Skip to main content
Log in

Thermogenetics as a New Direction in Controlling the Activity of Neural Networks

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

Thermogenetics appeared recently as an evolutionary advance in methods of optical stimulation of nerve cells and uses focused light to activate light-sensitive cation channels in the neuron membrane. Light activation and opening of light-sensitive channels, which can be expressed genetically in any type of neuron, induces neuron membrane depolarization and a resultant action potential. In contrast to classical methods of optogenetics, which use the visible spectrum, thermogenetics uses channels sensitive to warming. This provides the opportunity for additional activation of these channels not only using IR light, but also other methods of warming nervous tissue, such as ultrasound or microwave radiation. The penetrability of living tissue to stimulation with IR radiation is an order of magnitude greater than that for visible spectrum radiation, which allows thermogenetics methods to be used in vivo without invasive surgical methods to “clear the way” for optogenetic stimulation. On the other hand, the thermal nature of the stimulation imposes additional limits on use of the method, as heating must be sufficiently gentle so as not to induce heat shock at the cellular level, and the threshold of activation must be sufficiently high for channel opening not to occur spontaneously at normal physiological temperatures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adamantidis, A. R., Zhang, F., de Lecea, L., and Deisseroth, K., “Optogenetics: opsins and optical interfaces in neuroscience,” Cold Spring Harb. Protoc., 2014, 815–822 (2014).

  • Bath, D. E., Stowers, J. R., Hörmann, D., et al., “FlyMAD: rapid thermogenetic control of neuronal activity in freely walking Drosophila,” Nat. Methods, 11, No. 7, 756–762 (2014).

    Article  CAS  Google Scholar 

  • Caterina, M. J., Rosen, T. A., Tominaga, M., et al., “A capsaicin-receptor homologue with a high threshold for noxious heat,” Nature, 398, No. 6726, 436–441 (1999).

    Article  CAS  Google Scholar 

  • Chen, R., Romero, G., Christiansen, M. G., et al., “Wireless magnetothermal deep brain stimulation,” Science, 347, No. 6229, 1477–1480 (2015).

    Article  CAS  Google Scholar 

  • Chen, S. et al., “TRP channel mediated neuronal activation and ablation in freely behaving zebrafish,” Nat. Methods, 13, No. 2, 147–150 (2016).

    Article  Google Scholar 

  • Chugunov, A. O., Volynsky, P. E., Krylov, N. A., et al., “Temperaturesensitive gating of TRPV1 channel as probed by atomistic simulations of its trans- and juxtamembrane domains,” Sci. Rep., 6, 33112 (2016).

    Article  CAS  Google Scholar 

  • Cordero-Morales, J. F., Gracheva, E. O., and Julius, D., “Cytoplasmic ankyrin repeats of transient receptor potential A1 (TRPA1) dictate sensitivity to thermal and chemical stimuli,” Proc. Natl. Acad. Sci. USA, 108, No. 46, E1184–E1191 (2011).

    Article  CAS  Google Scholar 

  • DeBow, S. and Colbourne, F., “Brain temperature measurement and regulation in awake and freely moving rodents,” Methods, 30, No. 2003, 167–171.

    Article  CAS  Google Scholar 

  • Ermakova, Y. G., Lanin, A. A., Fedotov, I. V., et al., “Thermogenetic neurostimulation with single-cell resolution,” Nat. Commun., 8, 15362 (2017).

    Article  CAS  Google Scholar 

  • Fedotov, I. V., Safronov, N. A., Ermakova, Y. G., et al., “Fiber-optic control and thermometry of single-cell thermosensation logic,” Sci. Rep., 5, 15737 (2015).

    Article  CAS  Google Scholar 

  • Gau, P., Poon, J., Ufret-Vincenty, C., et al., “The zebrafish ortholog of TRPV1 is required for heat-induced locomotion,” J. Neurosci., 33, No. 12, 5249–5260 (2013).

    Article  CAS  Google Scholar 

  • Gracheva, E. O., Cordero-Morales, J. F., González-Carcacía, J. A., et al., “Ganglion-specific splicing of TRPV1 underlies infrared sensation in vampire bats,” Nature, 476, No. 7358, 88–91 (2011).

    Article  CAS  Google Scholar 

  • Gracheva, E. O., Ingolia, N. T., Kelly, Y. M., et al., “Molecular basis of infrared detection by snakes,” Nature, 464, No. 7291, 1006–1011 (2010).

    Article  CAS  Google Scholar 

  • Hamada, F. N., Rosenzweig, M., Kang, K., et al., “An internal thermal sensor controlling temperature preference in Drosophila,” Nature, 454, 217–220 (2008).

    Article  CAS  Google Scholar 

  • Ibsen, S., Tong, A., Schutt, C., et al., “Sonogenetics is a non-invasive approach to activating neurons in Caenorhabditis elegans,” Nat. Commun., 6, 8264 (2015).

    Article  CAS  Google Scholar 

  • Kohatsu, S., Koganezawa, M., and Yamamoto, D., “Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila,” Neuron, 69, No. 3, 498–508 (2011).

    Article  CAS  Google Scholar 

  • Lanin, A. A., Fedotov, I. V., Ermakova Yu, G., et al., “Fiber-optic electron-spin-resonance thermometry of single laser-activated neurons,” Opt. Lett., 41, No. 23, 5563–5566 (2016a).

    Article  CAS  Google Scholar 

  • Lanin, A. A., Stepanov, E. A., Tikhonov, R. A., et al., “A compact laser platform for nonlinear Raman microspectroscopy: multimodality through broad chirp tunability,” J. Raman Spectrosc., 47, 1042–1048 (2016b).

    Article  CAS  Google Scholar 

  • Liao, M., Cao, E., Julius, D., and Cheng, Y., “Structure of the TRPV1 ion channel determined by electron cryo-microscopy,” Nature, 504, No. 7478, 107–112 (2013).

    Article  CAS  Google Scholar 

  • Liu, X., Ramirez, S., Pang, P. T., et al., “Optogenetic stimulation of a hippocampal engram activates fear memory recall,” Nature, 484, 381–385 (2012).

    Article  CAS  Google Scholar 

  • Mishra, A., Salari, A., Berigan, B. R., et al., “The Drosophila Gr28bD product is a non-specific cation channel that can be used as a novel thermogenetic tool,” Sci. Rep., 8, No. 1, 901 (2018).

    Article  Google Scholar 

  • Nikitin, E. S., Roshchin, M. V., Ierusalimskii, V. N., et al., “Optogenetic stimulation of pyramidal neuron axons in the visual cortex and hippocampus in living brain slices,” Zh. Vyssh. Nerv. Deyat., 67, No. 5, 101–108 (2017).

    Google Scholar 

  • Oda, M., Kurogi, M., Kubo, Y., and Saitoh, O., “Sensitivities of two zebrafish TRPA1 paralogs to chemical and thermal stimuli analyzed in heterologous expression systems,” Chem. Senses, 41, No. 3, 261–272 (2016).

    Article  CAS  Google Scholar 

  • Paulsen, C. E., Armache, J. P., Gao, Y., et al., “Structure of the TRPA1 ion channel suggests regulatory mechanisms,” Nature, 525, No. 7570, 552 (2015a).

    Article  CAS  Google Scholar 

  • Paulsen, C. E., Armache, J. P., Gao, Y., et al., “Structure of the TRPA1 ion channel suggests regulatory mechanisms,” Nature, 520, No. 7548, 511–517 (2015b).

    Article  CAS  Google Scholar 

  • Prakash, R., Yizhar, O., Grewe, B., et al., “Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation,” Nat. Methods, 9, 1171–1179 (2012).

    Article  CAS  Google Scholar 

  • Pulver, S. R., Pashkovski, S. L., Hornstein, N. J., et al., “Temporal dynamics of neuronal activation by channelrhodopsin-2 and TRPA1 determine behavioral output in Drosophila larvae,” J. Neurophysiol., 101, No. 6, 3075–3788 (2009).

    Article  Google Scholar 

  • Richter, C. P. and Tan, X., “Photons and neurons,” Hear. Res., 311, 72–88 (2014).

    Article  Google Scholar 

  • Roshchin, M., Ermakova, Y. G., Lanin, A. A., et al., “Thermogenetic stimulation of single neocortical pyramidal neurons transfected with TRPV1-L channels,” Neurosci. Lett., 687, 153–157 (2018).

    Article  CAS  Google Scholar 

  • Safronov, N. A., Fedotov, I. V., Ermakova Yu, G., et al., “Microwaveinduced thermogenetic activation of single cells,” Appl. Phys. Letts., 106, No. 16, 163702 (2015).

    Article  Google Scholar 

  • Stanley, S. A., Gagner, J. E., Damanpour, S., et al., “Radio-wave heating of iron oxide nanoparticles can regulate plasma glucose in mice,” Science, 336, No. 6081, 604–608 (2012).

    Article  CAS  Google Scholar 

  • Takahashi, N. and Mori, Y., “TRP channels as sensors and signal integrators of redox status changes,” Front. Pharmacol., 2, 58 (2011).

  • Tseeb, V., Suzuki, M., Oyama, K., et al., “Highly thermosensitive Ca dynamics in a HeLa cell through IP(3) receptors,” HFSP J, 3, No. 2, 117–123 (2009).

    Article  CAS  Google Scholar 

  • Voronin, A. A. and Zheltikov, A. M., “Ionization penalty in nonlinear optical bioimaging,” Phys. Rev. E Stat. Nonlin. Soft. Matter. Phys, 81, No. 5, Pt 1, 051918 (2010).

  • Wang, Y. Y., Chang, R. B., Waters, H. N., et al., “The nociceptor ion channel TRPA1 is potentiated and inactivated by permeating calcium ions,” J. Biol. Chem., 283, No. 47, 32691–32703 (2008).

    Article  CAS  Google Scholar 

  • Wetsel, W. C., “Sensing hot and cold with TRP channels,” Int. J. Hyperthermia, 27, No. 4, 388–398 (2011).

    Article  CAS  Google Scholar 

  • Yang, F. and Zheng, J., “High temperature sensitivity is intrinsic to voltage-gated potassium channels,” eLife, 3, e03255 (2014).

    Article  Google Scholar 

  • Yao, J., Liu, B., and Qin, F., “Rapid temperature jump by infrared diode laser irradiation for patch-clamp studies,” Biophys. J., 96, 3611–3619 (2009).

    Article  CAS  Google Scholar 

  • Yarmolenko, P. S., Moon, E. J., Landon, C., et al., “Thresholds for thermal damage to normal tissues: An update,” Int. J. Hyperthermia, 27, 320–343 (2011).

    Article  Google Scholar 

  • Yizhar, O. et al., “Optogenetics in neural systems,” Neuron, 71, No. 1, 9–34 (2011).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. S. Nikitin.

Additional information

Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 70, No. 1, pp. 133–140, January–February, 2020.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ermakova, Y.G., Roshchin, M.V., Lanin, A.A. et al. Thermogenetics as a New Direction in Controlling the Activity of Neural Networks. Neurosci Behav Physi 50, 1018–1023 (2020). https://doi.org/10.1007/s11055-020-01001-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-020-01001-1

Keywords

Navigation