Document Type : Review Research Paper


1 M.Sc. Student, Biomedical Engineering Department, School of Electrical Engineering, Iran University of Science and Technology, Tehran, Iran

2 Associate Professor, Biomedical Engineering Department, School of Electrical Engineering, Iran University of Science and Technology, Tehran, Iran

3 Assistant Professor, Biomedical Engineering Department, School of Electrical Engineering, Iran University of Science and Technology, Tehran, Iran


The brain stimulation and its widespread use is one of the most important subjects in studies of neurophysiology. In brain electrical stimulation methods, following the surgery and electrode implantation, electrodes send electrical impulses to the specific targets in the brain. The use of this stimulation method is provided therapeutic benefits for treatment chronic pain, essential tremor, Parkinson’s disease, major depression, and neurological movement disorder syndrome (dystonia). One area in which advancements have been recently made is in controlling the movement and navigation of animals in a specific pathway. It is important to identify brain targets in order to stimulate appropriate brain regions for all the applications listed above. An animal navigation system based on brain electrical stimulation is used to develop new behavioral models for the aim of creating a platform for interacting with the animal nervous system in the spatial learning task. In the context of animal navigation the electrical stimulation has been used either as creating virtual sensation for movement guidance or virtual reward for movement motivation. In this paper, different approaches and techniques of brain electrical stimulation for this application has been reviewed.


Main Subjects

[1]     B. Graimann, B. Allison, and G. Pfurtscheller, "Brain–computer interfaces: A gentle introduction," in Brain-Computer Interfaces: Springer, 2009, pp. 1-27.
[2]     S. Ahn, K. Kim, and S. C. Jun, "Steady-State Somatosensory Evoked Potential for Brain-Computer Interface—Present and Future," Frontiers in human neuroscience, vol. 9, 2015.
[3]     U. Chaudhary, B. Xia, S. Silvoni, L. G. Cohen, and N. Birbaumer, "Brain–computer interface–based communication in the completely locked-in state," PLoS biology, vol. 15, no. 1, p. e1002593, 2017.
[4]     L. F. Nicolas-Alonso and J. Gomez-Gil, "Brain computer interfaces, a review," Sensors, vol. 12, no. 2, pp. 1211-1279, 2012.
[5]     S. Gopinath et al., "Seizure outcome following primary motor cortex-sparing resective surgery for perirolandic focal cortical dysplasia," International Journal of Surgery, vol. 36, pp. 466-476, 2016.
[6]     T. W. Kjaer and H. B. Sørensen, "A brain-computer interface to support functional recovery," in Clinical Recovery from CNS Damage, vol. 32: Karger Publishers, 2013, pp. 95-100.
[7]     E. W. Pang and O. Snead Iii, "From structure to circuits: the contribution of MEG connectivity studies to functional neurosurgery," Frontiers in neuroanatomy, vol. 10, 2016.
[8]     A. Khorasani, R. Foodeh, V. Shalchyan, and M. R. Daliri, "Brain Control of an External Device by Extracting the Highest Force-related Contents of Local Field Potentials in Freely Moving Rats," IEEE Transactions on Neural Systems and Rehabilitation Engineering, 2017.
[9]     A. Khorasani, N. H. Beni, V. Shalchyan, and M. R. Daliri, "Continuous Force Decoding from Local Field Potentials of the Primary Motor Cortex in Freely Moving Rats," Scientific reports, vol. 6, p. 35238, 2016.
[10] R. Holzer and I. Shimoyama, "Locomotion control of a bio-robotic system via electric stimulation," in Intelligent Robots and Systems, 1997. IROS'97., Proceedings of the 1997 IEEE/RSJ International Conference on, 1997, vol. 3, pp. 1514-1519: IEEE.
[11] L. Bao et al., "Flight control of tethered honeybees using neural electrical stimulation," in Neural Engineering (NER), 2011 5th International IEEE/EMBS Conference on, 2011, pp. 558-561: IEEE.
[12] L. Cai, Z. Dai, W. Wang, H. Wang, and Y. Tang, "Modulating motor behaviors by electrical stimulation of specific nuclei in pigeons," Journal of Bionic Engineering, vol. 12, no. 4, pp. 555-564, 2015.
[13] R.-t. Huai, J.-q. Yang, and H. Wang, "The robo-pigeon based on the multiple brain regions synchronization implanted microelectrodes," Bioengineered, vol. 7, no. 4, pp. 213-218, 2016.
[14] Z.-d. Dai and J.-r. Sun, "A biomimetic study of discontinuous-constraint metamorphic mechanism for gecko-like robot," Journal of Bionic Engineering, vol. 4, no. 2, pp. 91-95, 2007.
[15] C. Sun, N. Zheng, X. Zhang, W. Chen, and X. Zheng, "Automatic navigation for rat-robots with modeling of the human guidance," Journal of Bionic Engineering, vol. 10, no. 1, pp. 46-56, 2013.
[16] S. K. Talwar, S. Xu, E. S. Hawley, S. A. Weiss, K. A. Moxon, and J. K. Chapin, "Behavioural neuroscience: Rat navigation guided by remote control," Nature, vol. 417, no. 6884, pp. 37-38, 2002.
[17] M.-G. Lee et al., "Operant conditioning of rat navigation using electrical stimulation for directional cues and rewards," Behavioural processes, vol. 84, no. 3, pp. 715-720, 2010.
[18] Y. Yu et al., "Automatic training of rat cyborgs for navigation," Computational intelligence and neuroscience, vol. 2016, 2016.
[19] Y. Yu et al., "Intelligence-augmented rat cyborgs in maze solving," PloS one, vol. 11, no. 2, p. e0147754, 2016.
[20] C. Sun, X. Zhang, N. Zheng, W. Chen, and X. Zheng, "Bio-robots automatic navigation with electrical reward stimulation," in Engineering in Medicine and Biology Society (EMBC), 2012 Annual International Conference of the IEEE, 2012, pp. 348-351: IEEE.
[21] Y. Li, S. S. Panwar, and S. Mao, "A wireless biosensor network using autonomously controlled animals," IEEE Network, vol. 20, no. 3, pp. 6-11, 2006.
[22] A. Alcaro, R. Huber, and J. Panksepp, "Behavioral functions of the mesolimbic dopaminergic system: an affective neuroethological perspective," Brain research reviews, vol. 56, no. 2, pp. 283-321, 2007.
[23] O. Yizhar et al., "Neocortical excitation/inhibition balance in information processing and social dysfunction," Nature, vol. 477, no. 7363, p. 171, 2011.
[24] J. R. Krebs, "Animal behaviour: From Skinner box to the field," Nature, vol. 304, no. 5922, pp. 117-117, 1983.
[25] S. R. Flora, The power of reinforcement. SUNY Press, 2004.
[26] W. Schultz, "Neuronal reward and decision signals: from theories to data," Physiological Reviews, vol. 95, no. 3, pp. 853-951, 2015.
[27] T. Dalgleish, "The emotional brain," Nature reviews. Neuroscience, vol. 5, no. 7, p. 583, 2004.
[28] R. Huai, J. Yang, H. Wang, and X. Su, "A new robo-animals navigation method guided by the remote control," in Biomedical Engineering and Informatics, 2009. BMEI'09. 2nd International Conference on, 2009, pp. 1-4: IEEE.
[29] M. G. Baxter and E. A. Murray, "The amygdala and reward," Nature reviews. Neuroscience, vol. 3, no. 7, p. 563, 2002.
[30] A. Koene and T. J. Prescott, "Hippocampus, Amygdala and Basal Ganglia based navigation control," in International Conference on Artificial Neural Networks, 2009, pp. 267-276: Springer.
[31] S. Chen et al., "Optogenetics based rat–robot control: optical stimulation encodes “stop” and “escape” commands," Annals of biomedical engineering, vol. 43, no. 8, pp. 1851-1864, 2015.
[32] X. Chen, K. Xu, S. Ye, S. Guo, and X. Zheng, "A remote constant current stimulator designed for rat-robot navigation," in Engineering in Medicine and Biology Society (EMBC), 2013 35th Annual International Conference of the IEEE, 2013, pp. 2168-2171: IEEE.
[33] E. E. Benarroch, "Periaqueductal gray An interface for behavioral control," Neurology, vol. 78, no. 3, pp. 210-217, 2012.
[34] G. C. Kincheski, 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, vol. 7, no. 11, p. e50361, 2012.
[35] D. L. Walker, J. V. Cassella, Y. Lee, T. C. De Lima, and M. Davis, "Opposing roles of the amygdala and dorsolateral periaqueductal gray in fear-potentiated startle," Neuroscience & Biobehavioral Reviews, vol. 21, no. 6, pp. 743-753, 1997.
[36] C. Welker, "Microelectrode delineation of fine grain somatotopic organization of SmI cerebral neocortex in albino rat," Brain research, vol. 26, no. 2, pp. 259-275, 1971.
[37] A. R. Houweling and M. Brecht, "Behavioural report of single neuron stimulation in somatosensory cortex," e-Neuroforum, vol. 14, no. 1, pp. 174-176, 2008.
[38] Y. Yu et al., "Automatic training of ratbot for navigation," in International Workshop on Intelligence Science, in Conjunction with IJCAI-2013, Beijing, China, 2013.
[39] B. Koo et al., "Manipulation of Rat Movement via Nigrostriatal Stimulation Controlled by Human Visually Evoked Potentials," Scientific Reports, vol. 7, 2017.
[40] M. E. Diamond and E. Arabzadeh, "Whisker sensory system–from receptor to decision," Progress in neurobiology, vol. 103, pp. 28-40, 2013.
[41] N. J. Sofroniew, Y. A. Vlasov, S. A. Hires, J. Freeman, and K. Svoboda, "Neural coding in barrel cortex during whisker-guided locomotion," Elife, vol. 4, p. e12559, 2015.
[42] T. E. Robinson, D. M. Camp, and J. B. Becker, "Gonadectomy attenuates turning behavior produced by electrical stimulation of the nigrostriatal dopamine system in female but not male rats," Neuroscience letters, vol. 23, no. 2, pp. 203-208, 1981.
[43] D. A. Staunton, B. B. Wolfe, P. M. Groves, and P. B. Molinoff, "Dopamine receptor changes following destruction of the nigrostriatal pathway: lack of a relationship to rotational behavior," Brain research, vol. 211, no. 2, pp. 315-327, 1981.
[44] U. Ungerstedt and G. W. Arbuthnott, "Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system," Brain research, vol. 24, no. 3, pp. 485-493, 1970.
[45] E. N. Marieb and K. Hoehn, Human anatomy & physiology. Pearson Education, 2007.
[46] P. Anikeeva, "Optogenetics unleashed," Nature biotechnology, vol. 34, no. 1, pp. 43-45, 2016.
[47] A. Prochazka, "Targeted stimulation of the spinal cord to restore locomotor activity," Nature medicine, vol. 22, no. 2, pp. 125-127, 2016.
[48] K. J. Sekiguchi et al., "Imaging large-scale cellular activity in spinal cord of freely behaving mice," Nature communications, vol. 7, 2016.
[49] E. C. Field‐Fote, B. Anderson, V. J. Robertson, and N. I. Spielholz, "Monophasic and biphasic stimulation evoke different responses," Muscle & nerve, vol. 28, no. 2, pp. 239-241, 2003.
[50] J. E. Arle, "The neuromodulation approach," Essential neuromodulation. Academic Press, Waltham, pp. 1-16, 2011.
[51] G. Kantor, G. Alon, and H. S. Ho, "The effects of selected stimulus waveforms on pulse and phase characteristics at sensory and motor thresholds," Physical Therapy, vol. 74, no. 10, pp. 951-962, 1994.
[52] J. P. Reilly, Applied bioelectricity: from electrical stimulation to electropathology. Springer Science & Business Media, 2012.
[53] D. Huber et al., "Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice," Nature, vol. 451, no. 7174, p. 61, 2008.
[54] S. Sachidhanandam, V. Sreenivasan, A. Kyriakatos, Y. Kremer, and C. C. Petersen, "Membrane potential correlates of sensory perception in mouse barrel cortex," Nature neuroscience, vol. 16, no. 11, p. 1671, 2013.
[55] R. W. Doty, "Electrical stimulation of the brain in behavioral context," Annual review of psychology, vol. 20, no. 1, pp. 289-320, 1969.
[56] R. Romo, A. Hernández, A. Zainos, C. D. Brody, and L. Lemus, "Sensing without touching: psychophysical performance based on cortical microstimulation," Neuron, vol. 26, no. 1, pp. 273-278, 2000.
[57] L. Hermer-Vazquez et al., "Rapid learning and flexible memory in “habit” tasks in rats trained with brain stimulation reward," Physiology & behavior, vol. 84, no. 5, pp. 753-759, 2005.
[58] R. A. Wise, "Brain reward circuitry: insights from unsensed incentives," Neuron, vol. 36, no. 2, pp. 229-240, 2002.
[59] C. Harris and M. Stephens, "A combined corner and edge detector," in Alvey vision conference, 1988, vol. 15, no. 50, p. 10.5244: Manchester, UK.
[60] J. Shi, "Good features to track," in Computer Vision and Pattern Recognition, 1994. Proceedings CVPR'94., 1994 IEEE Computer Society Conference on, 1994, pp. 593-600: IEEE.
[61] C. Zhang, C. Sun, L. Gao, N. Zheng, W. Chen, and X. Zheng, "Bio-robots automatic navigation with graded electric reward stimulation based on Reinforcement Learning," in Engineering in Medicine and Biology Society (EMBC), 2013 35th Annual International Conference of the IEEE, 2013, pp. 6901-6904: IEEE.
[62] Y. Wang et al., "Visual cue-guided rat cyborg for automatic navigation [research frontier]," IEEE Computational Intelligence Magazine, vol. 10, no. 2, pp. 42-52, 2015.
[63] Z. Wu, N. Zheng, S. Zhang, X. Zheng, L. Gao, and L. Su, "Maze learning by a hybrid brain-computer system," Scientific reports, vol. 6, 2016.
[64] B.-K. Min and K.-R. Müller, "Electroencephalography/sonication-mediated human brain-brain interfacing technology," Trends in biotechnology, vol. 32, no. 7, p. 345, 2014.
[65] M. Pais-Vieira, M. Lebedev, C. Kunicki, J. Wang, and M. A. Nicolelis, "A brain-to-brain interface for real-time sharing of sensorimotor information," Scientific reports, vol. 3, p. 1319, 2013.
[66] C. Grau et al., "Conscious brain-to-brain communication in humans using non-invasive technologies," PLoS One, vol. 9, no. 8, p. e105225, 2014.
[67] R. P. Rao et al., "A direct brain-to-brain interface in humans," PloS one, vol. 9, no. 11, p. e111332, 2014.
[68] M. Hashimoto, A. Hata, T. Miyata, and H. Hirase, "Programmable wireless light-emitting diode stimulator for chronic stimulation of optogenetic molecules in freely moving mice," Neurophotonics, vol. 1, no. 1, pp. 011002-011002, 2014.
[69] T. K. Roseberry, A. M. Lee, A. L. Lalive, L. Wilbrecht, A. Bonci, and A. C. Kreitzer, "Cell-type-specific control of brainstem locomotor circuits by basal ganglia," Cell, vol. 164, no. 3, pp. 526-537, 2016.
[70] V. Gradinaru et al., "Targeting and readout strategies for fast optical neural control in vitro and in vivo," Journal of Neuroscience, vol. 27, no. 52, pp. 14231-14238, 2007.
[71] M. Jeong et al., "Comparative three-dimensional connectome map of motor cortical projections in the mouse brain," Scientific reports, vol. 6, p. 20072, 2016.
[72] A. M. Aravanis et al., "An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology," Journal of neural engineering, vol. 4, no. 3, p. S143, 2007.
[73] A. V. Kravitz et al., "Regulation of parkinsonian motor behaviors by optogenetic control of basal ganglia circuitry," Nature, vol. 466, no. 7306, p. 622, 2010.
[74] R. D. Proville et al., "Cerebellum involvement in cortical sensorimotor circuits for the control of voluntary movements," Nature Neuroscience, vol. 17, no. 9, pp. 1233-1239, 2014.
[75] R. Foodeh, A. Khorasani, V. Shalchyan, and M. R. Daliri, "Minimum Noise Estimate Filter: A Novel Automated Artifacts Removal Method for Field Potentials," IEEE Transactions on Neural Systems and Rehabilitation Engineering, vol. 25, no. 8, pp. 1143-1152, 2017.
[76] D. Zhang, Y. Dong, M. Li, and H. Wang, "A radio-telemetry system for navigation and recording neuronal activity in free-roaming rats," Journal of Bionic Engineering, vol. 9, no. 4, pp. 402-410, 2012
[77] S. Xu, S. K. Talwar, E. S. Hawley, L. Li, and J. K. Chapin, "A multi-channel telemetry system for brain microstimulation in freely roaming animals," Journal of neuroscience methods, vol. 133, no. 1, pp. 57-63, 2004.
[78] K. Xu, J. Zhang, H. Zhou, J. C. T. Lee, and X. Zheng, "A novel turning behavior control method for rat-robot through the stimulation of ventral posteromedial thalamic nucleus," Behavioural brain research, vol. 298, pp. 150-157, 2016.
[79] T. C. Harrison, O. G. Ayling, and T. H. Murphy, "Distinct cortical circuit mechanisms for complex forelimb movement and motor map topography," Neuron, vol. 74, no. 2, pp. 397-409, 2012.
[80] Comte P. Monopolar versus bipolar stimulation. Stereotactic and Functional Neurosurgery. 1982;45(1-2):156-9.
[81] Gao, Lixia, Xinjian Li, Wenwei Yang and Xinde Sun, "Modulation of azimuth tuning plasticity in rat primary auditory cortex by medial prefrontal cortex." Neuroscience 347 (2017): 36-47.