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Evidence of Resting-state Activity in Propofol-anesthetized Patients with Intracranial Tumors

Rationale and Objectives

Resting-state (RS) networks, revealed by functional magnetic resonance imaging (fMRI) studies in healthy volunteers, have never been evaluated in anesthetized patients with brain tumors. Our purpose was to examine the presence of residual brain activity on the auditory network during propofol-induced loss of consciousness in patients with brain tumors.

Materials and Methods

Twenty subjects with intracranial masses were prospectively studied by means of intraoperative RS-fMRI acquisitions before any craniectomy. After performing single-subject independent component analysis, spatial maps and time courses were assigned to an auditory RS network template from the literature and compared via spatial regression coefficients.

Results

All fMRI data were of sufficient quality for further postprocessing. In all but two patients, the RS functional activity of the auditory network could be successfully mapped. In almost all patients, contralateral activation of the auditory network was present. No significant difference was found between the mean distance of the RS activity clusters and the lesion periphery for tumors located in the temporal gyri vs. those in other brain regions. The spatial deviation between the activated cluster in our experiment and the template was significantly ( P = 0.04) higher in patients with tumors located in the temporal gyri than in patients with tumors located in other regions.

Conclusions

Propofol-induced anesthesia in patients with intracranial lesions does not alter the blood-oxygenation level-depended signal, and independent component analysis of intraoperative RS-fMRI may allow assessment of the auditory network in a clinical setting.

Introduction

Resting-state functional magnetic resonance imaging (RS-fMRI) acquisitions, based on system-wide coherent blood-oxygenation level dependent (BOLD) signal fluctuations, visualize a set of regions suggesting an underlying functional relationship despite deprivation of external stimuli . In humans, fMRI-visualized RS activity has been shown to be stable throughout light sleep/wake cycles , during light sleep, deep sleep, or sedation , as well as during different levels of consciousness including propofol-induced loss of consciousness . The partial preservation of functional connectivity in the absence of consciousness has been attributed to preserved anatomical connections dissociated from higher cognitive functions .

Thus far, however, these RS networks, revealed by fMRI studies mostly in healthy volunteers, have never been evaluated in anesthetized patients with brain tumors. The present study investigated the feasibility of acquiring whole-brain RS-fMRI measurements in patients with brain tumors by means of intraoperative fMRI during pharmacological modulation of the level of consciousness. The anesthetic drug used was propofol because of its advantage over isoflurane/sevoflurane in keeping low subdural intracranial pressure and arteriovenous oxygen difference while keeping higher cerebral perfusion pressure in patients with brain tumors . Under the proof-of-principle study design, we orientated in the RS activity of the auditory cortex because it has been shown in many studies to be robustly identifiable across healthy subjects and patients , its analysis is relatively simple compared to other networks , and previous works have tested the influence of different anesthetics on its activation in healthy subjects. The auditory network involves the superior temporal gyrus, the transverse temporal gyrus (Heschl’s gyrus), the insula, and the postcentral gyrus. The primary auditory cortex has also known interactions with the angular gyrus, the supramarginal gyrus, Broca’s, and Wernicke’s areas.

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Materials and Methods

Ethics Statement

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Subjects

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Intraoperative MRI

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Anesthesia Protocol

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Image Processing and Data Analysis

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Table 1

Demographics, Clinical Data, and Resting-state BOLD Fluctuations Analysis of the Auditory Network in Our Patient Cohort

Patient (Age/Sex) Tumor Site (Side) z-value Ratio Tumor-Cluster Distance (mm) Template-Cluster Distance (mm) 1 (55/M) Gyrus temporalis medius (R) 13.9 3.9 60.4 15.0 2 (39/F) Gyrus temporalis medius et superior (L) 15.8 4.0 55.2 12.6 3 (23/M) Gyrus temporalis (L) 11.1 1.7 50.5 11.0 4 (27/M) Gyrus temporalis inferior (R) 13.1 7.3 43.9 16.5 5 (19/F) Temporomesial and temporobasal (R) 1.9 2.6 46.5 26.8 6 (33/M) Gyrus temporalis medius et superior (R) 12.0 1.9 29.7 12.8 7 (27/M) Skull base (R) 9.5 3.4 n.a. \* n.a. \* 8 (46/F) Thalamus (R) 3.7 4.2 48.4 13.6 9 (52/F) Skull base (L) 10.3 2.3 n.a. \* n.a. \* 10 (44/M) Gyrus parahippocampalis (L) 9.2 4.9 24.3 12.0 11 (34/M) Gyrus parahippocampalis (L) 14.4 3.2 39.9 14.7 12 (77/F) Gyrus frontalis superior (L) 12.2 0.9 41.2 8.7 13 (30/M) Gyrus frontalis inferior et insula (L) 8.8 6.9 52.8 3.5 14 (30/F) Gyrus frontalis superior et medius (R) 8.6 3.4 18.0 6.3 15 (72/M) Gyrus postcentralis (L) 10.5 2.3 34.1 12.3 16 (48/F) Gyrus postcentralis (L) 9.8 1.8 52.6 12.8 17 (52/F) Gyrus postcentralis (L) 13.0 2.9 60.2 15.7 18 (24/M) Gyrus precentralis (R) 9.1 2.3 32.1 8.2 19 (25/M) Gyrus precentralis (L) 3.2 3.3 60.9 14.1 20 (29/F) Gyrus precentralis (L) 9.6 1.8 53.8 18.5

BOLD, blood-oxygenation level dependent.

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Results

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Figure 1, Spatial maps (axial, coronal, and sagittal views) of the auditory network using single-subject independent component analysis (ICA) of resting-state functional magnetic resonance imaging (RS-fMRI) in an awake healthy control. Images are z-statistic superimposed on the anatomical T1-weighted images. The independent component 17 regarded in our RS-fMRI analysis contains the left superior temporal gyrus (Brodman area 22) on both sides and the right middle cingulate cortex (Brodman area 24). (Color version of figure available online.)

Figure 2, ( a ) Segmented tumor (in red color) in subject no. 19 and the spatial extent of component no. 17 (resting-state auditory activity, in yellow color) from the published group of healthy controls (reference no. 14) superimposed on normalized axial three-dimensional (3D) T1-weighted images. In ( b ), the activated area during intraoperative resting-state functional magnetic resonance imaging (fMRI) tumor (colored in green) from our patient is demonstrated in relation to the segmented tumor. (Color version of figure is available online.)

Figure 3, Spatial maps (axial, coronal, and sagittal views) of auditory network resulting from single-subject independent component analysis of resting-state functional magnetic resonance imaging (fMRI) data in two anesthetized patients. Each row corresponds to one component of the auditory network. The upper ( a , b ) rows present results from patient no. 14; the lower ( c , d ) rows show results from patient no. 2. Images are z-statistic superimposed on the anatomical T1-weighted images. (Color version of figure available online.)

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Discussion

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Conclusions

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