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

Abstract : To ensure appropriate blood supply through the brain, the cerebral blood vessels, neurons, and as-trocyte glial cells must interact according to complex mechanisms. This interaction, named "neurovascular coupling" (NVC), describes the link between neuronal activity and cerebral blood flow (CBF) changes. 25 Several methods have been developed to assess the NVC in humans by exploring either cerebral tissue oxygenation using functional MRI, near-infrared spectrosco-py, or positron emission tomography, or CBF changes using transcranial Doppler (TCD) ultrasonography. 9,21 TCD ultrasonography is the ultrasound (US) imaging technique mostly used in the clinic to explore CBF because of its high temporal resolution and noninvasive nature. For example, sensorimotor or cognitive stimulatory effects on cerebral blood velocity have been studied using low-frequency (≤ 2-MHz) transducers. 4 In healthy individuals, this response leads to an average 10%-20% increase in CBF in the posterior cerebral artery during visual stimulation, 1 and a 5%-8% increase in the middle cerebral artery during a cognitive task. 22 However, despite good spatiotemporal resolution, TCD US imaging is limited to the exploration of large cerebral vessels and is not able to detect subtle changes of low blood flow in cortical vessels that may occur during a task. Recently, very high frame rate US imaging (> 10,000 frames per second) was shown to enable high-resolution and high-sensitivity power Doppler imaging, 2,29 allowing 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. 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 electro-stimulation 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 neurovas-cular 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) https://thejns.org/doi/abs/10.3171/2018.5.JNS18754
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Fabien Almairac, Denys Fontaine, Thomas Demarcy, Hervé Delingette, Stephanie Beuil, et al.. Motor cortex neurovascular coupling: inputs from ultra–high-frequency ultrasound imaging in humans. Journal of Neurosurgery, American Association of Neurological Surgeons, 2018, pp.1-7. ⟨10.3171/2018.5.jns18754⟩. ⟨hal-01984498⟩

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