Functional Connectivity with Cortical Depth Assessed by Resting State FMRI of Subregions of S1 in Squirrel Monkeys

Overview

Journal Hum Brain Mapp

Publisher Wiley

Specialty Neurology

Date 2018 Sep 26

PMID 30251760

Citations 8

Authors

Arabinda Mishra

Shantanu Majumdar

Feng Wang

George H Wilson 3rd

John C Gore

Li Min Chen

Affiliations

Soon will be listed here.

Abstract

Whereas resting state blood oxygenation-level dependent (BOLD) functional MRI has been widely used to assess functional connectivity between cortical regions, the laminar specificity of such measures is poorly understood. This study aims to determine: (a) whether the resting state functional connectivity (rsFC) between two functionally related cortical regions varies with cortical depth, (b) the relationship between layer-resolved tactile stimulus-evoked activation pattern and interlayer rsFC pattern between two functionally distinct but related somatosensory areas 3b and 1, and (c) the effects of spatial resolution on rsFC measures. We examined the interlayer rsFC between areas 3b and 1 of squirrel monkeys under anesthesia using tactile stimulus-driven and resting state BOLD acquisitions at submillimeter resolution. Consistent with previous observations in the areas 3b and 1, we detected robust stimulus-evoked BOLD activations with foci were confined mainly to the upper layers (centered at 21% of the cortical depth). By carefully placing seeds in upper, middle, and lower layers of areas 3b and 1, we observed strong rsFC between upper and middle layers of these two areas. The layer-resolved activation patterns in areas 3b and 1 agree with their interlayer rsFC patterns, and are consistent with the known anatomical connections between layers. In summary, using BOLD rsFC pattern, we identified an interlayer interareal microcircuit that shows strong intrinsic functional connections between upper and middle layer areas 3b and 1. RsFC can be used as a robust invasive tool to probe interlayer corticocortical microcircuits.

Citing Articles

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Sengupta A, Yang P, Reed J, Mishra A, Wang F, Manzanera Esteve I Neuroimage Clin. 2025; 45:103753.

PMID: 39983550 PMC: 11889736. DOI: 10.1016/j.nicl.2025.103753.

Layer-specific BOLD effects in gradient and spin-echo acquisitions in somatosensory cortex.

Yang Z, Arabinda M, Wang F, Chen L, Gore J Magn Reson Med. 2024; 93(3):1314-1328.

PMID: 39370926 PMC: 11680728. DOI: 10.1002/mrm.30326.

Detection and characterization of resting state functional networks in squirrel monkey brain.

Sengupta A, Wang F, Mishra A, Reed J, Chen L, Gore J Cereb Cortex Commun. 2023; 4(3):tgad018.

PMID: 37753115 PMC: 10518810. DOI: 10.1093/texcom/tgad018.

Pre-processing of Sub-millimeter GE-BOLD fMRI Data for Laminar Applications.

Pais-Roldan P, Yun S, Jon Shah N Front Neuroimaging. 2023; 1:869454.

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Pais-Roldan P, Yun S, Palomero-Gallagher N, Jon Shah N Front Neurosci. 2023; 17:1151544.

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References

Silva A, Koretsky A . Laminar specificity of functional MRI onset times during somatosensory stimulation in rat. Proc Natl Acad Sci U S A. 2002; 99(23):15182-7. PMC: 137564. DOI: 10.1073/pnas.222561899. View

Chen L, Mishra A, Newton A, Morgan V, Stringer E, Rogers B . Fine-scale functional connectivity in somatosensory cortex revealed by high-resolution fMRI. Magn Reson Imaging. 2011; 29(10):1330-7. PMC: 3285506. DOI: 10.1016/j.mri.2011.08.001. View

Opris I . Inter-laminar microcircuits across neocortex: repair and augmentation. Front Syst Neurosci. 2013; 7:80. PMC: 3832795. DOI: 10.3389/fnsys.2013.00080. View

Thomson A, Bannister A . Interlaminar connections in the neocortex. Cereb Cortex. 2002; 13(1):5-14. DOI: 10.1093/cercor/13.1.5. View

Baek K, Shim W, Jeong J, Radhakrishnan H, Rosen B, Boas D . Layer-specific interhemispheric functional connectivity in the somatosensory cortex of rats: resting state electrophysiology and fMRI studies. Brain Struct Funct. 2015; 221(5):2801-15. PMC: 4681693. DOI: 10.1007/s00429-015-1073-0. View

Bandettini P . The BOLD plot thickens: sign- and layer-dependent hemodynamic changes with activation. Neuron. 2012; 76(3):468-9. DOI: 10.1016/j.neuron.2012.10.026. View

Shi Z, Wu R, Yang P, Wang F, Wu T, Mishra A . High spatial correspondence at a columnar level between activation and resting state fMRI signals and local field potentials. Proc Natl Acad Sci U S A. 2017; 114(20):5253-5258. PMC: 5441782. DOI: 10.1073/pnas.1620520114. View

Zhao F, Wang P, Hendrich K, Ugurbil K, Kim S . Cortical layer-dependent BOLD and CBV responses measured by spin-echo and gradient-echo fMRI: insights into hemodynamic regulation. Neuroimage. 2006; 30(4):1149-60. DOI: 10.1016/j.neuroimage.2005.11.013. View

Polimeni J, Bhat H, Witzel T, Benner T, Feiweier T, Inati S . Reducing sensitivity losses due to respiration and motion in accelerated echo planar imaging by reordering the autocalibration data acquisition. Magn Reson Med. 2015; 75(2):665-79. PMC: 4580494. DOI: 10.1002/mrm.25628. View

10.

Chen G, Wang F, Gore J, Roe A . Layer-specific BOLD activation in awake monkey V1 revealed by ultra-high spatial resolution functional magnetic resonance imaging. Neuroimage. 2012; 64:147-55. PMC: 3508288. DOI: 10.1016/j.neuroimage.2012.08.060. View

11.

Ichinohe N . Small-scale module of the rat granular retrosplenial cortex: an example of the minicolumn-like structure of the cerebral cortex. Front Neuroanat. 2012; 5:69. PMC: 3254062. DOI: 10.3389/fnana.2011.00069. View

12.

Feinberg D, Vu A, Beckett A . Pushing the limits of ultra-high resolution human brain imaging with SMS-EPI demonstrated for columnar level fMRI. Neuroimage. 2017; 164:155-163. PMC: 5961953. DOI: 10.1016/j.neuroimage.2017.02.020. View

13.

Kim T, Kim S . Cortical layer-dependent arterial blood volume changes: improved spatial specificity relative to BOLD fMRI. Neuroimage. 2009; 49(2):1340-9. PMC: 2819732. DOI: 10.1016/j.neuroimage.2009.09.061. View

14.

Maier A, Adams G, Aura C, Leopold D . Distinct superficial and deep laminar domains of activity in the visual cortex during rest and stimulation. Front Syst Neurosci. 2010; 4. PMC: 2928665. DOI: 10.3389/fnsys.2010.00031. View

15.

Olman C, Harel N, Feinberg D, He S, Zhang P, Ugurbil K . Layer-specific fMRI reflects different neuronal computations at different depths in human V1. PLoS One. 2012; 7(3):e32536. PMC: 3308958. DOI: 10.1371/journal.pone.0032536. View

16.

Felleman D, Van Essen D . Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex. 1991; 1(1):1-47. DOI: 10.1093/cercor/1.1.1-a. View

17.

Guidi M, Huber L, Lampe L, Gauthier C, Moller H . Lamina-dependent calibrated BOLD response in human primary motor cortex. Neuroimage. 2016; 141:250-261. DOI: 10.1016/j.neuroimage.2016.06.030. View

18.

Tak S, Polimeni J, Wang D, Yan L, Chen J . Associations of resting-state fMRI functional connectivity with flow-BOLD coupling and regional vasculature. Brain Connect. 2014; 5(3):137-46. PMC: 4394176. DOI: 10.1089/brain.2014.0299. View

19.

Wu T, Mishra A, Wang F, Yang P, Gore J, Chen L . Effects of isoflurane anesthesia on resting-state fMRI signals and functional connectivity within primary somatosensory cortex of monkeys. Brain Behav. 2016; 6(12):e00591. PMC: 5167001. DOI: 10.1002/brb3.591. View

20.

Fox M, Snyder A, Vincent J, Raichle M . Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron. 2007; 56(1):171-84. DOI: 10.1016/j.neuron.2007.08.023. View