Prenatal thalamic waves regulate cortical area size prior to sensory processing

Nature Communications

Volumn 8, Issue , 2017, Pages

  Moreno Juan, Verónica ^a   Filipchuk, Anton ^a   Antón Bolaños, Noelia ^a   Mezzera, Cecilia ^a,b   Gezelius, Henrik ^a   Andrés, Belen ^a   Rodríguez Malmierca, Luis ^a   Susín, Rafael ^a   Schaad, Olivier ^c   Iwasato, Takuji ^d,e   Schüle, Roland ^f,g,h   Rutlin, Michael ^i,j   Nelson, Sacha ⁱ   Ducret, Sebastien ^k   Valdeolmillos, Miguel ^a   Rijli, Filippo M ^k   López Bendito, Guillermina ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b CHAMPALIMAUD CENTRE FOR THE UNKNOWN   (Portugal)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

^e GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^f UNIVERSITY OF FREIBURG   (Germany)

^g UNIVERSITY OF FREIBURG   (Germany)

^h Deutsches Konsortium für Translationale Krebsforschungs dktk   (Germany)

ⁱ BRANDEIS UNIVERSITY   (United States)

^j Department of Medicine   (United States)

^k FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

more..

Author keywords

[No Author keywords available]

Indexed keywords

RETINOID RELATED ORPHAN RECEPTOR BETA; CALCIUM; ORPHAN NUCLEAR RECEPTOR;

CALCIUM; COMMUNICATION; GENE EXPRESSION; RODENT; SENSORY SYSTEM; WAVE PROPAGATION;

ADULT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CALCIUM SIGNALING; CONTROLLED STUDY; EMBRYO; EYE ENUCLEATION; FEMALE; GENE CONTROL; GENE EXPRESSION; HUMAN; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRENATAL PERIOD; SENSORY SYSTEM; THALAMUS; THALAMUS NUCLEUS; UPREGULATION; ANATOMY AND HISTOLOGY; ANIMAL; C57BL MOUSE; EMBRYOLOGY; GAP JUNCTION; GENETICS; METABOLISM; PHYSIOLOGY; PREGNANCY; SOMATOSENSORY CORTEX; THALAMUS VENTRAL NUCLEUS; TRANSGENIC MOUSE; VISION;

MUS;

ANIMALS; CALCIUM; FEMALE; GAP JUNCTIONS; GENE EXPRESSION; HUMANS; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONAL PLASTICITY; ORPHAN NUCLEAR RECEPTORS; PREGNANCY; SOMATOSENSORY CORTEX; VENTRAL THALAMIC NUCLEI; VISION, OCULAR;

EID: 85011604977     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14172     Document Type: Article

References (67)

1. Miyashita-Lin, E., Hevner, R., Wassarman, K., Martinez, S. & Rubenstein, J. Early neocortical regionalization in the absence of thalamic innervation. Science 285, 906-909 (1999).
2. O'Leary, D. D., Chou, S. J. & Sahara, S. Area patterning of the mammalian cortex. Neuron 56, 252-269 (2007).
3. Grove, E. A. & Fukuchi-Shimogori, T. Generating the cerebral cortical area map. Annu. Rev. Neurosci. 26, 355-380 (2003).
4. Garel, S., Huffman, K. J. & Rubenstein, J. L. Molecular regionalization of the neocortex is disrupted in Fgf8 hypomorphic mutants. Development 130, 1903-1914 (2003).
5. Rakic, P. Specification of cerebral cortical areas. Science 241, 170-176 (1988).
6. Erzurumlu, R. S., Murakami, Y. & Rijli, F. M. Mapping the face in the somatosensory brainstem. Nat. Rev. Neurosci. 11, 252-263 (2010).
7. Erzurumlu, R. S. & Gaspar, P. Development and critical period plasticity of the barrel cortex. Eur. J. Neurosci. 35, 1540-1553 (2012).
8. Karlen, S. & Krubitzer, L. Effects of bilateral enucleation on the size of visual and nonvisual areas of the brain. Cereb. Cortex 19, 1360-1371 (2009).
9. Larsen, D. D., Luu, J. D., Burns, M. E. & Krubitzer, L. What are the effects of severe visual impairment on the cortical organization and connectivity of primary visual cortex? Front. Neuroanat. 3, 30 (2009).
10. Espinosa, J. S. & Stryker, M. P. Development and plasticity of the primary visual cortex. Neuron 75, 230-249 (2012).
11. Huberman, A. D., Speer, C. M. & Chapman, B. Spontaneous retinal activity mediates development of ocular dominance columns and binocular receptive fields in v1. Neuron 52, 247-254 (2006).
12. Ackman, J. B. & Crair, M. C. Role of emergent neural activity in visual map development. Curr. Opin. Neurobiol. 24, 166-175 (2014).
13. Meister, M., Wong, R. O., Baylor, D. A. & Shatz, C. J. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939-943 (1991).
14. Feller, M. B., Wellis, D. P., Stellwagen, D., Werblin, F. S. & Shatz, C. J. Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272, 1182-1187 (1996).
15. Chou, S. J. et al. Geniculocortical input drives genetic distinctions between primary and higher-order visual areas. Science 340, 1239-1242 (2013).
16. Lokmane, L. et al. Sensory map transfer to the neocortex relies on pretarget ordering of thalamic axons. Curr. Biol. 23, 810-816 (2013).
17. Karlen, S. J., Kahn, D. M. & Krubitzer, L. Early blindness results in abnormal corticocortical and thalamocortical connections. Neuroscience 142, 843-858 (2006).
18. Bronchti, G. et al. Auditory activation of 'visual' cortical areas in the blind mole rat (Spalax ehrenbergi). Eur. J. Neurosci. 16, 311-329 (2002).
19. Chabot, N. et al. Subcortical auditory input to the primary visual cortex in anophthalmic mice. Neurosci. Lett. 433, 129-134 (2008).
20. Zembrzycki, A., Chou, S. J., Ashery-Padan, R., Stoykova, A. & O'Leary, D. D. Sensory cortex limits cortical maps and drives top-down plasticity in thalamocortical circuits. Nat. Neurosci. 16, 1060-1067 (2013).
21. Rauschecker, J. P., Tian, B., Korte, M. & Egert, U. Crossmodal changes in the somatosensory vibrissa/barrel system of visually deprived animals. Proc. Natl Acad. Sci. USA 89, 5063-5067 (1992).
22. Zheng, D. & Purves, D. Effects of increased neural activity on brain growth. Proc. Natl Acad. Sci. USA 92, 1802-1806 (1995).
23. Fetter-Pruneda, I. et al. Shifts in developmental timing, and not increased levels of experience-dependent neuronal activity, promote barrel expansion in the primary somatosensory cortex of rats enucleated at birth. PLoS ONE 8, e54940 (2013).
24. Dehay, C., Horsburgh, G., Berland, M., Killackey, H. & Kennedy, H. Maturation and connectivity of the visual cortex in monkey is altered by prenatal removal of retinal input. Nature 337, 265-267 (1989).
25. Bronchti, G., Schonenberger, N., Welker, E. & Van der Loos, H. Barrelfield expansion after neonatal eye removal in mice. Neuroreport 3, 489-492 (1992).
26. Kozanian, O. O., Abbott, C. W. & Huffman, K. J. Rapid changes in cortical and subcortical brain regions after early bilateral enucleation in the mouse. PLoS ONE 10, e0140391 (2015).
27. Mizuno, H. et al. NMDAR-regulated dynamics of layer 4 neuronal dendrites during thalamocortical reorganization in neonates. Neuron 82, 365-379 (2014).
28. Bechara, A. et al. Hoxa2 selects barrelette neuron identity and connectivity in the mouse somatosensory brainstem. Cell Rep. 13, 783-797 (2015).
29. Woolsey, T. A. & Van der Loos, H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 17, 205-242 (1970).
30. Landers, M., Haidarliu, S. & Philip Zeigler, H. Development of rodent macrovibrissae: effects of neonatal whisker denervation and bilateral neonatal enucleation. Somatosens. Mot. Res. 23, 11-17 (2006).
31. Tritsch, N. X. et al. Calcium action potentials in hair cells pattern auditory neuron activity before hearing onset. Nat. Neurosci. 13, 1050-1052 (2010).
32. Blankenship, A. & Feller, M. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat. Rev. Neurosci. 11, 18-29 (2010).
33. Yuste, R., Nelson, D. A., Rubin, W. W. & Katz, L. C. Neuronal domains in developing neocortex: mechanisms of coactivation. Neuron 14, 7-17 (1995).
34. Barnett, H. M. et al. Relationship between individual neuron and network spontaneous activity in developing mouse cortex. J. Neurophysiol. 112, 3033-3045 (2014).
35. Lacar, B., Young, S. Z., Platel, J. C. & Bordey, A. Gap junction-mediated calcium waves define communication networks among murine postnatal neural progenitor cells. Eur. J. Neurosci. 34, 1895-1905 (2011).
36. Elias, L. A. & Kriegstein, A. R. Gap junctions: multifaceted regulators of embryonic cortical development. Trends Neurosci. 31, 243-250 (2008).
37. Becker-Andre, M., Andre, E. & DeLamarter, J. F. Identification of nuclear receptor mRNAs by RT-PCR amplification of conserved zinc-finger motif sequences. Biochem. Biophys. Res. Commun. 194, 1371-1379 (1993).
38. Jabaudon, D., Shnider, S. J., Tischfield, D. J., Galazo, M. J. & Macklis, J. D. ROR Induces Barrel-like Neuronal Clusters in the Developing Neocortex. Cereb. Cortex 22, 996-1006 (2012).
39. Nakagawa, Y. & Orsquo Leary, D. D. M. Dynamic patterned expression of orphan nuclear receptor genes RORalpha and RORbeta in developing mouse forebrain. Dev. Neurosci. 25, 234-244 (2003).
40. Gezelius, H. & Lopez-Bendito, G. Thalamic neuronal specification and early circuit formation. Dev. Neurobiol. doi: 10.1002/dneu.22460 (2016).
41. Mire, E. et al. Spontaneous activity regulates Robo1 transcription to mediate a switch in thalamocortical axon growth. Nat. Neurosci. 15, 1-12 (2012).
42. Lopez-Benditó, G. & Molnár, Z. Thalamocortical development: how are we going to get there? Nat. Rev. Neurosci. 4, 276-289 (2003).
43. Hensch, T. K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6, 877-888 (2005).
44. Dye, C. A., Abbott, C. W. & Huffman, K. J. Bilateral enucleation alters gene expression and intraneocortical connections in the mouse. Neural Dev. 7, 5 (2012).
45. Zembrzycki, A., Perez-Garcia, C. G., Wang, C. F., Chou, S. J. & O'Leary, D. D. Postmitotic regulation of sensory area patterning in the mammalian neocortex by Lhx2. Proc. Natl Acad. Sci. USA 112, 6736-6741 (2015).
46. Pouchelon, G., Frangeul, L., Rijli, F. M. & Jabaudon, D. Patterning of pre-thalamic somatosensory pathways. Eur. J. Neurosci. 35, 1533-1539 (2012).
47. Ackman, J. B., Burbridge, T. J. & Crair, M. C. Retinal waves coordinate patterned activity throughout the developing visual system. Nature 490, 219-225 (2012).
48. Mooney, R., Penn, A. A., Gallego, R. & Shatz, C. J. Thalamic relay of spontaneous retinal activity prior to vision. Neuron 17, 863-874 (1996).
49. Weliky, M. Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo. Science 285, 599-604 (1999).
50. Linden, M. L., Heynen, A. J., Haslinger, R. H. & Bear, M. F. Thalamic activity that drives visual cortical plasticity. Nat. Neurosci. 12, 390-392 (2009).
51. Stellwagen, D. & Shatz, C. J. An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 33, 357-367 (2002).
52. Xu, H. P. et al. An instructive role for patterned spontaneous retinal activity in mouse visual map development. Neuron 70, 1115-1127 (2011).
53. + oscillations in situ drive NMDAR-mediated neuronal excitation. Nat. Neurosci. 4, 803-812 (2001).
54. Schitine, C., Nogaroli, L., Costa, M. R. & Hedin-Pereira, C. Astrocyte heterogeneity in the brain: from development to disease. Front. Cell Neurosci. 9, 76 (2015).
55. Benito, E. & Barco, A. The neuronal activity-driven transcriptome. Mol. Neurobiol. 51, 1071-1088 (2015).
56. Castillo-Paterna, M. et al. DCC functions as an accelerator of thalamocortical axonal growth downstream of spontaneous thalamic activity. EMBO Rep. 16, 851-862 (2015).
57. Spitzer, N. Electrical activity in early neuronal development. Nature 444, 707-712 (2006).
58. Cohen, L. G. L. et al. Functional relevance of cross-modal plasticity in blind humans. Nature 389, 180-183 (1997).
59. Finney, E. M., Fine, I. & Dobkins, K. R. Visual stimuli activate auditory cortex in the deaf. Nat. Neurosci. 4, 1171-1173 (2001).
60. Sadato, N. et al. Activation of the primary visual cortex by Braille reading in blind subjects. Nature 380, 526-528 (1996).
61. Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140 (2010).
62. Chen, L., Guo, Q. & Li, J. Transcription factor Gbx2 acts cell-nonautonomously to regulate the formation of lineage-restriction boundaries of the thalamus. Development 136, 1317-1326 (2009).
63. Liu, H. et al. An isoform of retinoid-related orphan receptor beta directs differentiation of retinal amacrine and horizontal interneurons. Nat. Commun. 4, 1813 (2013).
64. Tronche, F. et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 23, 99-103 (1999).
65. Madisen, L. et al. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat. Neurosci. 15, 793-802 (2012).
66. López-Bendito, G. et al. Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 125, 127-142 (2006).
67. Carron, R. et al. Early hypersynchrony in juvenile PINK1(-)/(-) motor cortex is rescued by antidromic stimulation. Front. Syst. Neurosci. 8, 95 (2014).