Bedside functional monitoring of the dynamic brain connectivity in human neonates

Baranger, Jérôme; Demené, Charlie; Frérot, Alice; Faure, Flora; Delanoë, Catherine; Serroune, Hicham; Houdouin, Alexandre; Mairesse, Jérôme; Biran, Valérie; Baud, Olivier; Tanter, Mickaël

doi:10.1038/s41467-021-21387-x

Cited by 67 publications

(44 citation statements)

References 34 publications

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“…This approach could also be required for animal models with less genetic homogeneity, which could yield more diverse brain and vasculature shapes across subjects. This would certainly be the case for functional ultrasound imaging with BPS in primates 34 or humans, in the case of intraoperative 35 , 36 settings or neonate imaging 37 , 38 , where there can be a high natural variability between subject brains.…”

Section: Discussionmentioning

confidence: 99%

A functional ultrasound brain GPS for automatic vascular-based neuronavigation

Nouhoum

Ferrier²,

Osmanski³

et al. 2021

Sci Rep

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Recent advances in ultrasound imaging triggered by transmission of ultrafast plane waves have rendered functional ultrasound (fUS) imaging a valuable neuroimaging modality capable of mapping cerebral vascular networks, but also for the indirect capture of neuronal activity with high sensitivity thanks to the neurovascular coupling. However, the expansion of fUS imaging is still limited by the difficulty to identify cerebral structures during experiments based solely on the Doppler images and the shape of the vessels. In order to tackle this challenge, this study introduces the vascular brain positioning system (BPS), a GPS of the brain. The BPS is a whole-brain neuronavigation system based on the on-the-fly automatic alignment of ultrafast ultrasensitive transcranial Power Doppler volumic images to common templates such as the Allen Mouse Brain Common Coordinates Framework. This method relies on the online registration of the complex cerebral vascular fingerprint of the studied animal to a pre-aligned reference vascular atlas, thus allowing rapid matching and identification of brain structures. We quantified the accuracy of the automatic registration using super-resolution vascular images obtained at the microscopic scale using Ultrasound Localization Microscopy and found a positioning error of 44 µm and 96 µm for intra-animal and inter-animal vascular registration, respectively. The proposed BPS approach outperforms the manual vascular landmark recognition performed by expert neuroscientists (inter-annotator errors of 215 µm and 259 µm). Using the online BPS approach coupled with the Allen Atlas, we demonstrated the capability of the system to position itself automatically over chosen anatomical structures and to obtain corresponding functional activation maps even in complex oblique planes. Finally, we show that the system can be used to acquire and estimate functional connectivity matrices automatically. The proposed functional ultrasound on-the-fly neuronavigation approach allows automatic brain navigation and could become a key asset to ensure standardized experiments and protocols for non-expert and expert researchers.

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Section: Discussionmentioning

confidence: 99%

A functional ultrasound brain GPS for automatic vascular-based neuronavigation

Nouhoum

Ferrier²,

Osmanski³

et al. 2021

Sci Rep

View full text Add to dashboard Cite

show abstract

“…This approach could also be required for animal models with less genetic homogeneity which could yield more diverse brain and vasculature shapes across subjects. This would certainly be the case for functional ultrasound imaging with BPS in primate [29] or humans in the case of intraoperative [30,31] settings or neonate imaging [32,33] where there can be a high natural variability between subject brains.…”

Section: Discussionmentioning

confidence: 99%

Fully-automatic ultrasound-based neuro-navigation : The functional ultrasound brain GPS

Nouhoum

Ferrier²,

Osmanski³

et al. 2021

Preprint

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Recent advances in ultrasound imaging triggered by ultrafast plane waves transmission have rendered functional ultrasound (fUS) imaging a valuable neuroimaging modality capable of mapping cerebral vascular networks, but also to indirectly capture neuronal activity with high sensitivity thanks to the neurovascular coupling. However, the expansion of fUS imaging is still limited by the difficulty to identify cerebral structures during experiments based solely on the Doppler images and the shape of the vessels. In order to tackle this challenge, this study introduces the vascular brain positioning system (BPS), a GPS of the brain. The BPS is a whole-brain neuro-navigation system based on the on-the-fly automatic alignment of ultrafast ultrasensitive transcranial Power Doppler volumic images to common templates such as the Allen mouse brain Common Coordinates Framework. This method relies on the online registration of the complex cerebral vascular fingerprint of the studied animal to a pre-aligned reference vascular atlas, thus allowing rapid matching and identification of brain structures. We quantified the accuracy of the automatic registration using super-resolution vascular images obtained at the microscopic scale using Ultrasound Localization Microscopy and found a positioning error of 44 µm and 96 µm for intra-animal and inter-animals vascular registration, respectively. The proposed BPS approach outperforms the manual vascular landmarks recognition performed by expert neuroscientists (inter-annotator errors of 215 µm and 259 µm). Using the online BPS approach coupled with the Allen Atlas, we demonstrated the capability of the system to position itself automatically over chosen anatomical structures and to obtain corresponding functional activation maps even in complex oblique planes. Finally, we show that the system can be used to acquire and estimate functional connectivity matrices automatically. The proposed functional ultrasound on the fly neuro-navigation approach allows automatic brain navigation and could become a key asset to ensure standardized experiments and protocols for non-expert and expert researchers.

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“…The first application of this so-called functional ultrasound technique brought new insight into the complex subcortical and cortical hemodynamics during epileptiform seizures ( Demene et al, 2017 ). The observed CBV spontaneous oscillations also prove to be different in thalamic and cortical areas between preterm and control term-born neonates ( Baranger et al, 2021 ). Future development of Ultrafast Doppler implies the commercialization of dedicated scanners, as most of the current devices remain research systems.…”

Section: Imaging Techniques To Assess Cbf In Neonates (Graphical Abstract)mentioning

confidence: 93%