Motor cortex neurovascular coupling: inputs from ultra–high-frequency ultrasound imaging in humans

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OBJECTIVE

Neurovascular coupling reflects the link between neural activity and changes in cerebral blood flow. Despite many technical advances in functional exploration of the brain, including functional MRI, there are only a few reports of direct evidence of neurovascular coupling in humans. The authors aimed to explore, for the first time in humans, the local cerebral blood flow of the primary motor cortex using ultra–high-frequency ultrasound (UHF-US) Doppler imaging to detect low blood flow velocity (1 mm/sec).

METHODS

Four consecutive patients underwent awake craniotomy for glioma resection using cortical direct electrostimulation for brain mapping. The primary motor cortical area eliciting flexion of the contralateral forearm was identified. UHF-US color Doppler imaging of this cortical area was acquired at rest, during repeated spontaneous forearm flexion, and immediately after the movement’s termination. In each condition, the surface areas of the detectable vessels were measured after extraction of non–zero-velocity colored pixels and summed.

RESULTS

During movement, local cerebral blood flow increased significantly by 14.4% (range 5%–30%) compared with baseline. Immediately after the termination of movements, the local hyperemia decreased significantly by 8.6% (range 1.9%–15.7%).

CONCLUSIONS

To the authors’ knowledge, this study is the first to provide a real-time demonstration of the neurovascular coupling in the human cortex by ultrasound imaging. They assume that UHF-US may be used to gather original and advanced data on brain functioning, which could be used to help in the identification of functional cortical areas during brain surgery.

Clinical trial registration no.: NCT03179176 (clinicaltrials.gov)

ABBREVIATIONS BOLD = blood oxygen level–dependent; CBF = cerebral blood flow; DES = direct electrostimulation; fUS = functional US; mSA = median surface area; NVC = neurovascular coupling; TCD = transcranial Doppler; UHF-US = ultra–high-frequency US; US = ultrasound.

Article Information

Correspondence Fabien Almairac: Hôpital Pasteur 2, Nice, France. almairac.f@chu-nice.fr.

INCLUDE WHEN CITING Published online November 9, 2018; DOI: 10.3171/2018.5.JNS18754.

Disclosures Dr. Demarcy: employee of Oticon Medical.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Study methods, UHF-US image acquisition, and processing. A: Intraoperative photograph of the left motor area and functional mapping using DES. Tags 1–4 are located in the precentral gyrus. DES applied on the tag 4 cortical site induced flexion of the contralateral forearm (inset). B: Intraoperative photograph showing the UHF-US Doppler probe within the sterile sheath positioned on cortical site 4, during spontaneous continuous flexion of the contralateral forearm (inset). C: Morphological UHF-US image acquired over the motor area (tag 4) showing the central sulcus (black arrow), the precentral gyrus, and the underlying white matter. D: Image processing after UHF-US color Doppler imaging, acquired over the motor area tag 4, showing pial superficial and sulcal vessels and their penetrating branches (white arrows). All colored pixels with a nonzero velocity (delineated in yellow) were extracted and summed to be converted into square millimeters. Figure is available in color online only.

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    Motor cortex CBF changes during movements in UHF-US in 4 patients who underwent awake craniotomy for tumor resection. A: Preoperative MR images showing the location of the brain tumors. B: Intraoperative photographs showing cortical mapping using DES. Yellow circles indicate motor cortical sites where DES induced forearm flexion, which were further explored using UHF-US. C: UHF-US color Doppler imaging at rest1 before movements. D: UHF-US color Doppler imaging during repeated forearm flexion. Local CBF in the motor area increased during movements compared with rest1 and rest2 conditions. E: UHF-US color Doppler imaging at rest2 after termination of movements. CS = central sulcus; MC = motor cortex; PCS = precentral sulcus. Figure is available in color online only.

  • View in gallery

    Changes in the surface area of the vessels, measured on UHF-US Doppler images, during rest and movements, in 4 patients who underwent awake craniotomy. The “rest1,” “movement,” and “rest2” annotations and their underlying segments represent the time duration of each experimental condition. Red curve: median value of vessels’ surface area over a 5-second period (−2.5 seconds; +2.5 seconds). Gray curve: absolute value of vessels’ surface area. Figure is available in color online only.

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