Effects of Isoflurane Anesthesia on Resting-state FMRI Signals and Functional Connectivity Within Primary Somatosensory Cortex of Monkeys

Overview

Journal Brain Behav

Specialty Psychology

Date 2016 Dec 30

PMID 28032008

Citations 29

Authors

Tung-Lin Wu

Arabinda Mishra

Feng Wang

Pai-Feng Yang

John C Gore

Li Min Chen

Affiliations

Soon will be listed here.

Abstract

Introduction: Correlated low-frequency fluctuations of resting-state functional magnetic resonance imaging (rsfMRI) signals have been widely used for inferring intrinsic brain functional connectivity (FC). In animal studies, accurate estimate of anesthetic effects on rsfMRI signals is demanded for reliable interpretations of FC changes. We have previously shown that inter-regional FC can reliably delineate local millimeter-scale circuits within digit representations of primary somatosensory cortex (S1) subregions (areas 3a, 3b, and 1) in monkeys under isoflurane anesthesia. The goals of this study are to determine (1) the general effects of isoflurane on rsfMRI signals in the S1 circuit and (2) whether the effects are functional- and regional- dependent, by quantifying the relationships between isoflurane levels, power and inter-regional correlation coefficients in digit and face regions of distinct S1 subregions.

Methods: Functional MRI data were collected from male adult squirrel monkeys at three different isoflurane levels (1.25%, 0.875%, and 0.5%). All scans were acquired on a 9.4T magnet with a 3-cm-diameter surface transmit-receive coil centered over the S1 cortex. Power and seed-based inter-regional functional connectivity analyses were subsequently performed.

Results: As anesthesia level increased, we observed (1) diminishing amplitudes of signal fluctuations, (2) reduced power of fluctuations in the low-frequency band used for connectivity measurements, (3) decreased inter-voxel connectivity around seed regions, and (4) weakened inter-regional FC across all pairs of regions of interest (digit-to-digit). The low-frequency power measures derived from rsfMRI signals from control muscle regions, however, did not exhibit any isoflurane level-related changes. Within the isoflurane dosage range we tested, the inter-regional functional connectivity differences were still detectable, and the effects of isoflurane did not differ across region-of-interest (ROI) pairs.

Conclusion: Our data demonstrate that isoflurane induced similar dose-dependent suppressive effects on the power of rsfMRI signals and local fine-scale FC across functionally related but distinct S1 subregions.

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References

Deshpande G, Kerssens C, Sebel P, Hu X . Altered local coherence in the default mode network due to sevoflurane anesthesia. Brain Res. 2010; 1318:110-21. PMC: 2845285. DOI: 10.1016/j.brainres.2009.12.075. View

Liu X, Pillay S, Li R, Vizuete J, Pechman K, Schmainda K . Multiphasic modification of intrinsic functional connectivity of the rat brain during increasing levels of propofol. Neuroimage. 2013; 83:581-92. PMC: 3815996. DOI: 10.1016/j.neuroimage.2013.07.003. 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

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

Hemmings Jr H . Sodium channels and the synaptic mechanisms of inhaled anaesthetics. Br J Anaesth. 2009; 103(1):61-9. PMC: 2700013. DOI: 10.1093/bja/aep144. View

Jonckers E, Delgado Y Palacios R, Shah D, Guglielmetti C, Verhoye M, Van Der Linden A . Different anesthesia regimes modulate the functional connectivity outcome in mice. Magn Reson Med. 2013; 72(4):1103-12. DOI: 10.1002/mrm.24990. View

Lv P, Xiao Y, Liu B, Wang Y, Zhang X, Sun H . Dose-dependent effects of isoflurane on regional activity and neural network function: A resting-state fMRI study of 14 rhesus monkeys: An observational study. Neurosci Lett. 2015; 611:116-22. DOI: 10.1016/j.neulet.2015.11.037. View

Shmuel A, Leopold D . Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: Implications for functional connectivity at rest. Hum Brain Mapp. 2008; 29(7):751-61. PMC: 6870786. DOI: 10.1002/hbm.20580. View

Chen L, Qi H, Kaas J . Dynamic reorganization of digit representations in somatosensory cortex of nonhuman primates after spinal cord injury. J Neurosci. 2012; 32(42):14649-63. PMC: 3498942. DOI: 10.1523/JNEUROSCI.1841-12.2012. View

10.

Barttfeld P, Uhrig L, Sitt J, Sigman M, Jarraya B, Dehaene S . Signature of consciousness in the dynamics of resting-state brain activity. Proc Natl Acad Sci U S A. 2015; 112(3):887-92. PMC: 4311826. DOI: 10.1073/pnas.1418031112. View

11.

Zou Q, Wu C, Stein E, Zang Y, Yang Y . Static and dynamic characteristics of cerebral blood flow during the resting state. Neuroimage. 2009; 48(3):515-24. PMC: 2739419. DOI: 10.1016/j.neuroimage.2009.07.006. View

12.

Hutchison R, Hutchison M, Manning K, Menon R, Everling S . Isoflurane induces dose-dependent alterations in the cortical connectivity profiles and dynamic properties of the brain's functional architecture. Hum Brain Mapp. 2014; 35(12):5754-75. PMC: 6869297. DOI: 10.1002/hbm.22583. View

13.

Wang Z, Chen L, Negyessy L, Friedman R, Mishra A, Gore J . The relationship of anatomical and functional connectivity to resting-state connectivity in primate somatosensory cortex. Neuron. 2013; 78(6):1116-26. PMC: 3723346. DOI: 10.1016/j.neuron.2013.04.023. View

14.

Lu H, Zuo Y, Gu H, Waltz J, Zhan W, Scholl C . Synchronized delta oscillations correlate with the resting-state functional MRI signal. Proc Natl Acad Sci U S A. 2007; 104(46):18265-9. PMC: 2084331. DOI: 10.1073/pnas.0705791104. View

15.

Lee M, Smyser C, Shimony J . Resting-state fMRI: a review of methods and clinical applications. AJNR Am J Neuroradiol. 2012; 34(10):1866-72. PMC: 4035703. DOI: 10.3174/ajnr.A3263. View

16.

Hutchison R, Everling S . Monkey in the middle: why non-human primates are needed to bridge the gap in resting-state investigations. Front Neuroanat. 2012; 6:29. PMC: 3405297. DOI: 10.3389/fnana.2012.00029. View

17.

Peltier S, Kerssens C, Hamann S, Sebel P, Byas-Smith M, Hu X . Functional connectivity changes with concentration of sevoflurane anesthesia. Neuroreport. 2005; 16(3):285-8. DOI: 10.1097/00001756-200502280-00017. View

18.

Qi H, Chen L, Kaas J . Reorganization of somatosensory cortical areas 3b and 1 after unilateral section of dorsal columns of the spinal cord in squirrel monkeys. J Neurosci. 2011; 31(38):13662-75. PMC: 3183096. DOI: 10.1523/JNEUROSCI.2366-11.2011. View

19.

Heinke W, Koelsch S . The effects of anesthetics on brain activity and cognitive function. Curr Opin Anaesthesiol. 2006; 18(6):625-31. DOI: 10.1097/01.aco.0000189879.67092.12. View

20.

Chen L, Mishra A, Yang P, Wang F, Gore J . Injury alters intrinsic functional connectivity within the primate spinal cord. Proc Natl Acad Sci U S A. 2015; 112(19):5991-6. PMC: 4434735. DOI: 10.1073/pnas.1424106112. View