3D Functional Ultrasound Imaging of Pigeons

Recent advances in ultrasound Doppler imaging have allowed to visualize brain activity in small mammalian species such as rats and mice. In birds, this type of functional ultrasound imaging was impossible up to now because birds have physiological characteristics that are unfavorable for current functional ultrasound acquisition schemes. Here, we introduce a high-definition functional ultrasound acquisition method (HDfUS) acquiring 20,000 frames per second continuously. This enabled first successful functional studies on awake pigeons subjected to auditory and visual stimulation. We show that the improved spatiotemporal resolution and sensitivity of HDfUS allows to visualize and investigate the temporally resolved 3D neural activity evoked by a complex stimulation pattern, such as a moving light source. This illustrates the enormous potential of HDfUS imaging to become a new standard functional brain imaging method revealing unknown, stimulus related hemodynamics at excellent signal-to-noise ratio and spatiotemporal resolution. Highlights - We describe a novel ultrafast functional ultrasound technique (HDfUS) - HDfUS offers continuous recording with unmatched spatiotemporal resolution - HDfUS allows to resolve complex 4D neurovascular responses in the brain - First fUS study on non-mammalian species

[1]  J. Polzehl,et al.  Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography , 2007, Proceedings of the National Academy of Sciences.

[2]  M. Manns,et al.  The impact of asymmetrical light input on cerebral hemispheric specialization and interhemispheric cooperation , 2012, Nature Communications.

[3]  Mickael Tanter,et al.  Ultrafast imaging in biomedical ultrasound , 2014, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[4]  N. de Jong,et al.  Plane-wave ultrasound beamforming using a nonuniform fast fourier transform , 2012, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[5]  O. Güntürkün,et al.  A 3-dimensional digital atlas of the ascending sensory and the descending motor systems in the pigeon brain , 2012, Brain Structure and Function.

[6]  J Bercoff,et al.  Ultrafast compound doppler imaging: providing full blood flow characterization , 2011, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[7]  Michael Colombo,et al.  Delay activity in avian prefrontal cortex – sample code or reward code? , 2011, The European journal of neuroscience.

[8]  J. Bolhuis,et al.  Localized neuronal activation in the zebra finch brain is related to the strength of song learning. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Thomas Deffieux,et al.  3D functional ultrasound imaging of the cerebral visual system in rodents , 2017, NeuroImage.

[10]  N. Logothetis.  What we can do and what we cannot do with fMRI , 2008, Nature.

[11]  H. Karten,et al.  A stereotaxic atlas of the brain of the pigeon (Columba livia) , 1967 .

[12]  Elodie Tiran,et al.  Transcranial Functional Ultrasound Imaging in Freely Moving Awake Mice and Anesthetized Young Rats without Contrast Agent , 2017, Ultrasound in medicine & biology.

[13]  G. Montaldo,et al.  Real-time imaging of brain activity in freely moving rats using functional ultrasound , 2015, Nature Methods.

[14]  Mark A. Suckow,et al.  The Laboratory Mouse , 2000 .

[15]  O. Güntürkün,et al.  Asymmetry pays: visual lateralization improves discrimination success in pigeons , 2000, Current Biology.

[16]  Elodie Tiran,et al.  EEG and functional ultrasound imaging in mobile rats , 2015, Nature Methods.

[17]  John M. Reid,et al.  Scattering of Ultrasound by Blood , 1976, IEEE Transactions on Biomedical Engineering.

[18]  Conny Gunkel,et al.  Current Techniques in Avian Anesthesia , 2005 .

[19]  M. Fee,et al.  A role for descending auditory cortical projections in songbird vocal learning , 2014, eLife.

[20]  L. Boorman,et al.  Comparison of stimulus-evoked cerebral hemodynamics in the awake mouse and under a novel anesthetic regime , 2015, Scientific reports.

[21]  Annemie Van der Linden,et al.  Current state-of-the-art of auditory functional MRI (fMRI) on zebra finches: Technique and scientific achievements , 2013, Journal of Physiology-Paris.

[22]  Jack A. Wells,et al.  fMRI mapping of the visual system in the mouse brain with interleaved snapshot GE-EPI , 2016, NeuroImage.

[23]  M. Fink,et al.  Coherent plane-wave compounding for very high frame rate ultrasonography and transient elastography , 2009, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[24]  Charlie Demené,et al.  4D microvascular imaging based on ultrafast Doppler tomography , 2016, NeuroImage.

[25]  Charlie Demené,et al.  Spatiotemporal Clutter Filtering of Ultrafast Ultrasound Data Highly Increases Doppler and fUltrasound Sensitivity , 2015, IEEE Transactions on Medical Imaging.

[26]  P. Kuhl,et al.  Birdsong and human speech: common themes and mechanisms. , 1999, Annual review of neuroscience.

[27]  Juan Esteban Arango,et al.  3D ultrafast ultrasound imaging in vivo , 2014, Physics in medicine and biology.

[28]  M. Fink,et al.  Functional ultrasound imaging of the brain , 2011, Nature Methods.

[29]  Johan J. Bolhuis,et al.  Neural mechanisms of birdsong memory , 2006, Nature Reviews Neuroscience.

[30]  Jean Rossier,et al.  Chronic assessment of cerebral hemodynamics during rat forepaw electrical stimulation using functional ultrasound imaging , 2014, NeuroImage.

[31]  M. Fink,et al.  Functional ultrasound imaging of the brain: theory and basic principles , 2013, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[32]  J. Jensen.  Estimation of Blood Velocities Using Ultrasound: A Signal Processing Approach , 1996 .

[33]  Dirk Jancke,et al.  Dominant Vertical Orientation Processing without Clustered Maps: Early Visual Brain Dynamics Imaged with Voltage-Sensitive Dye in the Pigeon Visual Wulst , 2010, The Journal of Neuroscience.

[34]  E. Jarvis,et al.  Learned Birdsong and the Neurobiology of Human Language , 2004, Annals of the New York Academy of Sciences.

[35]  M. Tanter,et al.  Light controls cerebral blood flow in naive animals , 2017, Nature Communications.

[36]  O. Güntürkün,et al.  Asymmetric top-down modulation of ascending visual pathways in pigeons , 2016, Neuropsychologia.

[37]  Philip Kollmannsberger,et al.  Architecture of the osteocyte network correlates with bone material quality , 2013, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[38]  Mickael Tanter,et al.  Functional ultrasound imaging of intrinsic connectivity in the living rat brain with high spatiotemporal resolution , 2014, Nature Communications.

[39]  M. Tanter,et al.  Functional ultrasound imaging of brain activity in human newborns , 2017, Science Translational Medicine.

[40]  M. Jung-Beeman.  Bilateral brain processes for comprehending natural language , 2005, Trends in Cognitive Sciences.

[41]  P. Kuhl.  Early language acquisition: cracking the speech code , 2004, Nature Reviews Neuroscience.