No retraction, correction or concern found when last checked on Nov 2, 2026.
Cell-Type-Selective Effects of Intramembrane Cavitation as a Unifying Theoretical Framework for Ultrasonic Neuromodulation
Michael Plaksin, Eitan Kimmel, Shy Shoham
eneuro · 2016 · CC BY-NC-SA
doi:10.1523/eneuro.0136-15.2016
Abstract
Diverse translational and research applications could benefit from the noninvasive ability to reversibly modulate (excite or suppress) CNS activity using ultrasound pulses, however, without clarifying the underlying mechanism, advanced design-based ultrasonic neuromodulation remains elusive. Recently, intramembrane cavitation within the bilayer membrane was proposed to underlie both the biomechanics and the biophysics of acoustic bio-effects, potentially explaining cortical stimulation results through a neuronal intramembrane cavitation excitation (NICE) model. Here, NICE theory is shown to provide a detailed predictive explanation for the ability of ultrasonic (US) pulses to also suppress neural circuits through cell-type-selective mechanisms: according to the predicted mechanism T-type calcium channels boost charge accumulation between short US pulses selectively in low threshold spiking interneurons, promoting net cortical network inhibition. The theoretical results fit and clarify a wide array of earlier empirical observations in both the cortex and thalamus regarding the dependence of ultrasonic neuromodulation outcomes (excitation-suppression) on stimulation and network parameters. These results further support a unifying hypothesis for ultrasonic neuromodulation, highlighting the potential of advanced waveform design for obtaining cell-type-selective network control.
Shown for reading. Its publisher allows quoting it, not republishing it.
References 51
- 1.
Alkire MT, Miller J (2005 ) General anesthesia and the neural correlates of consciousness. Prog Brain Res 150:229-244.
Not in our library10.1016/s0079-6123(05)50017-7
- 2.
Bystritsky A, Korb AS, Douglas PK, Cohen MS, Melega WP, Mulgaonkar AP, DeSalles A, Min BK, Yoo SS (2011 ) A review of low-intensity focused ultrasound pulsation. Brain Stimul. 4:125-136.
Not in our library10.1016/j.brs.2011.03.007
- 3.
Colucci V, Strichartz G, Jolesz F, Vykhodtseva N, Hynynen K (2009 ) Focused ultrasound effects on nerve action potential in vitro. Ultrasound Med Biol 35:1737-1747.
Not in our library10.1016/j.ultrasmedbio.2009.05.002
- 4.
- 5.
Cruikshank SJ, Lewis TJ, Connors BW (2007 ) Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat Neurosci 10:462-468.
Not in our library10.1038/nn1861
- 6.
Deffieux T, Younan Y, Wattiez N, Tanter M, Pouget P, Aubry JF (2013 ) Low-intensity focused ultrasound modulates monkey visuomotor behavior. Curr Biol 23:2430-2433.
Not in our library10.1016/j.cub.2013.10.029
- 7.
Destexhe A, Bal T, McCormick DA, Sejnowski TJ (1996a ) Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. J Neurophysiol 76:2049-2070.
Not in our library10.1152/jn.1996.76.3.2049
- 8.
Destexhe A, Contreras D, Steriade M, Sejnowski TJ, Huguenard JR (1996b ) In vivo, in vitro, and computational analysis of dendritic calcium currents in thalamic reticular neurons. J Neurosci 16:169-185.
Not in our library10.1523/jneurosci.16-01-00169.1996
- 9.
Destexhe A, Contreras D, Steriade M (1998a ) Mechanisms underlying the synchronizing action of corticothalamic feedback through inhibition of thalamic relay cells. J Neurophysiol 79:999-1016.
Not in our library10.1152/jn.1998.79.2.999
- 10.
Destexhe A, Neubig M, Ulrich D, Huguenard J (1998b ) Dendritic low-threshold calcium currents in thalamic relay cells. J Neurosci 18:3574-3588.
Not in our library10.1523/jneurosci.18-10-03574.1998
- 11.
Destexhe A, Paré D (1999 ) Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol 81:1531-1547.
Not in our library10.1152/jn.1999.81.4.1531
- 12.
Gibbins IL, Rodgers HF, Matthew SE, Murphy SM (1998 ) Synaptic organisation of lumbar sympathetic ganglia of guinea pigs: serial section ultrastructural analysis of dye‐filled sympathetic final motor neurons. J Comp Neurol 402:285-302.
Not in our library
- 13.
Hayut I, Fanselow EE, Connors BW, Golomb D (2011 ) LTS and FS inhibitory interneurons, short-term synaptic plasticity, and cortical circuit dynamics. PLoS Comput Biol 7:e1002248.
Not in our library10.1371/journal.pcbi.1002248
- 14.
Hendee WR, Ritenour ER (2002 ) Medical imaging physics, Ed 4 New York, MA: Wiley.
Not in our library
- 15.
Huguenard JR, McCormick DA (1992 ) Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. J Neurophysiol 68:1373-1383.
Not in our library10.1152/jn.1992.68.4.1373
- 16.
Juan EJ, González R, Albors G, Ward MP, Irazoqui P (2014 ) Vagus nerve modulation using focused pulsed ultrasound: potential applications and preliminary observations in a rat. Int J Imaging Syst Technol 24:67-71.
Not in our library10.1002/ima.22080
- 17.
Kim H, Chiu A, Lee SD, Fischer K, Yoo SS (2014 ) Focused ultrasound-mediated non-invasive brain stimulation: examination of sonication parameters. Brain Stimul 7:748-756.
Not in our library10.1016/j.brs.2014.06.011
- 18.
Kim H, Park MY, Lee SD, Lee W, Chiu A, Yoo SS (2015 ) Suppression of EEG visual-evoked potentials in rats through neuromodulatory focused ultrasound. Neuroreport 26:211-215.
Not in our library10.1097/wnr.0000000000000330
- 19.
Kim H, Taghados SJ, Fischer K, Maeng LS, Park S, Yoo, SS (2012 ) Noninvasive transcranial stimulation of rat abducens nerve by focused ultrasound. Ultrasound Med Biol 38:1568-1575.
Not in our library10.1016/j.ultrasmedbio.2012.04.023
- 20.
King RL, Brown JR, Newsome WT, Pauly KB (2013 ) Effective parameters for ultrasound-induced in vivo neurostimulation. Ultrasound Med Biol 39:312-331.
Not in our library10.1016/j.ultrasmedbio.2012.09.009
- 21.
King RL, Brown JR, Pauly KB (2014 ) Localization of ultrasound-induced in vivo neurostimulation in the mouse model. Ultrasound Med Biol 40:1512-1522.
Not in our library10.1016/j.ultrasmedbio.2014.01.020
- 22.
Kleppe IC, Robinson HP (1999 ) Determining the activation time course of synaptic AMPA receptors from openings of colocalized NMDA receptors. Biophys J 77:1418-1427.
Not in our library10.1016/s0006-3495(99)76990-0
- 23.
Krasovitski B, Frenkel V, Shoham S, Kimmel E (2011 ) Intramembrane cavitation as a unifying mechanism for ultrasound-induced bioeffects. Proc Natl Acad Sci U S A 108:3258-3263.
Not in our library10.1073/pnas.1015771108
- 24.
Lee SE, Lee J, Latchoumane C, Lee B, Oh SJ, Saud ZA, Park C, Sun N, Cheong E, Chen CC, Choi EJ, Lee CJ, Shin HS (2014 ). Rebound burst firing in the reticular thalamus is not essential for pharmacological absence seizures in mice. Proc Natl Acad Sci U S A 111:11828-11833.
Not in our library10.1073/pnas.1408609111
- 25.
- 26.
Legon W, Sato TF, Opitz A, Mueller J, Barbour A, Williams A, Tyler WJ (2014 ) Transcranial focused ultrasound modulates the activity of primary somatosensory cortex in humans. Nat Neurosci 17:322-329.
Not in our library10.1038/nn.3620
- 27.
Lele PP (1963 ) Effects of focused ultrasonic radiation on peripheral nerve, with observations on local heating. Exp Neurol 8:47-83.
Not in our library10.1016/0014-4886(63)90008-6
- 28.
Lillemeier BF, Pfeiffer JR, Surviladze Z, Wilson BS, Davis MM (2006 ) Plasma membrane-associated proteins are clustered into islands attached to the cytoskeleton. Proc Natl Acad Sci U S A 103:18992-18997.
Not in our library10.1073/pnas.0609009103
- 29.
Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004 ) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.
Not in our library10.1038/nrn1519
- 30.
Menz MD, Oralkan O, Khuri-Yakub PT, Baccus SA (2013 ) Precise neural stimulation in the retina using focused ultrasound. J Neurosci 33:4550-4560.
Not in our library10.1523/jneurosci.3521-12.2013
- 31.
- 32.
Moore JH, Gieck JH, Saliba EN, Perrin DH, Ball DW, McCue FC (2000 ) The biophysical effects of ultrasound on median nerve distal latencies. Electromyogr Clin Neurophysiol 40:169-180.
Not in our library
- 33.
Naor O, Hertzberg Y, Zemel E, Kimmel E, Shoham S (2012 ) Towards multifocal ultrasonic neural stimulation II: design considerations for an acoustic retinal prosthesis. J Neural Eng 9:026006.
Not in our library10.1088/1741-2560/9/2/026006
- 34.
Naor O, Krupa S, Shoham S (2016 ) Ultrasonic neuromodulation. J Neural Eng 13:031003.
Not in our library10.1088/1741-2560/13/3/031003
- 35.
Nikonenko I, Bancila M, Bloc A, Muller D, Bijlenga P (2005 ) Inhibition of T-type calcium channels protects neurons from delayed ischemia-induced damage. Mol Pharmacol 68:84-89.
Not in our library10.1124/mol.104.010066
- 36.
- 37.
Pospischil M, Rodriguez MT, Monier C, Piwkowska Z, Bal T, Frégnac Y, Markram H, Destexhe A (2008 ) Minimal Hodgkin–Huxley type models for different classes of cortical and thalamic neurons. Biol Cybern 99:427-441.
Not in our library10.1007/s00422-008-0263-8
- 38.
Prieto ML, Oralkan Ö, Khuri-Yakub BT, Maduke MC (2013 ) Dynamic response of model lipid membranes to ultrasonic radiation force PLoS ONE 8:e77115.
Not in our library10.1371/journal.pone.0077115
- 39.
Slaght SJ, Leresche N, Deniau JM, Crunelli V, Charpier S (2002 ) Activity of thalamic reticular neurons during spontaneous genetically determined spike and wave discharges. J Neurosci 22:2323-2334.
Not in our library10.1523/jneurosci.22-06-02323.2002
- 40.
Storozhuk MV, Ivanova SY, Balaban PM, Kostyuk PG (2005 ) Possible role of mitochondria in posttetanic potentiation of GABAergic synaptic transmission in rat neocortical cell cultures. Synapse 58:45-52.
Not in our library10.1002/syn.20186
Cited by papers we hold 6
- Focused ultrasound excites cortical neurons via mechanosensitive calcium accumulation and ion channel amplification · 2022No notice
- Intrinsic functional neuron-type selectivity of transcranial focused ultrasound neuromodulation · 2021No notice
- Systematic examination of low-intensity ultrasound parameters on human motor cortex excitability and behavior · 2020No notice
- A retrospective qualitative report of symptoms and safety from transcranial focused ultrasound for neuromodulation in humans · 2020No notice
- Transcranial focused ultrasound neuromodulation of the human primary motor cortex · 2018No notice
- Effects of transcranial focused ultrasound on human primary motor cortex using 7T fMRI: a pilot study · 2018No notice
Reads
Read by people on this page
None yet.
Checked or read by AI through naulon
None yet.
A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.
Are you an author?
Is this your paper?
Claim it to add your note and be paid when agents cite it. Free.