Skip to main content

Advertisement

Log in

Optogenetics Based Rat–Robot Control: Optical Stimulation Encodes “Stop” and “Escape” Commands

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Electric brain stimulation is frequently used in bio-robot control. However, one possible limitation of electric stimulation is the resultant wide range of influences that may lead to unexpected side-effects. Although there has been prior research done towards optogenetics based brain activation, there has not been much development regarding the comparisons between electric and optical methods of brain activation. In this study, we first encode “Stop” and “Escape” commands by optical stimulation in the dorsal periaqueductal grey (dPAG). The rats behavioral comparisons are then noted down under these two methods. The dPAG neural activity recorded during optical stimulation suggests rate and temporal coding mechanisms in behavioral control. The behavioral comparisons show that rats exhibit anxiety under the “Stop” command conveyed through both optical and electric methods. However, rats are able to recover more quickly from freezing only under optical “Stop” command. Under “Escape” commands, also conveyed through optical means, the rat would move with lessened urgency but the results are more stable. Moreover, c-Fos study shows the optical stimulation activates restricted range in midbrain: the optical stimulation affected only dPAG and its downstreams but electric stimulation activates both the upstream and downstream circuits, in which the glutamatergic neurons are largely occupied and play important role in “Stop” and “Escape” behavior controls. We conclude that optical stimulation is more suited for encoding “Stop” and “Escape” commands for rat–robot control.

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.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Arantes, R., J. Tejada, G. G. Bosco, S. Morato, and A. C. Roque. Mathematical methods to model rodent behavior in the elevated plus-maze. J. Neurosci. Methods 220(2):141–148, 2013.

    Article  PubMed  Google Scholar 

  2. Bittencourt, A. S., E. M. Nakamura-Palacios, H. Mauad, S. Tufik, and L. C. Schenberg. Organization of electrically and chemically evoked defensive behaviors within the deeper collicular layers as compared to the periaqueductal gray matter of the rat. Neuroscience 133(4):873–892, 2005.

    Article  CAS  PubMed  Google Scholar 

  3. Chen, S., Y. Qu, S. Guo, Z. Shi, K. Xu, and X. Zheng. Encode the “STOP” command by photo-stimulation for precise control of rat–robot. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2013:2172–2175, 2013.

    PubMed  Google Scholar 

  4. Chen, X., K. Xu, S. Ye, S. Guo, and X. Zheng. A remote constant current stimulator designed for rat–robot navigation. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2013:2168–2171, 2013.

    PubMed  Google Scholar 

  5. Coimbra, N. C., R. De Oliveira, R. L. Freitas, S. J. Ribeiro, K. G. Borelli, R. C. Pacagnella, J. E. Moreira, L. A. da Silva, L. L. Melo, L. O. Lunardi, and M. L. Brandao. Neuroanatomical approaches of the tectum-reticular pathways and immunohistochemical evidence for serotonin-positive perikarya on neuronal substrates of the superior colliculus and periaqueductal gray matter involved in the elaboration of the defensive behavior and fear-induced analgesia. Exp. Neurol. 197(1):93–112, 2006.

    Article  CAS  PubMed  Google Scholar 

  6. Feng, Z. Y., W. D. Chen, X. S. Ye, S. M. Zhang, X. J. Zheng, P. Wang, J. Jiang, L. Jin, Z. J. Xu, C. Q. Liu, F. X. Liu, J. H. Luo, Y. T. Zhuang, and X. X. Zheng. A remote control training system for rat navigation in complicated environment. J. Zhejiang Univ. Sci. A 8(2):323–330, 2007.

    Article  Google Scholar 

  7. Furigo, I. C., W. F. de Oliveira, A. R. de Oliveira, E. Comoli, M. V. Baldo, S. R. Mota-Ortiz, and N. S. Canteras. The role of the superior colliculus in predatory hunting. Neuroscience 165(1):1–15, 2010.

    Article  CAS  PubMed  Google Scholar 

  8. Gale, J. T., K. H. Lee, R. Amirnovin, D. W. Roberts, Z. M. Williams, C. D. Blaha, and E. N. Eskandar. Electrical stimulation-evoked dopamine release in the primate striatum. Stereotact. Funct. Neurosurg. 91(6):355–363, 2013.

    Article  PubMed  Google Scholar 

  9. Gerits, A., and W. Vanduffel. Optogenetics in primates: a shining future? Trends Genet. 29(7):403–411, 2013.

    Article  CAS  PubMed  Google Scholar 

  10. Gradinaru, V., M. Mogri, K. R. Thompson, J. M. Henderson, and K. Deisseroth. Optical deconstruction of parkinsonian neural circuitry. Science 324(5925):354–359, 2009.

    Article  CAS  PubMed  Google Scholar 

  11. Guo, S., H. Zhou, J. Zhang, K. Xu, and X. Zheng. A multi-electrode array coupled with fiberoptic for deep-brain optical neuromodulation and electrical recording. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2013:2752–2755, 2013.

    PubMed  Google Scholar 

  12. Jasnow, A. M., E. D. Ehrlich, D. C. Choi, J. Dabrowska, M. E. Bowers, K. M. McCullough, D. G. Rainnie, and K. J. Ressler. Thy1-expressing neurons in the basolateral amygdala may mediate fear inhibition. J. Neurosci. 33(25):10396–10404, 2013.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Kincheski, G. C., and A. P. Carobrez. The dorsal periaqueductal gray modulates the increased fear-like behavior exhibited by experienced rats in the elevated plus-maze. Behav. Brain Res. 206(1):120–126, 2010.

    Article  PubMed  Google Scholar 

  14. Kincheski, G. C., S. R. Mota-Ortiz, E. Pavesi, N. S. Canteras, and A. P. Carobrez. The dorsolateral periaqueductal gray and its role in mediating fear learning to life threatening events. PLoS ONE 7(11):e50361, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. LaLumiere, R. T. A new technique for controlling the brain: optogenetics and its potential for use in research and the clinic. Brain Stimul. 4(1):1–6, 2011.

    Article  PubMed  Google Scholar 

  16. Lim, L. W., A. Blokland, V. Visser-Vandewalle, R. Vlamings, T. Sesia, H. Steinbusch, K. Schruers, E. Griez, and Y. Temel. High-frequency stimulation of the dorsolateral periaqueductal gray and ventromedial hypothalamus fails to inhibit panic-like behaviour. Behav. Brain Res. 193(2):197–203, 2008.

    Article  PubMed  Google Scholar 

  17. Martinelli, E., D. Polese, F. Dini, R. Paolesse, D. Filippini, I. Lundstrom, and C. Di Natale. An investigation on the role of spike latency in an artificial olfactory system. Front. Neuroeng. 4:16, 2011.

    Article  PubMed Central  PubMed  Google Scholar 

  18. McIntyre, C. C., and W. M. Grill. Finite element analysis of the current-density and electric field generated by metal microelectrodes. Ann. Biomed. Eng. 29(3):227–235, 2001.

    Article  CAS  PubMed  Google Scholar 

  19. McIntyre, C. C., W. M. Grill, D. L. Sherman, and N. V. Thakor. Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J. Neurophysiol. 91(4):1457–1469, 2004.

    Article  PubMed  Google Scholar 

  20. McIntyre, C. C., S. Mori, D. L. Sherman, N. V. Thakor, and J. L. Vitek. Electric field and stimulating influence generated by deep brain stimulation of the subthalamic nucleus. Clin. Neurophysiol. 115(3):589–595, 2004.

    Article  PubMed  Google Scholar 

  21. Moers-Hornikx, V. M., J. S. Vles, L. W. Lim, M. Ayyildiz, S. Kaplan, A. W. Gavilanes, G. Hoogland, H. W. Steinbusch, and Y. Temel. Periaqueductal grey stimulation induced panic-like behaviour is accompanied by deactivation of the deep cerebellar nuclei. Cerebellum 10(1):61–69, 2011.

    Article  PubMed Central  PubMed  Google Scholar 

  22. Phongphanphanee, P., R. A. Marino, K. Kaneda, Y. Yanagawa, D. P. Munoz, and T. Isa. Distinct local circuit properties of the superficial and intermediate layers of the rodent superior colliculus. Eur. J. Neurosci. 40(2):2329–2343, 2014.

    Article  PubMed  Google Scholar 

  23. Roncon, C. M., C. Biesdorf, N. C. Coimbra, E. A. Audi, H. Zangrossi, Jr., and F. G. Graeff. Cooperative regulation of anxiety and panic-related defensive behaviors in the rat periaqueductal grey matter by 5-HT1A and mu-receptors. J. Psychopharmacol. 27(12):1141–1148, 2013.

    Article  CAS  PubMed  Google Scholar 

  24. Thanos, P. K., L. Robison, E. J. Nestler, R. Kim, M. Michaelides, M. K. Lobo, and N. D. Volkow. Mapping brain metabolic connectivity in awake rats with muPET and optogenetic stimulation. J. Neurosci. 33(15):6343–6349, 2013.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Towal, R. B., and M. J. Hartmann. Right-left asymmetries in the whisking behavior of rats anticipate head movements. J. Neurosci. 26(34):8838–8846, 2006.

    Article  CAS  PubMed  Google Scholar 

  26. Tulogdi, A., P. Soros, M. Toth, R. Nagy, L. Biro, M. Aliczki, B. Klausz, E. Mikics, and J. Haller. Temporal changes in c-Fos activation patterns induced by conditioned fear. Brain Res. Bull. 88(4):359–370, 2012.

    Article  CAS  PubMed  Google Scholar 

  27. Vianna, D. M., K. G. Borelli, C. Ferreira-Netto, C. E. Macedo, and M. L. Brandao. Fos-like immunoreactive neurons following electrical stimulation of the dorsal periaqueductal gray at freezing and escape thresholds. Brain Res. Bull. 62(3):179–189, 2003.

    Article  CAS  PubMed  Google Scholar 

  28. Wang, H., Y. Chen, and Y. Chen. First-spike latency in Hodgkin’s three classes of neurons. J. Theor. Biol. 328:19–25, 2013.

    Article  PubMed  Google Scholar 

  29. Xiao, N., E. Privman, and B. J. Venton. Optogenetic control of serotonin and dopamine release in Drosophila larvae. ACS Chem. Neurosci. 5(8):666–673, 2014.

    Article  CAS  PubMed  Google Scholar 

  30. Yizhar, O., L. E. Fenno, T. J. Davidson, M. Mogri, and K. Deisseroth. Optogenetics in neural systems. Neuron 71(1):9–34, 2011.

    Article  CAS  PubMed  Google Scholar 

  31. Zhang, C. L., X. Houbaert, M. Lepleux, M. Deshors, E. Normand, F. Gambino, E. Herzog, and Y. Humeau. The hippocampo-amygdala control of contextual fear expression is affected in a model of intellectual disability. Brain Struct. Funct., 2014. doi:10.1007/s00429-014-0882-x.

Download references

Acknowledgments

We thank Dr. ShuMin Duan for assistance with virus injection and frozen brain slices preparation. We thank ChaoNan Yu for the animal surgery and the fabrication of the multi-electrode array and LiQiang Gao for the assistance with partial EPM image processing. We thank Tristan of National University of Singapore for language editing. This research was supported by (1) National Basic Research Program of China, 2011CB504400; (2) The National High Technology Research and Development Program of China, 2012AA020408; (3) National Natural Science Foundation of China, 61305145, 61305146, 31371001; (4) Specialized Research Fund for Doctoral Program of Higher Education, 20130101120166; (5) Fundamental Research Funds for the Central Universities; (6) Zhejiang Provincial Natural Science Foundation of China LQ13H180001.

Conflict of interest

All authors declare no conflict and financial interest relating to this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to KeDi Xu.

Additional information

Associate Editor Anastasios G. Bezerianos oversaw the review of this article.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10439_2014_1235_MOESM1_ESM.tif

Fig. S1 Retrograde labeling of neurons by CTB. (A) CTB-AF555 was microinjected into the dPAG, and fluorescent cell bodies were found in the cont-dPAG and ips-SC in the midbrain and are magnified in (B) and (C), separately. (D) CTB-AF555 was microinjected into the SC. Some neurons in the cont-SC showed fluorescent cell bodies, and a very high density of fluorescent cell bodies was shown in a broad range of ips-SC and is magnified in (E) and (F) separately. The asterisks show the cell body positions in (B) and (E). (TIFF 24931 kb)

10439_2014_1235_MOESM2_ESM.tif

Fig. S2 The glutamatergic neurons axon projection directions. (A) Glutamatergic neuron projection from dPAG (injection position labeled as shadow); The fluorescent axons exhibited in contralateral dPAG (B), ipsilateral BIC (C), ipsilateral cp (D) and ipsilateral PPTg (E); (F) Glutamatergic neuron projection from SC (injection position labeled as shadow); The fluorescent axons exhibited in ipsilateral BIC (G) via ipsilateral SC (H), in ipsilateral dPAG (I) and contralateral SC (J). (TIFF 48831 kb)

Supplementary material 3 (DOCX 12 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, S., Zhou, H., Guo, S. et al. Optogenetics Based Rat–Robot Control: Optical Stimulation Encodes “Stop” and “Escape” Commands. Ann Biomed Eng 43, 1851–1864 (2015). https://doi.org/10.1007/s10439-014-1235-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-014-1235-x

Keywords

Navigation