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Thalamic low frequency activity facilitates resting-state cortical interhemispheric MRI functional connectivity.
Neuroimage 2019; 201:115985N

Abstract

Blood-oxygen-level-dependent (BOLD) resting-state functional MRI (rsfMRI) has emerged as a valuable tool to map complex brain-wide functional networks, predict cognitive performance and identify biomarkers for neurological diseases. However, interpreting these findings poses challenges, as the neural basis of rsfMRI connectivity remains poorly understood. The thalamus serves as a relay station and modulates diverse long-range cortical functional integrations, yet few studies directly interrogate its role in brain-wide rsfMRI connectivity. Utilizing a multi-modal approach of rsfMRI, optogenetic stimulation and multi-depth cortical electrophysiology recording, we examined whether and how the somatosensory thalamus contributes to cortical interhemispheric rsfMRI connectivity. We found that low frequency (1 Hz) optogenetic stimulation of somatosensory-specific ventral posteromedial (VPM) thalamocortical excitatory neurons increased the interhemispheric rsfMRI connectivity in all examined sensory cortices, somatosensory, visual and auditory, and the local intrahemispheric BOLD activity at infraslow frequency (0.01-0.1 Hz). In parallel, multi-depth local field potential recordings at bilateral primary somatosensory cortices revealed increased interhemispheric correlations of low frequency neural oscillations (i.e., mainly < 10 Hz) at all cortical layers. Meanwhile, pharmacologically inhibiting VPM thalamocortical neurons decreased interhemispheric rsfMRI connectivity and local intrahemispheric infraslow BOLD activity in all sensory cortices. Taken together, our findings demonstrate that low frequency activities in the thalamo-cortical network contribute to brain-wide rsfMRI connectivity, highlighting the thalamus as a pivotal region that underlies rsfMRI connectivity.

Authors+Show Affiliations

Laboratory of Biomedical Imaging and Signal Processing, The University of Hong Kong, Hong Kong, China; Department of Electrical and Electronic Engineering, The University of Hong Kong, Hong Kong, China.Laboratory of Biomedical Imaging and Signal Processing, The University of Hong Kong, Hong Kong, China; Department of Electrical and Electronic Engineering, The University of Hong Kong, Hong Kong, China.Laboratory of Biomedical Imaging and Signal Processing, The University of Hong Kong, Hong Kong, China; Department of Electrical and Electronic Engineering, The University of Hong Kong, Hong Kong, China; Department of Neurology and Neurological Sciences, Stanford University, Stanford, United States.Laboratory of Biomedical Imaging and Signal Processing, The University of Hong Kong, Hong Kong, China; Department of Electrical and Electronic Engineering, The University of Hong Kong, Hong Kong, China.Laboratory of Biomedical Imaging and Signal Processing, The University of Hong Kong, Hong Kong, China; Department of Electrical and Electronic Engineering, The University of Hong Kong, Hong Kong, China. Electronic address: ewu@eee.hku.hk.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31299370

Citation

Wang, Xunda, et al. "Thalamic Low Frequency Activity Facilitates Resting-state Cortical Interhemispheric MRI Functional Connectivity." NeuroImage, vol. 201, 2019, p. 115985.
Wang X, Leong ATL, Chan RW, et al. Thalamic low frequency activity facilitates resting-state cortical interhemispheric MRI functional connectivity. Neuroimage. 2019;201:115985.
Wang, X., Leong, A. T. L., Chan, R. W., Liu, Y., & Wu, E. X. (2019). Thalamic low frequency activity facilitates resting-state cortical interhemispheric MRI functional connectivity. NeuroImage, 201, p. 115985. doi:10.1016/j.neuroimage.2019.06.063.
Wang X, et al. Thalamic Low Frequency Activity Facilitates Resting-state Cortical Interhemispheric MRI Functional Connectivity. Neuroimage. 2019 Nov 1;201:115985. PubMed PMID: 31299370.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Thalamic low frequency activity facilitates resting-state cortical interhemispheric MRI functional connectivity. AU - Wang,Xunda, AU - Leong,Alex T L, AU - Chan,Russell W, AU - Liu,Yilong, AU - Wu,Ed X, Y1 - 2019/07/09/ PY - 2018/12/14/received PY - 2019/06/18/revised PY - 2019/06/26/accepted PY - 2019/7/13/pubmed PY - 2019/7/13/medline PY - 2019/7/13/entrez KW - Cortical layers KW - Optogenetic KW - Resting-state MRI functional connectivity KW - Thalamus KW - fMRI SP - 115985 EP - 115985 JF - NeuroImage JO - Neuroimage VL - 201 N2 - Blood-oxygen-level-dependent (BOLD) resting-state functional MRI (rsfMRI) has emerged as a valuable tool to map complex brain-wide functional networks, predict cognitive performance and identify biomarkers for neurological diseases. However, interpreting these findings poses challenges, as the neural basis of rsfMRI connectivity remains poorly understood. The thalamus serves as a relay station and modulates diverse long-range cortical functional integrations, yet few studies directly interrogate its role in brain-wide rsfMRI connectivity. Utilizing a multi-modal approach of rsfMRI, optogenetic stimulation and multi-depth cortical electrophysiology recording, we examined whether and how the somatosensory thalamus contributes to cortical interhemispheric rsfMRI connectivity. We found that low frequency (1 Hz) optogenetic stimulation of somatosensory-specific ventral posteromedial (VPM) thalamocortical excitatory neurons increased the interhemispheric rsfMRI connectivity in all examined sensory cortices, somatosensory, visual and auditory, and the local intrahemispheric BOLD activity at infraslow frequency (0.01-0.1 Hz). In parallel, multi-depth local field potential recordings at bilateral primary somatosensory cortices revealed increased interhemispheric correlations of low frequency neural oscillations (i.e., mainly < 10 Hz) at all cortical layers. Meanwhile, pharmacologically inhibiting VPM thalamocortical neurons decreased interhemispheric rsfMRI connectivity and local intrahemispheric infraslow BOLD activity in all sensory cortices. Taken together, our findings demonstrate that low frequency activities in the thalamo-cortical network contribute to brain-wide rsfMRI connectivity, highlighting the thalamus as a pivotal region that underlies rsfMRI connectivity. SN - 1095-9572 UR - https://www.unboundmedicine.com/medline/citation/31299370/Thalamic_low_frequency_activity_facilitates_resting-state_cortical_interhemispheric_MRI_functional_connectivity L2 - https://linkinghub.elsevier.com/retrieve/pii/S1053-8119(19)30560-9 DB - PRIME DP - Unbound Medicine ER -