Non-genetic photoacoustic stimulation of single neurons by a tapered fiber optoacoustic emitter

Linli Shi; Ying Jiang; Fernando R. Fernandez; Guo Chen; Lu Lan; Heng-Ye Man; John A. White; Ji-Xin Cheng; Chen Yang

doi:10.1038/s41377-021-00580-z

Go to Nature Website

Your Location：

Home >

Browse articles >

Non-genetic photoacoustic stimulation of single neurons by a tapered fiber optoacoustic emitter

Articles

- Non-genetic photoacoustic stimulation of single neurons by a tapered fiber optoacoustic emitter
- Non-genetic photoacoustic stimulation of single neurons by a tapered fiber optoacoustic emitter
- LSA 2021年10卷第8期页码：1494-1506
- Affiliations：
  
  1.Department of Chemistry, Boston University, 580 Commonwealth Avenue, Boston, MA, 02215, USA
  2.Department of Biomedical Engineering, Boston University, 44 Cummington Mall, Boston, MA, 02215, USA
  3.Center for Systems Neuroscience, Boston University, 610 Commonwealth Ave, Boston, MA, 02215, USA
  4.Neurophotonics Center, Photonics Center, Boston University, 8 St. Mary's Street, Boston, MA, 02215, USA
  5.Department of Electrical and Computer Engineering, 8 St. Mary's Street, Boston, MA, 02215, USA
  6.Department of Biology, Boston University, 5 Cummington Mall, Boston, MA, 02215, USA
- Author bio：
  
  Ji-Xin Cheng (jxcheng@bu.edu)
  Chen Yang(cheyang@bu.edu)
- Funds：
- DOI：10.1038/s41377-021-00580-z
  中图分类号：
- 纸质出版日期：2021-08-31，
  
  网络出版日期：2021-07-14，
  
  收稿日期：2021-02-03，
  
  修回日期：2021-06-09，
  
  录用日期：2021-06-21
- Accepted：
Scan QR Code
Non-genetic photoacoustic stimulation of single neurons by a tapered fiber optoacoustic emitter[J]. LSA, 2021,10(8):1494-1506.

Shi, L. L. et al. Non-genetic photoacoustic stimulation of single neurons by a tapered fiber optoacoustic emitter. Light: Science & Applications, 10, 1494-1506 (2021).
Non-genetic photoacoustic stimulation of single neurons by a tapered fiber optoacoustic emitter[J]. LSA, 2021,10(8):1494-1506. DOI： 10.1038/s41377-021-00580-z.

Shi, L. L. et al. Non-genetic photoacoustic stimulation of single neurons by a tapered fiber optoacoustic emitter. Light: Science & Applications, 10, 1494-1506 (2021). DOI： 10.1038/s41377-021-00580-z.

摘要

Abstract

Neuromodulation at high spatial resolution poses great significance in advancing fundamental knowledge in the field of neuroscience and offering novel clinical treatments. Here

we developed a tapered fiber optoacoustic emitter (TFOE) generating an ultrasound field with a high spatial precision of 39.6 µm

enabling optoacoustic activation of single neurons or subcellular structures

such as axons and dendrites. Temporally

a single acoustic pulse of sub-microsecond converted by the TFOE from a single laser pulse of 3 ns is shown as the shortest acoustic stimuli so far for successful neuron activation. The precise ultrasound generated by the TFOE enabled the integration of the optoacoustic stimulation with highly stable patch-clamp recording on single neurons. Direct measurements of the electrical response of single neurons to acoustic stimulation

which is difficult for conventional ultrasound stimulation

have been demonstrated. By coupling TFOE with ex vivo brain slice electrophysiology

we unveil cell-type-specific responses of excitatory and inhibitory neurons to acoustic stimulation. These results demonstrate that TFOE is a non-genetic single-cell and sub-cellular modulation technology

which could shed new insights into the mechanism of ultrasound neurostimulation.

关键词

Keywords

references

Houweling, A. R.&Brecht, M. Behavioural report of single neuron stimulation in somatosensory cortex.Nature451, 65–68 (2008)..

Li, C. -Y. T., Poo, M. -m.&Dan, Y. Burst spiking of a single cortical neuron modifies global brain state.Science324, 643–646 (2009)..

Rizzo, J. F. III Update on retinal prosthetic research: the Boston Retinal Implant Project.J. Neuro-Ophthalmol.31, 160–168 (2011)..

Palanker, D. et al. Design of a high-resolution optoelectronic retinal prosthesis.J. Neural Eng.2, S105 (2005)..

Grunt, S., Becher, J. G.&Vermeulen, R. J. Long‐term outcome and adverse effects of selective dorsal rhizotomy in children with cerebral palsy: a systematic review.Dev. Med. Child Neurol.53, 490–498 (2011)..

Boon, P. et al. Deep brain stimulation in patients with refractory temporal lobe epilepsy.Epilepsia48, 1551–1560 (2007)..

Mayberg, H. S. et al. Deep brain stimulation for treatment-resistant depression.Neuron45, 651–660 (2005)..

Rosin, B. et al. Closed-loop deep brain stimulation is superior in ameliorating parkinsonism.Neuron72, 370–384 (2011)..

Ineichen, C., Shepherd, N. R.&Sürücü, O. Understanding the effects and adverse reactions of deep brain stimulation: is it time for a paradigm shift toward a focus on heterogenous biophysical tissue properties instead of electrode design only?Front. Hum. Neurosci.12, 468 (2018)..

Boyden, E. S. et al. Millisecond-timescale, genetically targeted optical control of neural activity.Nat. Neurosci.8, 1263–1268 (2005)..

Kim, C. K., Adhikari, A.&Deisseroth, K. Integration of optogenetics with complementary methodologies in systems neuroscience.Nat. Rev. Neurosci.18, 222–235 (2017)..

Wells, J. et al. Optical stimulation of neural tissue in vivo.Opt. Lett.30, 504–506 (2005)..

Wells, J. et al. Biophysical mechanisms of transient optical stimulation of peripheral nerve.Biophys. J.93, 2567–2580 (2007)..

Izzo, A. D. et al. Laser stimulation of the auditory nerve.Lasers Surg. Med.38, 745–753 (2006)..

Cayce, J. M. et al. Infrared neural stimulation of primary visual cortexin non-human primates.Neuroimage84, 181–190 (2014)..

Cayce, J. M. et al. Infrared neural stimulation of human spinal nerve roots in vivo.Neurophotonics2, 015007 (2015)..

Xu, A. G. et al. Focal infrared neural stimulation with high-field functional MRI: a rapid way to map mesoscale brain connectomes.Sci. Adv.5, eaau7046 (2019)..

Chernov, M. M., Chen, G.&Roe, A. W. Histological assessment of thermal damage in the brain following infrared neural stimulation.Brain Stimulation7, 476–482 (2014)..

Legon, W. et al. Transcranial focused ultrasound modulates the activity of primary somatosensory cortex in humans.Nat. Neurosci.17, 322–329 (2014)..

Tufail, Y. et al. Ultrasonic neuromodulation by brain stimulation with transcranial ultrasound.Nat. Protoc.6, 1453–1470 (2011)..

Blackmore, J. et al. Ultrasound neuromodulation: a review of results, mechanisms and safety.Ultrasound Med. Biol.45, 1509–1536 (2019)..

Naor, O., Krupa, S.&Shoham, S. Ultrasonic neuromodulation.J. Neural Eng.13, 031003 (2016)..

Tyler, W. J. et al. Remote excitation of neuronal circuits using low-intensity, low-frequency ultrasound.PLoS ONE3, e3511 (2008)..

Kodandaramaiah, S. B. et al. Automated whole-cell patch-clamp electrophysiology of neurons in vivo.Nat. Methods9, 585–587 (2012)..

Wang, L. V.&Hu, S. Photoacoustic tomography: in vivo imaging from organelles to organs.Science335, 1458–1462 (2012)..

Jiang, Y. et al. Optoacoustic brain stimulation at submillimeter spatial precision.Nat. Commun.11, 881 (2020)..

Shi, L. et al. A fiber optoacoustic emitter with controlled ultrasound frequency for cell membrane sonoporation at submillimeter spatial resolution.Photoacoustics20, 100208 (2020)..

Noimark, S. et al. Polydimethylsiloxane composites for optical ultrasound generation and multimodality imaging.Adv. Funct. Mater.28, 1704919 (2018)..

Noimark, S. et al. Carbon‐nanotube–PDMS composite coatings on optical fibers for all‐optical ultrasound imaging.Adv. Funct. Mater.26, 8390–8396 (2016)..

Poduval, R. K. et al. Optical fiber ultrasound transmitter with electrospun carbon nanotube-polymer composite.Appl. Phys. Lett.110, 223701 (2017)..

Lyu, Y. et al. Semiconducting polymer nanobioconjugates for targeted photothermal activation of neurons.J. Am. Chem. Soc.138, 9049–9052 (2016)..

Shapiro, M. G. et al. Infrared light excites cells by changing their electrical capacitance.Nat. Commun.3, 736 (2012)..

Cohen, J. E.&Fields, R. D. Extracellular calcium depletion in synaptic transmission.Neuroscientist10, 12–17 (2004)..

Asteriti, S., Liu, C. -H.&Hardie, R. C. Calcium signalling inDrosophilaphotoreceptors measured with GCaMP6f.Cell Calcium65, 40–51 (2017)..

Ha, G. E.&Cheong, E. Spike frequency adaptation in neurons of the central nervous system.Exp. Neurobiol.26, 179–185 (2017)..

Lin, C. -R. et al. Sonoporation-mediated gene transfer into adult rat dorsal root ganglion cells.J. Biomed. Sci.17, 44 (2010)..

Shemesh, O. A. et al. Temporally precise single-cell-resolution optogenetics.Nat. Neurosci.20, 1796–1806 (2017)..

Tufail, Y. et al. Transcranial pulsed ultrasound stimulates intact brain circuits.Neuron66, 681–694 (2010)..

Mehić, E. et al. Increased anatomical specificity of neuromodulation via modulated focused ultrasound.PLoS ONE9, e86939 (2014)..

Dana, H. et al. High-performance GFP-based calcium indicators for imaging activity in neuronal populations and microcompartments.Nat. Methods16, 649–657 (2018)..

King, R. L. et al. Effective parameters for ultrasound-induced in vivo neurostimulation.Ultrasound Med. Biol.39, 312–331 (2013)..

Mihran, R. T., Barnes, F. S.&Wachtel, H. Temporally-specific modification of myelinated axon excitability in vitro following a single ultrasound pulse.Ultrasound Med. Biol.16, 297–309 (1990)..

Nakamura, T. et al. Synergistic release of Ca2+ from IP3-sensitive stores evoked by synaptic activation of mGluRs paired with backpropagating action potentials.Neuron24, 727–737 (1999)..

Micheva, K. D. et al. A large fraction of neocortical myelin ensheathes axons of local inhibitory neurons.Elife5, e15784 (2016)..

Kubanek, J. Neuromodulation with transcranial focused ultrasound.Neurosurgical Focus44, E14 (2018)..

Tyler, W. J. Noninvasive neuromodulation with ultrasound? A continuum mechanics hypothesis.Neuroscientist17, 25–36 (2011)..

Deffieux, T. et al. Low-intensity focused ultrasound modulates monkey visuomotor behavior.Curr. Biol.23, 2430–2433 (2013)..

Mahmud, M.&Vassanelli, S. Differential modulation of excitatory and inhibitory neurons during periodic stimulation.Front. Neurosci.10, 62 (2016)..

Prestigio, C. et al. Spike-related electrophysiological identification of cultured hippocampal excitatory and inhibitory neurons.Molecular Neurobiology56, 6276–6292 (2019)..

Kubanek, J. et al. Ultrasound modulates ion channel currents.Sci. Rep.6, 1–14 (2016)..

Kubanek, J., Shukla, P., Das, A., Baccus, S. A.&Goodman, M. B. Ultrasound elicits behavioral responses through mechanical effects on neurons and ion channels in a simple nervous system.J. Neurosci.38, 3081–3091 (2018)..

Yoo, S., Mittelstein, D. R., Hurt, R. C., Lacroix, J. J.&Shapiro, M. G. Focused ultrasound excites neurons via mechanosensitive calcium accumulation and ion channel amplification. Preprint athttps://www.biorxiv.org/content/10.1101/2020.05.19.101196v1https://www.biorxiv.org/content/10.1101/2020.05.19.101196v1(2020).

Ye, J. et al. Ultrasonic control of neural activity through activation of the mechanosensitive channel MscL.Nano Lett.18, 4148–4155 (2018)..

Krasovitski, B., Frenkel, V., Shoham, S.&Kimmel, E. Intramembrane cavitation as a unifying mechanism for ultrasound-induced bioeffects.Proc. Natl Acad. Sci. USA108, 3258–3263 (2011)..

Plaksin, M., Shoham, S.&Kimmel, E. Intramembrane cavitation as a predictive bio-piezoelectric mechanism for ultrasonic brain stimulation.Phys. Rev. X4, 011004 (2014)..

Gaub, B. M. et al. Neurons differentiate magnitude and location of mechanical stimuli.Proc. Natl Acad. Sci. USA117, 848–856 (2020)..

Liu, Y., Zhou, X., Ma, J., Ge, Y.&Cao, X. The diameters and number of nerve fibers in spinal nerve roots.J. Spinal Cord. Med.38, 532–537 (2015)..

Chen, Y. et al. MRI-guided robotic arm drives optogenetic fMRI with concurrent Ca 2+ recording.Nat. Commun.10, 2536 (2019)..

Fernandez, F. R., Rahsepar, B.&White, J. A. Differences in the electrophysiological properties of mouse somatosensory layer 2/3 neurons in vivo and slice stem from intrinsic sources rather than a network-generated high conductance state.Eneuro5, 2 (2018)..

浏览量

Downloads

CSCD

文章被引用时，请邮件提醒。

Submit

工具集

关联资源

暂无数据