Brain Circuit-gene Expression Relationships and Neuroplasticity of Multisensory Cortices in Blind Children

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2017 Jun 14

PMID 28607055

Citations 23

Authors

Laura Ortiz-Teran

Ibai Diez

Tomas Ortiz

David L Perez

Jose Ignacio Aragon

Victor Costumero

Alvaro Pascual-Leone

Georges El Fakhri

Jorge Sepulcre

Affiliations

Soon will be listed here.

Abstract

Sensory deprivation reorganizes neurocircuits in the human brain. The biological basis of such neuroplastic adaptations remains elusive. In this study, we applied two complementary graph theory-based functional connectivity analyses, one to evaluate whole-brain functional connectivity relationships and the second to specifically delineate distributed network connectivity profiles downstream of primary sensory cortices, to investigate neural reorganization in blind children compared with sighted controls. We also examined the relationship between connectivity changes and neuroplasticity-related gene expression profiles in the cerebral cortex. We observed that multisensory integration areas exhibited enhanced functional connectivity in blind children and that this reorganization was spatially associated with the transcription levels of specific members of the cAMP Response Element Binding protein gene family. Using systems-level analyses, this study advances our understanding of human neuroplasticity and its genetic underpinnings following sensory deprivation.

Citing Articles

Brain spatial reconciliation through multisensory integration in the impact of pandemic fatigue on workplace.

Arinta R, Satwiko P, Widjaja R, Kusrohmaniah S Front Hum Neurosci. 2024; 18:1419889.

PMID: 39713173 PMC: 11659956. DOI: 10.3389/fnhum.2024.1419889.

Longitudinal stability of individual brain plasticity patterns in blindness.

Amaral L, Thomas P, Amedi A, Striem-Amit E Proc Natl Acad Sci U S A. 2024; 121(32):e2320251121.

PMID: 39078671 PMC: 11317565. DOI: 10.1073/pnas.2320251121.

A late-life neurogenetic signature of exposure to combat stress - A monozygotic discordant twin study.

Beucke J, Diez I, Sepulcre J, Mundorf A, Kaufmann C, Orr S J Psychiatr Res. 2024; 171:230-237.

PMID: 38316103 PMC: 11113072. DOI: 10.1016/j.jpsychires.2024.01.032.

Spatial transcriptomic patterns underlying amyloid-β and tau pathology are associated with cognitive dysfunction in Alzheimer's disease.

Yu M, Risacher S, Nho K, Wen Q, Oblak A, Unverzagt F Cell Rep. 2024; 43(2):113691.

PMID: 38244198 PMC: 10926093. DOI: 10.1016/j.celrep.2024.113691.

Longitudinal stability of individual brain plasticity patterns in blindness.

Amaral L, Thomas P, Amedi A, Striem-Amit E bioRxiv. 2023; .

PMID: 37986779 PMC: 10659359. DOI: 10.1101/2023.11.01.565196.

References

Hawellek D, Schepers I, Roeder B, Engel A, Siegel M, Hipp J . Altered intrinsic neuronal interactions in the visual cortex of the blind. J Neurosci. 2013; 33(43):17072-80. PMC: 6618438. DOI: 10.1523/JNEUROSCI.1625-13.2013. View

Jenkinson M, Bannister P, Brady M, Smith S . Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002; 17(2):825-41. DOI: 10.1016/s1053-8119(02)91132-8. View

Yang G, Pan F, Gan W . Stably maintained dendritic spines are associated with lifelong memories. Nature. 2009; 462(7275):920-4. PMC: 4724802. DOI: 10.1038/nature08577. View

Murray M, Matusz P, Amedi A . Neuroplasticity: Unexpected Consequences of Early Blindness. Curr Biol. 2015; 25(20):R998-R1001. DOI: 10.1016/j.cub.2015.08.054. View

Satterthwaite T, Wolf D, Loughead J, Ruparel K, Elliott M, Hakonarson H . Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. Neuroimage. 2012; 60(1):623-32. PMC: 3746318. DOI: 10.1016/j.neuroimage.2011.12.063. View

Kitanishi T, Ikegaya Y, Matsuki N, Yamada M . Experience-dependent, rapid structural changes in hippocampal pyramidal cell spines. Cereb Cortex. 2009; 19(11):2572-8. PMC: 2758678. DOI: 10.1093/cercor/bhp012. View

Richiardi J, Altmann A, Milazzo A, Chang C, Chakravarty M, Banaschewski T . BRAIN NETWORKS. Correlated gene expression supports synchronous activity in brain networks. Science. 2015; 348(6240):1241-4. PMC: 4829082. DOI: 10.1126/science.1255905. View

Sepulcre J, Sabuncu M, Yeo T, Liu H, Johnson K . Stepwise connectivity of the modal cortex reveals the multimodal organization of the human brain. J Neurosci. 2012; 32(31):10649-61. PMC: 3483645. DOI: 10.1523/JNEUROSCI.0759-12.2012. View

Zhang R, Rapin N, Ying Z, Shklanka E, Bodnarchuk T, Verge V . Zhangfei/CREB-ZF - a potential regulator of the unfolded protein response. PLoS One. 2013; 8(10):e77256. PMC: 3796484. DOI: 10.1371/journal.pone.0077256. View

10.

Collignon O, Dormal G, Albouy G, Vandewalle G, Voss P, Phillips C . Impact of blindness onset on the functional organization and the connectivity of the occipital cortex. Brain. 2013; 136(Pt 9):2769-83. DOI: 10.1093/brain/awt176. View

11.

Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguchi J . Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci. 2010; 33(3):121-9. DOI: 10.1016/j.tins.2010.01.001. View

12.

Sporns O . Network attributes for segregation and integration in the human brain. Curr Opin Neurobiol. 2013; 23(2):162-71. DOI: 10.1016/j.conb.2012.11.015. View

13.

Lowe M, Mock B, Sorenson J . Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage. 1998; 7(2):119-32. DOI: 10.1006/nimg.1997.0315. View

14.

Van Essen D . A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. Neuroimage. 2005; 28(3):635-62. DOI: 10.1016/j.neuroimage.2005.06.058. View

15.

Kandel E . The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Mol Brain. 2012; 5:14. PMC: 3514210. DOI: 10.1186/1756-6606-5-14. View

16.

Ortega-Martinez S . A new perspective on the role of the CREB family of transcription factors in memory consolidation via adult hippocampal neurogenesis. Front Mol Neurosci. 2015; 8:46. PMC: 4549561. DOI: 10.3389/fnmol.2015.00046. View

17.

Siuda-Krzywicka K, Bola L, Paplinska M, Sumera E, Jednorog K, Marchewka A . Massive cortical reorganization in sighted Braille readers. Elife. 2016; 5:e10762. PMC: 4805536. DOI: 10.7554/eLife.10762. View

18.

Van Dijk K, Hedden T, Venkataraman A, Evans K, Lazar S, Buckner R . Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J Neurophysiol. 2009; 103(1):297-321. PMC: 2807224. DOI: 10.1152/jn.00783.2009. View

19.

Krienen F, Yeo B, Ge T, Buckner R, Sherwood C . Transcriptional profiles of supragranular-enriched genes associate with corticocortical network architecture in the human brain. Proc Natl Acad Sci U S A. 2016; 113(4):E469-78. PMC: 4739529. DOI: 10.1073/pnas.1510903113. View

20.

Amedi A, Jacobson G, Hendler T, Malach R, Zohary E . Convergence of visual and tactile shape processing in the human lateral occipital complex. Cereb Cortex. 2002; 12(11):1202-12. DOI: 10.1093/cercor/12.11.1202. View