journal article·2025-05Open access

Disentangling the Switching Behavior in Functional Connectivity Dynamics in Autism Spectrum Disorder: Insights from Developmental Cohort Analysis and Molecular‐Cellular Associations

Wei Li, Xia Qiu, Jin Chen, Kexuan Chen, Meiling Chen, Yinyan Wang, Wenjie Sun, Jing Su, Yongchang Chen, Xiaobao Liu, Congying Chu, Jiaojian Wang

Advanced Science· Volume 12· Issue 20

Abstract

Abstract Characterizing the transition or switching behavior between multistable brain states in functional connectivity dynamics (FCD) holds promise for uncovering the underlying neuropathology of Autism Spectrum Disorder (ASD). However, whether and how switching behaviors in FCD change in patients with developmental ASD, as well as their cellular and molecular basis, remains unexplored. This study develops a region‐wise FCD switching index (RFSI) to investigate the drivers of FCD. This work finds that brain regions within the salience, default mode, and frontoparietal networks serve as abnormal drivers of FCD in ASD across different developmental stages. Additionally, changes in RFSI at different developmental stages of ASD correlated with transcriptomic profiles and neurotransmitter density maps. Importantly, the abnormal RFSI identifies in humans has also been observed in genetically edited ASD monkeys. Finally, single‐nucleus RNA sequencing data from patients with developmental ASD are analyzed and aberrant switching behaviors in FCD may be mediated by somatostatin‐expressing interneurons and altered differentiation patterns in astrocyte State2. In conclusion, this study provides the first evidence of abnormal drivers of FCD across different stages of ASD and their associated cellular and molecular mechanisms. These findings deepen the understanding of ASD neuropathology and offer valuable insights into treatment strategies.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Functional Brain Connectivity Studies · Neural dynamics and brain function · Single-cell and spatial transcriptomics

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

State Key Laboratory of Primate Biomedical Research Institute of Primate Translational Medicine Kunming University of Science and Technology Kunming 650500 China

Faculty of Mechanical and Electrical Engineering Kunming University of Science and Technology Kunming 650500 China

Medical School Kunming University of Science and Technology Kunming 650500 China

Department of Clinical Psychology the First People's Hospital of Yunnan Province The Affiliated Hospital of Kunming University of Science and Technology Kunming 650500 China

Department of Neurosurgery Beijing Tiantan Hospital Capital Medical University Beijing 100070 China

Brainnetome Center & National Laboratory of Pattern Recognition Institute of Automation Chinese Academy of Sciences Beijing 100190 China

Yunnan Key Laboratory of Primate Biomedical Research Kunming 650500 China

References (100+)

Show source-provided references
1. 10.1089/brain.2011.000810.1089/brain.2011.0008 ↗
2. 10.1162/netn_a_0012110.1162/netn_a_00121 ↗
3. 10.1016/j.neuroimage.2015.12.01710.1016/j.neuroimage.2015.12.017 ↗
4. 10.1073/pnas.152536911310.1073/pnas.1525369113 ↗
5. 10.1002/hbm.2205810.1002/hbm.22058 ↗
6. 10.1038/s41467-019-10317-710.1038/s41467-019-10317-7 ↗
7. 10.1162/netn_a_0011610.1162/netn_a_00116 ↗
8. 10.1073/pnas.170512011410.1073/pnas.1705120114 ↗
9. 10.1073/pnas.140018111110.1073/pnas.1400181111 ↗
10. 10.1038/s41598-017-03073-510.1038/s41598-017-03073-5 ↗
11. 10.1016/j.neuroimage.2014.11.00110.1016/j.neuroimage.2014.11.001 ↗
12. 10.1038/s41467-021-26704-y10.1038/s41467-021-26704-y ↗
13. 10.1038/nrg234610.1038/nrg2346 ↗
14. 10.1176/appi.books.978089042559610.1176/appi.books.9780890425596 ↗
15. 10.1002/hbm.2376410.1002/hbm.23764 ↗
16. 10.1089/brain.2015.038910.1089/brain.2015.0389 ↗
17. 10.3389/fnhum.2019.0000610.3389/fnhum.2019.00006 ↗
18. 10.1002/aur.221210.1002/aur.2212 ↗
19. 10.1016/j.nicl.2017.05.02410.1016/j.nicl.2017.05.024 ↗
20. 10.1016/j.neuroimage.2018.06.00310.1016/j.neuroimage.2018.06.003 ↗
21. 10.1016/j.neubiorev.2009.06.00210.1016/j.neubiorev.2009.06.002 ↗
22. 10.1016/j.biopsych.2021.12.00410.1016/j.biopsych.2021.12.004 ↗
23. 10.1186/s13023-023-02619-310.1186/s13023-023-02619-3 ↗
24. 10.1038/s41380-021-01156-410.1038/s41380-021-01156-4 ↗
25. 10.1111/j.1601-183X.2007.00381.x10.1111/j.1601-183X.2007.00381.x ↗
26. 10.1016/S0006-3223(02)01601-310.1016/S0006-3223(02)01601-3 ↗
27. 10.1016/j.cell.2017.04.03510.1016/j.cell.2017.04.035 ↗
28. 10.1093/cercor/bhab16610.1093/cercor/bhab166 ↗
29. 10.1111/jmp.1212710.1111/jmp.12127 ↗
30. Reader J. R. · Comp. Med. · 2016 · 66 · 162
31. 10.1038/oby.2004.21910.1038/oby.2004.219 ↗
32. 10.18632/genesandcancer.17010.18632/genesandcancer.170 ↗
33. 10.1089/ars.2010.331110.1089/ars.2010.3311 ↗
34. 10.1016/j.tics.2018.10.00510.1016/j.tics.2018.10.005 ↗
35. 10.1523/JNEUROSCI.2830-16.201610.1523/JNEUROSCI.2830-16.2016 ↗
36. 10.1038/s41593-022-01186-310.1038/s41593-022-01186-3 ↗
37. 10.1016/j.neuroimage.2021.11787810.1016/j.neuroimage.2021.117878 ↗
38. 10.3389/fnana.2017.0007810.3389/fnana.2017.00078 ↗
39. 10.1038/nprot.2016.01510.1038/nprot.2016.015 ↗
40. Scidraw S. · Human Brain · 2020
41. Scidraw S. · human brain silhouette · 2020
42. Breault M. S. · Human Brain · 2020
43. Breault M. S. · Monkey Brain · 2020
44. Kraemer P. · synapse · 2020
45. 10.1038/s41467-021-26704-y10.1038/s41467-021-26704-y ↗
46. 10.1152/jn.00338.201110.1152/jn.00338.2011 ↗
47. 10.1038/nmeth.446310.1038/nmeth.4463 ↗
48. 10.1016/j.neuron.2020.08.01210.1016/j.neuron.2020.08.012 ↗
49. 10.1016/S0140-6736(18)31129-210.1016/S0140-6736(18)31129-2 ↗
50. 10.1038/tp.2014.2410.1038/tp.2014.24 ↗
51. 10.1007/s10548-019-00744-610.1007/s10548-019-00744-6 ↗
52. 10.1016/j.neuroimage.2017.02.06610.1016/j.neuroimage.2017.02.066 ↗
53. 10.1038/ncomms1604810.1038/ncomms16048 ↗
54. 10.1093/cercor/bhs35210.1093/cercor/bhs352 ↗
55. 10.1016/j.neuron.2014.10.01510.1016/j.neuron.2014.10.015 ↗
56. 10.1016/j.neuroimage.2009.12.01110.1016/j.neuroimage.2009.12.011 ↗
57. 10.1073/pnas.121685611010.1073/pnas.1216856110 ↗
58. 10.1016/j.tics.2017.11.00210.1016/j.tics.2017.11.002 ↗
59. 10.7554/eLife.6211610.7554/eLife.62116 ↗
60. 10.1126/sciadv.abq385110.1126/sciadv.abq3851 ↗
61. 10.1126/sciadv.abf270910.1126/sciadv.abf2709 ↗
62. 10.1016/j.neuron.2015.09.00810.1016/j.neuron.2015.09.008 ↗
63. 10.1038/nature0910810.1038/nature09108 ↗
64. 10.1007/s00429-010-0262-010.1007/s00429-010-0262-0 ↗
65. 10.1177/117906951985180910.1177/1179069519851809 ↗
66. 10.1038/nrn331310.1038/nrn3313 ↗
67. 10.1038/s41467-020-20039-w10.1038/s41467-020-20039-w ↗
68. 10.3389/neuro.09.004.200910.3389/neuro.09.004.2009 ↗
69. 10.1093/cercor/bhi06310.1093/cercor/bhi063 ↗
70. 10.1007/s00702-022-02555-910.1007/s00702-022-02555-9 ↗
71. 10.24272/j.issn.2095-8137.2021.25110.24272/j.issn.2095-8137.2021.251 ↗
72. 10.1007/s00401-017-1736-410.1007/s00401-017-1736-4 ↗
73. 10.1371/journal.pone.002148910.1371/journal.pone.0021489 ↗
74. Higo N. · Front. Syst. Neurosci. · 2021 · 15
75. 10.1007/s12264-023-01067-010.1007/s12264-023-01067-0 ↗
76. 10.1016/j.neubiorev.2005.07.00210.1016/j.neubiorev.2005.07.002 ↗
77. 10.1093/scan/nsp01710.1093/scan/nsp017 ↗
78. 10.1016/j.nicl.2018.04.03610.1016/j.nicl.2018.04.036 ↗
79. 10.1038/8295910.1038/82959 ↗
80. 10.1016/j.nicl.2013.10.01110.1016/j.nicl.2013.10.011 ↗
81. 10.1093/cercor/bhaa38010.1093/cercor/bhaa380 ↗
82. 10.1038/nature1298310.1038/nature12983 ↗
83. 10.1038/s41467-020-16710-x10.1038/s41467-020-16710-x ↗
84. 10.1016/j.cell.2017.09.02010.1016/j.cell.2017.09.020 ↗
85. 10.1073/pnas.030533710110.1073/pnas.0305337101 ↗
86. 10.1016/j.celrep.2019.01.03110.1016/j.celrep.2019.01.031 ↗
87. 10.1038/ejhg.2008.14810.1038/ejhg.2008.148 ↗
88. 10.2147/NDT.S39005310.2147/NDT.S390053 ↗
89. 10.1093/cercor/bhu17810.1093/cercor/bhu178 ↗
90. 10.3389/fnins.2023.112542810.3389/fnins.2023.1125428 ↗
91. 10.1038/nature0961310.1038/nature09613 ↗
92. 10.1038/sj.jcbfm.960055810.1038/sj.jcbfm.9600558 ↗
93. 10.1111/jnc.1371310.1111/jnc.13713 ↗
94. 10.1002/jnr.2456010.1002/jnr.24560 ↗
95. 10.1016/j.pnpbp.2017.09.01110.1016/j.pnpbp.2017.09.011 ↗
96. 10.1016/j.pnpbp.2017.09.02610.1016/j.pnpbp.2017.09.026 ↗
97. 10.1038/s41380-021-01092-310.1038/s41380-021-01092-3 ↗
98. 10.1002/aur.274010.1002/aur.2740 ↗
99. 10.1007/s12264-021-00788-410.1007/s12264-021-00788-4 ↗
100. 10.1038/s41467-024-53211-710.1038/s41467-024-53211-7 ↗