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Analysis of temporal firing patterns of primary afferent C-fibers for different sensations in mice

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Abstract

Some people with amputated limbs can benefit from neural prosthetics to restore tactile sensation through electrical stimulation of the afferent nerve. The temporal spike train pattern generated in healthy subject’s nerve by various types of somatosensation could provide key information to closely mimic natural sensations using electrical stimulation. However, the temporal firing patterns of peripheral sensory fibers have not been well understood yet. To interpret somatosensory spike trains, we performed ex vivo singlefiber recordings from the saphenous nerve in isolated skin-nerve preparations from mice. Some mechanically sensitive primary afferent C-fibers could also be activated by hot, cold, and itching stimuli, and we observed stimulus-specific firing patterns. These temporal patterns of the C-fibers for chemical stimuli were analyzed using a computational model based on quadruplets of spikes, which we classified into three groups of responses, i.e., capsaicin (hot), allyl-isothiocyanate (cold), and α-methyl-serotonin (itching). Each group of responses to the chemical stimuli was different from that evoked by mechanical stimuli. Therefore, these findings indicate that nontactile somatosensation can be decoded and used as input to a computerized system. Our quadruplet approach to the temporal patterns of spike trains contributes valuable insight to the identification of temporal profiles of other biological conditions.

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References

  1. Sul, O., Chun, H., Choi, E., Choi, J., Cho, K., et al., “Touch Stimulated Pulse Generation in Biomimetic Single-Layer Graphene,” Nanoscale, Vol. 8, No. 6, pp. 3425–3431, 2016.

    Article  Google Scholar 

  2. Tabot, G. A., Dammann, J. F., Berg, J. A., Tenore, F. V., Boback, J. L.,et al., “Restoring the Sense of Touch with a Prosthetic Hand through a Brain Interface,” Proceedings of the National Academy of Sciences, Vol. 110, No. 45, pp. 18279–18284, 2013.

    Article  Google Scholar 

  3. Tan, D. W., Schiefer, M. A., Keith, M. W., Anderson, J. R., Tyler, J., and Tyler, D. J., “A Neural Interface Provides Long-Term Stable Natural Touch Perception,” Science Translational Medicine, Vol. 6, No. 257, pp. 257ra138, 2014.

    Article  Google Scholar 

  4. Oddo, C. M., Raspopovic, S., Artoni, F., Mazzoni, A., Spigler, G., et al., “Intraneural Stimulation Elicits Discrimination of Textural Features by Artificial Fingertip in Intact and Amputee Humans,” Elife, Vol. 5, Paper No. e09148, 2016.

    Article  Google Scholar 

  5. Raspopovic, S., Capogrosso, M., Petrini, F. M., Bonizzato, M., Rigosa, J., et al., “Restoring Natural Sensory Feedback in Real-Time Bidirectional Hand Prostheses,” Science Translational Medicine, Vol. 6, No. 222, pp. 222ra219, 2014.

    Article  Google Scholar 

  6. Rongala, U. B., Mazzoni, A., and Oddo, C. M., “Neuromorphic Artificial Touch for Categorization of Naturalistic Textures,” IEEE Transactions on Neural Networks and Learning Systems, Vol. 28, No. 4, pp. 819–829, 2015.

    Article  Google Scholar 

  7. Martín-Alguacil, N., de Gaspar, I., Schober, J. M., and Pfaff, D. W., “Somatosensation: End Organs for Tactile Sensation,” in: Neuroscience in the 21st Century, Pfaff, D. W., (Ed.), Springer, pp. 743–780, 2013.

    Chapter  Google Scholar 

  8. Aubdool, A. A., Graepel, R., Kodji, X., Alawi, K. M., Bodkin, J. V., et al., “TRPA1 is Essential for the Vascular Response to Environmental Cold Exposure,” Nature Communications, Vol. 5, Article No. 5732, 2014.

  9. Lee, S. H., “Molecular Mechanism of Serotonin-Induced Itch in Mice,” Ph.D. Thesis, Hanyang University, 2015.

    Google Scholar 

  10. Benham, C. D., Gunthorpe, M. J., and Davis, J. B., “TRPV Channels as Temperature Sensors,” Cell Calcium, Vol. 33, Nos. 5-6, pp. 479–487, 2003.

    Article  Google Scholar 

  11. Hachisuka, J., Furue, H., Furue, M., and Yoshimura, M., “Responsiveness of C Neurons in Rat Dorsal Root Ganglion to 5-Hydroxytryptamine-Induced Pruritic Stimuli in Vivo,” Journal of Neurophysiology, Vol. 104, No. 1, pp. 271–279, 2010.

    Article  Google Scholar 

  12. Pierre, M. S., Reeh, P. W., and Zimmermann, K., “Differential Effects of TRPV Channel Block on Polymodal Activation of Rat Cutaneous Nociceptors in Vitro,” Experimental Brain Research, Vol. 196, No. 1, pp. 31–44, 2009.

    Article  Google Scholar 

  13. Zimmermann, K., Hein, A., Hager, U., Kaczmarek, J. S., Turnquist, B.P., Clapham, D. E., and Reeh, P.W., “Phenotyping Sensory Nerve Endings in Vitro in the Mouse,” Nature Protocols, Vol. 4, No. 2, pp. 174–196, 2009.

    Article  Google Scholar 

  14. Yamaguchi, T., Nagasawa, T., Satoh, M., and Kuraishi, Y., “Itch-Associated Response Induced by Intradermal Serotonin through 5-HT2 Receptors in Mice,” Neuroscience Research, Vol. 35, No. 2, pp. 77–83, 1999.

    Article  Google Scholar 

  15. Moparthi, L., Survery, S., Kreir, M., Simonsen, C., Kjellbom, P., et al., “Human TRPA1 is Intrinsically Cold-and Chemosensitive with and Without Its N-Terminal Ankyrin Repeat Domain,” Proceedings of the National Academy of Sciences, Vol. 111, No. 47, pp. 16901–16906, 2014.

    Article  Google Scholar 

  16. Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D., and Julius, D., “The Capsaicin Receptor: A Heat-Activated Ion Channel in the Pain Pathway,” Nature, Vol. 389, No. 6653, pp. 816–824, 1997.

    Article  Google Scholar 

  17. Zhao, M., Isami, K., Nakamura, S., Shirakawa, H., Nakagawa, T., and Kaneko, S., “Acute Cold Hypersensitivity Characteristically Induced by Oxaliplatin is Caused by the Enhanced Responsiveness of TRPA1 in Mice,” Molecular Pain, Vol. 8, No. 1, Paper No. 55, 2012.

    Google Scholar 

  18. De Col, R., Messlinger, K., and Carr, R. W., “Repetitive Activity Slows Axonal Conduction Velocity and Concomitantly Increases Mechanical Activation Threshold in Single Axons of the Rat Cranial Dura,” The Journal of Physiology, Vol. 590, No. 4, pp. 725–736, 2012.

    Article  Google Scholar 

  19. Gerstner, W., Kistler, W. M., Naud, R., and Paninski, L., “Neuronal Dynamics: From Single Neurons to Networks and Models of Cognition,” Cambridge University Press, 2014.

    Book  Google Scholar 

  20. Cover, T. and Hart, P., “Nearest Neighbor Pattern Classification,” IEEE Transactions on Information Theory, Vol. 13, No. 1, pp. 21–27, 1967.

    Article  MATH  Google Scholar 

  21. Györfi, L., Devroye, L., and Lugosi, G., “A Probabilistic Theory of Pattern Recognition,” Springer-Verlag, 1996.

    MATH  Google Scholar 

  22. Grigg, P., Robichaud, D. R., and Bove, G. M., “A Feedback-Controlled Dynamic Linear Actuator to Test Foot Withdrawal Thresholds in Rat,” Journal of Neuroscience Methods, Vol. 163, No. 1, pp. 44–51, 2007.

    Article  Google Scholar 

  23. Wooten, M., Weng, H.-J., Hartke, T. V., Borzan, J., Klein, A. H., et al., “Three Functionally Distinct Classes of C-Fibre Nociceptors in Primates,” Nature Communications, Vol. 5, Article No. 4122, 2014.

  24. Izhikevich, E. M., “Simple Model of Spiking Neurons,” IEEE Transactions on Neural Networks, Vol. 14, No. 6, pp. 1569–1572, 2003.

    Article  MathSciNet  Google Scholar 

  25. Du, J., Blanche, T. J., Harrison, R. R., Lester, H. A., and Masmanidis, S. C., “Multiplexed, High Density Electrophysiology WITH Nanofabricated Neural Probes,” PLoS One, Vol. 6, No. 10, Paper No. e26204, 2011.

    Article  Google Scholar 

  26. Martinez, D., Py, C., Denhoff, M. W., Martina, M., Monette, R., et al., “High-Fidelity Patch-Clamp Recordings from Neurons Cultured on a Polymer Microchip,” Biomedical Microdevices, Vol. 12, No. 6, pp. 977–985, 2010.

    Article  Google Scholar 

  27. Py, C., Martina, M., Monette, R., Comas, T., Denhoff, M. W., et al., “Culturing and Electrophysiology of Cells on NRCC Patch-Clamp Chips,” Journal of Visualized Experiments, Vol. 60, Paper No. e3288, 2012.

    Google Scholar 

  28. Kwok, R., “Once More, with Feeling,” Nature, Vol. 497, No. 7448, pp. 176–178, 2013.

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Biomedical Engineering, Hanyang University, 222, Wangsimni-ro, Seongdong-gu, Seoul, 04763, South Korea

    Kyeongwon Cho, Jeongbong Choi, Min Ki Song, In Young Kim & Dong Pyo Jang

  2. Department of Biomedical Science, Hanyang University, 222, Wangsimni-ro, Seongdong-gu, Seoul, 04763, South Korea

    Jun Ho Jang & Sung Jun Jung

  3. Department of Human and Systems Engineering, Ulsan National Institute of Science and Technology, 50, UNIST-gil, Eonyang-eup, Ulju-gun, Ulsan, 44919, South Korea

    Sung-Phil Kim

Authors
  1. Kyeongwon Cho
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  2. Jun Ho Jang
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  3. Sung-Phil Kim
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  4. Jeongbong Choi
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Correspondence to Sung Jun Jung.

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Cho, K., Jang, J.H., Kim, SP. et al. Analysis of temporal firing patterns of primary afferent C-fibers for different sensations in mice. Int. J. Precis. Eng. Manuf. 18, 739–745 (2017). https://doi.org/10.1007/s12541-017-0088-2

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  • DOI: https://doi.org/10.1007/s12541-017-0088-2

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