinogeniculate refinement. J Neurosci. 2015;35(8):3652–62. doi: 10.1523/JNEUROSCI.2343-14.2015 25716863; PubMed Central PMCID: PMC4339365.

10. Cheadle L, Tzeng CP, Kalish BT, Harmin DA, Rivera S, Ling E, et al. Visual Experience-Dependent Expression of Fn14 Is Required for Retinogeniculate Refinement. Neuron. 2018;99(3):525–39 e10. doi: 10.1016/j.neuron.2018.06.036 30033152; PubMed Central PMCID: PMC6101651.

11. Wang H, Liu H, Storm DR, Zhang ZW. Adenylate cyclase 1 promotes strengthening and experience-dependent plasticity of whisker relay synapses in the thalamus. J Physiol. 2011. doi: 10.1113/jphysiol.2011.213702 21930601.

12. Louros SR, Hooks BM, Litvina L, Carvalho AL, Chen C. A role for stargazin in experience-dependent plasticity. Cell Rep. 2014;7(5):1614–25. doi: 10.1016/j.celrep.2014.04.054 24882000; PubMed Central PMCID: PMC4115130.

13. Niswender CM, Conn PJ. Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu Rev Pharmacol Toxicol. 2010;50:295–322. doi: 10.1146/annurev.pharmtox.011008.145533 20055706; PubMed Central PMCID: PMC2904507.

14. Lüscher C, Huber KM. Group 1 mGluR-dependent synaptic long-term depression: mechanisms and implications for circuitry and disease. Neuron. 2010;65(4):445–59. doi: 10.1016/j.neuron.2010.01.016 20188650; PubMed Central PMCID: PMC2841961.

15. Wang H, Zhuo M. Group I metabotropic glutamate receptor-mediated gene transcription and implications for synaptic plasticity and diseases. Front Pharmacol. 2012;3:189. doi: 10.3389/fphar.2012.00189 23125836; PubMed Central PMCID: PMC3485740.

16. Kano M, Hashimoto K, Tabata T. Type-1 metabotropic glutamate receptor in cerebellar Purkinje cells: a key molecule responsible for long-term depression, endocannabinoid signalling and synapse elimination. Philos Trans R Soc Lond B Biol Sci. 2008;363(1500):2173–86. doi: 10.1098/rstb.2008.2270 18339599; PubMed Central PMCID: PMC2610189.

17. Narushima M, Uchigashima M, Yagasaki Y, Harada T, Nagumo Y, Uesaka N, et al. The Metabotropic Glutamate Receptor Subtype 1 Mediates Experience-Dependent Maintenance of Mature Synaptic Connectivity in the Visual Thalamus. Neuron. 2016;91(5):1097–109. doi: 10.1016/j.neuron.2016.07.035 27545713.

18. Godwin DW, Van Horn SC, Eriir A, Sesma M, Romano C, Sherman SM. Ultrastructural localization suggests that retinal and cortical inputs access different metabotropic glutamate receptors in the lateral geniculate nucleus. J Neurosci. 1996;16(24):8181–92. doi: 10.1523/JNEUROSCI.16-24-08181.1996 8987843.

19. Thompson AD, Picard N, Min L, Fagiolini M, Chen C. Cortical Feedback Regulates Feedforward Retinogeniculate Refinement. Neuron. 2016;91(5):1021–33. doi: 10.1016/j.neuron.2016.07.040 27545712; PubMed Central PMCID: PMC5156570.

20. Arsenault D, Zhang ZW. Developmental remodelling of the lemniscal synapse in the ventral basal thalamus of the mouse. J Physiol. 2006;573(Pt 1):121–32. Epub 2006/04/04. doi: 10.1113/jphysiol.2006.106542 16581865; PubMed Central PMCID: PMC1779701.

21. Takeuchi Y, Asano H, Katayama Y, Muragaki Y, Imoto K, Miyata M. Large-scale somatotopic refinement via functional synapse elimination in the sensory thalamus of developing mice. J Neurosci. 2014;34(4):1258–70. doi: 10.1523/JNEUROSCI.3865-13.2014 24453317.

22. Takeuchi Y, Yamasaki M, Nagumo Y, Imoto K, Watanabe M, Miyata M. Rewiring of afferent fibers in the somatosensory thalamus of mice caused by peripheral sensory nerve transection. J Neurosci. 2012;32(20):6917–30. Epub 2012/05/18. doi: 10.1523/JNEUROSCI.5008-11.2012 22593060.

23. Ohtani Y, Miyata M, Hashimoto K, Tabata T, Kishimoto Y, Fukaya M, et al. The synaptic targeting of mGluR1 by its carboxyl-terminal domain is crucial for cerebellar function. J Neurosci. 2014;34(7):2702–12. doi: 10.1523/JNEUROSCI.3542-13.2014 24523559.

24. Hong YK, Park S, Litvina EY, Morales J, Sanes JR, Chen C. Refinement of the retinogeniculate synapse by bouton clustering. Neuron. 2014;84(2):332–9. doi: 10.1016/j.neuron.2014.08.059 25284005; PubMed Central PMCID: PMC4322918.

25. Vidnyanszky Z, Gorcs TJ, Negyessy L, Borostyankio Z, Knopfel T, Hamori J. Immunocytochemical visualization of the mGluR1a metabotropic glutamate receptor at synapses of corticothalamic terminals originating from area 17 of the rat. Eur J Neurosci. 1996;8(6):1061–71. doi: 10.1111/j.1460-9568.1996.tb01273.x 8752575.

26. Liu XB, Muñoz A, Jones EG. Changes in subcellular localization of metabotropic glutamate receptor subtypes during postnatal development of mouse thalamus. J Comp Neurol. 1998;395(4):450–65. doi: 10.1002/(sici)1096-9861(19980615)395:4<450::aid-cne3>3.0.co;2-0 [pii]. 9619499.

27. Narushima M. Comparison of the role of metabotropic glutamate receptor subtype 1 in developmental refinement of neuronal connectivity between the cerebellum and the sensory thalamus. Neurosci Res. 2018;129:24–31. doi: 10.1016/j.neures.2017.06.004 28711710.

28. Kano M, Watanabe T, Uesaka N, Watanabe M. Multiple Phases of Climbing Fiber Synapse Elimination in the Developing Cerebellum. Cerebellum. 2018. doi: 10.1007/s12311-018-0964-z 30009357.

29. Wilkerson JR, Tsai NP, Maksimova MA, Wu H, Cabalo NP, Loerwald KW, et al. A role for dendritic mGluR5-mediated local translation of Arc/Arg3.1 in MEF2-dependent synapse elimination. Cell Rep. 2014;7(5):1589–600. doi: 10.1016/j.celrep.2014.04.035 24857654; PubMed Central PMCID: PMC4057996.

30. Kalinowska M, Chávez AE, Lutzu S, Castillo PE, Bukauskas FF, Francesconi A. Actinin-4 Governs Dendritic Spine Dynamics and Promotes Their Remodeling by Metabotropic Glutamate Receptors. J Biol Chem. 2015;290(26):15909–20. doi: 10.1074/jbc.M115.640136 25944910; PubMed Central PMCID: PMC4481196.

31. Ramiro-Cortés Y, Israely I. Long lasting protein synthesis- and activity-dependent spine shrinkage and elimination after synaptic depression. PLoS One. 2013;8(8):e71155. doi: 10.1371/journal.pone.0071155 23951097; PubMed Central PMCID: PMC3739806.

32. Li S, Wang L, Tie X, Sohya K, Lin X, Kirkwood A, et al. Brief Novel Visual Experience Fundamentally Changes Synaptic Plasticity in the Mouse Visual Cortex. J Neurosci. 2017;37(39):9353–60. doi: 10.1523/JNEUROSCI.0334-17.2017 28821676; PubMed Central PMCID: PMC5618258.

33. Wang H, Ardiles AO, Yang S, Tran T, Posada-Duque R, Valdivia G, et al. Metabotropic Glutamate Receptors Induce a Form of LTP Controlled by Translation and Arc Signaling in the Hippocampus. J Neurosci. 2016;36(5):1723–9. doi: 10.1523/JNEUROSCI.0878-15.2016 26843652; PubMed Central PMCID: PMC4737780.

34. Ran I, Laplante I, Bourgeois C, Pepin J, Lacaille P, Costa-Mattioli M, et al. Persistent transcription- and translation-dependent long-term potentiation induced by mGluR1 in hippocampal interneurons. J Neurosci. 2009;29(17):5605–15. doi: 10.1523/JNEUROSCI.5355-08.2009 19403827.

35. Wen JA, DeBlois MC, Barth AL. Initiation, labile, and stabilization phases of experience-dependent plasticity at neocortical synapses. J Neurosci. 2013;33(19):8483–93. doi: 10.1523/JNEUROSCI.3575-12.2013 23658185; PubMed Central PMCID: PMC3740338.

36. Kubota J, Mikami Y, Kanemaru K, Sekiya H, Okubo Y, Iino M. Whisker experience-dependent mGluR signaling maintains synaptic strength in the mouse adolescent cortex. Eur J Neurosci. 2016;44(3):2004–14. doi: 10.1111/ejn.13285 27225340.

37. Sugawara T, Hisatsune C, Miyamoto H, Ogawa N, Mikoshiba K. Regulation of spinogenesis in mature Purkinje cells via mGluR/PKC-mediated phosphorylation of CaMKIIbeta. Proc Natl Acad Sci U S A. 2017;114(26):E5256–E65. doi: 10.1073/pnas.1617270114 28607044; PubMed Central PMCID: PMC5495224.

38. Takeuchi Y, Osaki H, Yagasaki Y, Katayama Y, Miyata M. Afferent Fiber Remodeling in the Somatosensory Thalamus of Mice as a Neural Basis of Somatotopic Reorganization in the Brain and Ectopic Mechanical Hypersensitivity after Peripheral Sensory Nerve Injury. eNeuro. 2017;4(2). Epub 2017/04/03. doi: 10.1523/ENEURO.0345-16.2017 28396882; PubMed Central PMCID: PMC5378058.

39. Noutel J, Hong YK, Leu B, Kang E, Chen C. Experience-dependent retinogeniculate synapse remodeling is abnormal in MeCP2-deficient mice. Neuron. 2011;70(1):35–42. S0896-6273(11)00167-X [pii] doi: 10.1016/j.neuron.2011.03.001 21482354; PubMed Central PMCID: PMC3082316.

40. Wang H, Liu H, Zhang ZW. Elimination of redundant synaptic inputs in the absence of synaptic strengthening. J Neurosci. 2011;31(46):16675–84. 31/46/16675 [pii] doi: 10.1523/JNEUROSCI.4569-11.2011 22090494.

41. Kano M, Hashimoto K, Chen C, Abeliovich A, Aiba A, Kurihara H, et al. Impaired synapse elimination during cerebellar development in PKC gamma mutant mice. Cell. 1995;83(7):1223–31. 0092-8674(95)90147-7 [pii]. doi: 10.1016/0092-8674(95)90147-7 8548808.

42. Mikuni T, Uesaka N, Okuno H, Hirai H, Deisseroth K, Bito H, et al. Arc/Arg3.1 is a postsynaptic mediator of activity-dependent synapse elimination in the developing cerebellum. Neuron. 2013;78(6):1024–35. doi: 10.1016/j.neuron.2013.04.036 23791196; PubMed Central PMCID: PMC3773328.

43. Sherman SM, Guillery RW. Exploring the thalamus and its role in cortical function. 2nd ed. Cambridge, Mass.: MIT Press; 2006. xxi, 484 p. p.

44. Guillery RW, Sherman SM. Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron. 2002;33(2):163–75. doi: 10.1016/s0896-6273(01)00582-7 11804565.

45. Briggs F, Usrey WM. Emerging views of corticothalamic function. Curr Opin Neurobiol. 2008;18(4):403–7. doi: 10.1016/j.conb.2008.09.002 18805486; PubMed Central PMCID: PMC2626162.

46. Brooks JM, Su J, Levy C, Wang JS, Seabrook TA, Guido W, et al. A molecular mechanism regulating the timing of corticogeniculate innervation. Cell Rep. 2013;5(3):573–81. doi: 10.1016/j.celrep.2013.09.041 24183669; PubMed Central PMCID: PMC3849812.

47. Seabrook TA, El-Danaf RN, Krahe TE, Fox MA, Guido W. Retinal input regulates the timing of corticogeniculate innervation. J Neurosci. 2013;33(24):10085–97. doi: 10.1523/JNEUROSCI.5271-12.2013 23761904; PubMed Central PMCID: PMC3682386.

48. Shanks JA, Ito S, Schaevitz L, Yamada J, Chen B, Litke A, et al. Corticothalamic Axons Are Essential for Retinal Ganglion Cell Axon Targeting to the Mouse Dorsal Lateral Geniculate Nucleus. J Neurosci. 2016;36(19):5252–63. doi: 10.1523/JNEUROSCI.4599-15.2016 27170123; PubMed Central PMCID: PMC4863061.

49. Golshani P, Warren RA, Jones EG. Progression of change in NMDA, non-NMDA, and metabotropic glutamate receptor function at the developing corticothalamic synapse. J Neurophysiol. 1998;80(1):143–54. doi: 10.1152/jn.1998.80.1.143 9658036.

The metabotropic glutamate receptor subtype 1 regulates development and maintenance of lemniscal synaptic connectivity in the somatosensory thalamus

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