Review of Human Enhancement through Electrical Nerve Stimulation
Pan Ziqi1, Zhu Bingquan2, Liu Jing1*
1(China National Center for Biotechnology Development, Beijing 100039, China) 2 (School of Aerospace Engineering, Tsinghua University, Beijing 100084, China)
Abstract：Recently there has been growing research on electrical nerve stimulation for human enhancement, including augmentations on cognition (memory, learning and emotion), perception and movement. In addition, brain machine interfaces (BMIs) stimulate human brain precisely. And a tremendous effort has been applied to boost BMI’s information gathering and processing capacity. Transcranial direct current stimulation (tDCS), representing non-invasive stimulation, implements easily but needs further investigation of long-term effectiveness and spatial resolution. Invasive stimulation methods, including deep brain stimulation (DBS) and vagus nerve stimulation (VNS), have been widely accepted in clinical practice with high spatial resolution. But these methods have the restriction for enhancement in both research and application. This article reviews the research progresses in electrical stimulation for human enhancement and advances in BMI, and discusses the limitations and tendency.
潘子奇, 朱秉泉, 刘静. 神经电刺激下的人体增强研究进展[J]. 中国生物医学工程学报, 2018, 37(4): 489-497.
Pan Ziqi, Zhu Bingquan, Liu Jing. Review of Human Enhancement through Electrical Nerve Stimulation. Chinese Journal of Biomedical Engineering, 2018, 37(4): 489-497.
[1] Clark VP, Parasuraman R. Neuroenhancement: enhancing brain and mind in health and in disease[J]. Neuroimage, 2014, 85(2): 889-894.
[2] Hatsopoulos NG, Donoghue JP. The science of neural interface systems[J]. Annual Review of Neuroscience, 2009, 32(1): 249-266.
[3] McGaugh JL. Memory--A century of consolidation[J]. Science, 2000, 287(5451): 248-251.
[4] Wilson MA, McNaughton BL. Reactivation of hippocampal ensemble memories during sleep[J]. Science, 1994, 265(5172): 676-679.
[5] Stickgold R. Sleep-dependent memory consolidation[J]. Nature, 2005, 437(7063): 1272-1278.
[6] Foster DJ, Wilson MA. Reverse replay of behavioural sequences in hippocampal place cells during the awake state[J]. Nature, 2006, 440(7084): 680-683.
[7] Ji D, Wilson MA. Coordinated memory replay in the visual cortex and hippocampus during sleep[J]. Nature neuroscience, 2007, 10(1): 100-107.
[8] Brunoni AR, Nitsche MA, Bolognini N,et al. Clinical research with transcranial direct current stimulation (tDCS): challenges and future directions[J]. Brain Stimulation: Basic, Translational, and Clinical Research in Neuromodulation, 2012, 5: 175-195.
[9] Giordano J, Bikson M, Kappenman ES, et al. Mechanisms and effects of transcranial direct current stimulation[J]. Dose-Response, 2017, 15: 1559325816685467.
[10] Yavari F, Jamil A, Samani MM, et al. Basic and functional effects of transcranial Electrical Stimulation (tES)-An introduction[J]. Neuroscience & Biobehavioral Reviews, 2017, 85: 81-92.
[11] Hunter MA,Coffman BA, Coffman GC. Baseline effects of transcranial direct current stimulation on glutamatergic neurotransmission and large-scale network connectivity[J]. Brain Research, 2015, 1594: 92-107.
[12] Datta A, Krause MR, Pilly PK, et al. On comparing in vivo intracranial recordings in non-human primates to predictions of optimized transcranial electrical stimulation[C]// 2016 IEEE 38th Annual International Conference of the Engineering in Medicine and Biology Society. Orlando: 2016: 1774-1777.
[13] Krause MR, Zanos TP, Csorba BA, et al. Transcranial direct current stimulation facilitates associative learning and alters functional connectivity in the primate brain[J]. Current Biology, 2017, 27(20): 3086-3096.
[14] Kringelbach ML, Jenkinson N, Owen SLF, et al. Translational principles of deep brain stimulation[J]. Nature Reviews Neuroscience, 2007, 8(8): 623-635.
[15] Enrici I, Mitkova A, Castelli L, et al. Deep Brain Stimulation of the subthalamic nucleus does not negatively affect social cognitive abilities of patients with Parkinson′s disease[J]. Scientific Reports, 2017, 7(1): 1-9.
[16] Witt K, Pulkowski U, Herzog J, et al. Deep brain stimulation of the subthalamic nucleus improves cognitive flexibility but impairs response inhibition in Parkinson disease[J]. Archives of Neurology, 2004, 61(5): 697-700.
[17] Zangaglia R, Pacchetti C, Pasotti C, et al. Deep brain stimulation and cognitive functions in Parkinson′s disease: A three‐year controlled study[J]. Movement Disorders, 2009, 24(11): 1621-1628.
[18] Suthana N, Fried I. Deep brain stimulation for enhancement of learning and memory[J]. Neuroimage, 2014, 85(2): 996-1002.
[19] Costa A, Carlesimo GA, Caltagirone C, et al. Effects of deep brain stimulation of the peduncolopontine area on working memory tasks in patients with Parkinson′s disease[J]. Parkinsonism & Related Disorders, 2010, 16(1): 64-67.
[20] Laxton AW, TangWDF, McAndrews MP, et al. A phase Itrial of deep brain stimulation of memory circuits in Alzheimer′s disease[J]. Annals of Neurology, 2010, 68(4): 521-534.
[21] Merkl A, Röck E, Schmitz-Hübsch T, et al. Effects of subthalamic nucleus deep brain stimulation on emotional working memory capacity and mood in patients with Parkinson′s disease[J]. Neuropsychiatric Disease and Treatment, 2017, 13: 1603-1611.
[22] Schunk DH. Learning theories an educational perspective sixth edition[M]. Boston: Pearson, 2012.
[23] Marin M, Camprodon JA, Dougherty DD, et al. Deviced-based brain stimulation to augment fear extinction: Implications for PTSD treatment and beyond[J]. Depression and Anxiety, 2014, 31(4): 269-278.
[24] Nikolin S, Loo CK, Bai S, et al. Focalised stimulation using high definition transcranial direct current stimulation (HD-tDCS) to investigate declarative verbal learning and memory functioning[J]. Neuroimage, 2015, 117: 11-19.
[25] Summers JJ, Kang N, Cauraugh JH. Does transcranial direct current stimulation enhance cognitive and motor functions in the ageing brain? A systematic review and meta-analysis[J]. Ageing Research Reviews, 2016, 25: 42-54.
[26] Mure H, Tang CC, Argyelan M, et al. Improved sequence learning with subthalamic nucleus deep brain stimulation: evidence for treatment-specific network modulation[J]. Journal of Neuroscience, 2012, 32(8): 2804-2813.
[27] Van Hartevelt TJ, Fernandes HM, Stevner ABA, et al. Neural plasticity in human brain connectivity: The effects of deep brain stimulation[M]//The Rewiring Brain, 2017.
[28] Edwards CA, Kouzani A, Lee KH, et al. Neurostimulation Devices for the Treatment of Neurologic Disorders[J]. Mayo Clinic Proceedings, 2017, 92(9): 1427-1444.
[29] Carreno FR, Frazer A. Vagal nerve stimulation for treatment-resistant depression[J]. Neurotherapeutics, 2017, 14(3): 716-727.
[30] Thimot J, Shepard KL. Bioelectronic devices: Wirelessly powered implants[J]. Nature Biomedical Engineering, 2017, 1(3): 1161-1165.
[31] Bendor D, Wang X. The neuronal representation of pitch in primate auditory cortex[J]. Nature, 2005, 436(7054): 1161-1165.
[32] Wang X, Walker KMM. Neural mechanisms for the abstraction and use of pitch information in auditory cortex[J]. Journal of Neuroscience, 2012, 32(39): 13339-13342.
[33] Roy S, Wang X, Olson A, et al. A wideband RF link at the 5.8 GHz ISM band for multi-channel neural telemetry for small animals[C]//Biomedical Circuits and Systems Conference (BioCAS). San Diego: IEEE, 2011: 106-109.
[34] Engineer ND, Riley JR, Seale JD, et al. Reversing pathological neural activity using targeted plasticity[J]. Nature, 2011, 470(7332): 106-109.
[35] Tyler R, Cacace A, Stocking C, et al. Vagus nerve stimulation paired with tones for the treatment of tinnitus: A prospective randomized double-blind controlled pilot study in humans[J]. Scientific Reports, 2017, 7(1): 1-11.
[36] Engineer CT, Shetake JA, Engineer ND, et al. Temporal plasticity in auditory cortex improves neural discrimination of speech sounds[J]. Brain Stimulation: Basic, Translational, and Clinical Research in Neuromodulation, 2017, 10(3): 543-552.
[37] Rolls ET. On the brain and emotion[J]. Behavioral & Brain Sciences, 2000, 23(2): 219-228.
[38] Zald DH. The human amygdala and the emotional evaluation of sensory stimuli[J]. Brain Research Reviews, 2003, 41(1): 88-123.
[39] Phelps EA, LeDoux JE. Contributions of the amygdala to emotion processing: from animal models to human behavior[J]. Neuron, 2005, 48(2): 175-187.
[40] Vuilleumier P, Armony JL, Driver J, et al. Distinct spatial frequency sensitivities for processing faces and emotional expressions[J]. Nature Neuroscience, 2003, 6(6): 624-631.
[41] Whalen PJ, Kagan J, Cook RG, et al. Human amygdala responsivity to masked fearful eye whites[J]. Science, 2004, 306(5704): 2061-2061.
[42] Spezio ML, Adolphs R, Hurley RSE, et al. Analysis of face gaze in autism using ″Bubbles″[J]. Neuropsychologia, 2007, 45(1): 144-151.
[43] Teasdale JD, Howard RJ, Cox SG, et al. Functional MRI study of the cognitive generation of affect[J]. AmericanJournal of Psychiatry, 1999, 156(2): 209-215.
[44] Ochsner KN, Ray RR, Hughes B, et al. Bottom-up and top-down processes in emotion generation: common and distinct neural mechanisms[J]. Psychological Science, 2009, 20(11): 1322-1331.
[45] Waugh CE, Hamilton JP, Gotlib IH. The neural temporal dynamics of the intensity of emotional experience[J]. Neuroimage, 2010, 49(2): 1699-1707.
[46] Schiefer M, Tan D, Sidek SM, et al. Sensory feedback by peripheral nerve stimulation improves task performance in individuals with upper limb loss using a myoelectric prosthesis[J]. Journal of Neural Engineering, 2015, 13(1): 1-25.
[47] Sackeim HA, George MS. Brain stimulation-Basic, translational, and clinical research in neuromodulation: Why a new journal?[J]. Brain Stimulation: Basic, Translational, and Clinical Research in Neuromodulation, 2008, 1(1): 4-6.
[48] Noble LJ, Gonzalez IJ, Meruva VB, et al. Effects of vagus nerve stimulation on extinction of conditioned fear and post-traumatic stress disorder symptoms in rats[J]. Translational Psychiatry, 2017, 7(8): 1-8.
[49] Lhommée E, Wojtecki L, Czernecki V, et al. Behavioural outcomes of subthalamic stimulation and medical therapy versus medical therapy alone for Parkinson′s disease with early motor complications (EARLYSTIM trial): secondary analysis of an open-label randomised trial[J]. The Lancet Neurology, 2018, 17(3): 223-231.
[50] Albuquerque L, Coelho M, Martins M, et al. STN-DBS does not change emotion recognition in advanced Parkinson′s disease[J]. Parkinsonism & Related Disorders, 2014, 20(2): 166-169.
[51] Huys D, Bartsch C, Koester P, et al. Motor improvement and emotional stabilization in patients with tourette syndrome after deep brain stimulation of the ventral anterior and ventrolateral[J]. Biological Psychiatry, 2016, 79(5): 392-401.
[52] Greenhouse I, Gould S, Houser M, et al. Stimulation at dorsal and ventral electrode contacts targeted at the subthalamic nucleus has different effects on motor and emotion functions in Parkinson′s disease[J]. Neuropsychologia, 2011, 49(3): 233-267.
[53] Bick SKB, Folley BS, Mayer JS, et al. Subthalamic Nucleus Deep Brain Stimulation Alters Prefrontal Correlates of Emotion Induction[J]. Neuromodulation Technology at the Neural Interface, 2017, 20(3): 528-534.
[54] Ebisch SJ, Perrucci MG, Ferretti A, et al. The sense of touch: embodied simulation in a visuotactile mirroring mechanism for observed animate or inanimate touch[J]. Journal of Cognitive Neuroscience, 2008, 20(9): 1611-1623.
[55] Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation[J]. The Journal of Physiology, 2000, 527(3): 633-639.
[56] Min HK, Hwang SC, Marsh MP, et al. Deep brain stimulation induces BOLD activation in motor and non-motor networks: an fMRI comparison study of STN and EN/GPi DBS in large animals[J]. Neuroimage, 2012, 63(3): 1408-1420.
[57] Marasco PD, Hebert JS, Sensinger JW, et al. Illusory movement perception improves motor control for prosthetic hands[J]. Science Translational Medicine, 2018, 10(432): eaao6990.
[58] Dweiri YM, Stone MA, Tyler DJ, et al. Fabrication of high contact-density, flat-interface nerve electrodes for recording and stimulation applications.[J]. Journal of Visualized Experiments, 2016,2016:116.
[59] Christie BP, Freeberg M, Memberg WD, et al. Long-term stability of stimulating spiral nerve cuff electrodes on human peripheral nerves[J]. Journal of Neuroengineering and Rehabilitation, 2017, 14(1): 1-12.
[60] Tan DW, Schiefer MA, Keith MW, et al. A neural interface provides long-term stable natural touch perception[J]. Science Translational Medicine, 2014, 6(257): 1-12.
[61] Wang Y, Hao Y, Zhou J, et al. Direct current stimulation over the human sensorimotor cortex modulates the brain′s hemodynamic response to tactile stimulation[J]. European Journal of Neuroscience, 2015, 42(3): 1933-1940.
[62] Labbé S, Meftah EM, Chapman CE. Effects of transcranial direct current stimulation of primary somatosensory cortex on vibrotactile detection and discrimination[J]. Journal of Neurophysiology, 2016, 115(4): 1978-1987.
[63] Fujimoto S, Kon N, Otaka Y, et al. Transcranial direct current stimulation over the primary and secondary somatosensory cortices transiently improves tactile spatial discrimination in stroke patients[J]. Frontiers in Neuroscience, 2016, 10: 1-9.
[64] Zhou J, Lo OY, Lipsitz LA, et al. Transcranial direct current stimulation enhances foot sole somatosensation when standing in older adults[J]. Experimental Brain Research, 2018, 236(3): 795-802.
[65] Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans[J]. Neurology, 2001, 57(10): 1899-1901.
[66] Hummel F, Celnik P, Giraux P, et al. Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke[J]. Brain, 2005, 128(3): 490-499.
[67] Bolognini N, Pascual-Leone A, Fregni F. Using non-invasive brain stimulation to augment motor training-induced plasticity[J]. Journal of Neuroengineering and Rehabilitation, 2009, 6(1): 1-13.
[68] Boggio PS, Castro LO, Savagim EA, et al. Enhancement of non-dominant hand motor function by anodal transcranial direct current stimulation[J]. Neuroscience Letters, 2006, 404(1-2): 232-236.
[69] Hornyak T. Smarter, not harder[J]. Nature, 2017, 549(7670): S1-S3.
[70] Angius L, Marcora SM, Hopker JG, et al. Transcranial direct current stimulation improves cycling performance in healthy individuals[C]// Proceedings of The Physiological Society.Nottingham: Physiological Society, 2016: 29-31.
[71] Reis J, Schambra HM, Cohen LG, et al. Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation[J]. Proceedings of the National Academy of Sciences, 2009, 106(5): 1590-1595.
[72] Koyama S, Tanaka S, Tanabe S, et al. Dual-hemisphere transcranial direct current stimulation over primary motor cortex enhances consolidation of a ballistic thumb movement[J]. Neuroscience Letters, 2015, 588: 49-53.
[73] Koller WC, Lyons KE, Wilkinson SB, et al. Efficacy of unilateral deep brain stimulation of the VIM nucleus of the thalamus for essential head tremor[J]. Movement Disorders, 1999, 14(5): 847-850.
[74] Ondo W, Jankovic J, Schwartz K, et al. Unilateral thalamic deep brain stimulation for refractory essential tremor and Parkinson′s disease tremor[J]. Neurology, 1998, 51(4): 1063-1069.
[75] Rehncrona S, Johnels B, Widner H, et al. Long‐term efficacy of thalamic deep brain stimulation for tremor: Double‐blind assessments[J]. Movement Disorders, 2003, 18(2): 163-170.
[76] Huss DS, Dallapiazza RF, Shah BB, et al. Functional assessment and quality of life in essential tremor with bilateral or unilateral DBS and focused ultrasound thalamotomy[J]. Movement Disorders, 2015, 30(14): 1937-1943.
[77] Baizabal-Carvallo JF, Kagnoff MN, Jimenez-Shahed J, et al. The safety and efficacy of thalamic deep brain stimulation in essential tremor: 10 years and beyond[J]. J Neurol Neurosurg Psychiatry, 2014, 85(5): 567-572.
[78] Kumar R, Lozano AM, Sime E, et al. Long-term follow-up of thalamic deep brain stimulation for essential and parkinsonian tremor[J]. Neurology, 2003, 61(11): 1601-1604.
[79] Anderson VC, Burchiel KJ, Hogarth P, et al. Pallidal vs subthalamic nucleus deep brain stimulation in Parkinson disease[J]. Archives of Neurology, 2005, 62(4): 554-560.
[80] Peppe A, Pierantozzi M, Altibrandi MG, et al. Bilateral GPi DBS is useful to reduce abnormal involuntary movements in advanced Parkinson′s disease patients, but its action is related to modality and site of stimulation[J]. European Journal of Neurology, 2001, 8(6): 579-586.
[81] Bastian AJ, Kelly VE, Revilla FJ, et al. Different effects of unilateral versus bilateral subthalamic nucleus stimulation on walking and reaching in Parkinson′s disease[J]. Movement Disorders, 2003, 18(9): 1000-1007.
[82] Ferrarin M, Rizzone M, Bergamasco B, et al. Effects of bilateral subthalamic stimulation on gait kinematics and kinetics in Parkinson′s disease[J]. Experimental Brain Research, 2005, 160(4): 517-527.
[83] Beudel M, Little S, Pogosyan A, et al. Tremor reduction by deep brain stimulation is associated with gamma power suppression in Parkinson′s disease[J]. Neuromodulation: Technology at the Neural Interface, 2015, 18(5): 349-354.
[84] Drachman DA. Do we have brain to spare?[J]. Neurology, 2005, 64(12): 2004-2005.
[85] Schwarz DA, Lebedev MA, Hanson TL, et al. Chronic, wireless recordings of large-scale brain activity in freely moving rhesus monkeys[J]. Nature Methods, 2014, 11(6): 670-676.
[86] Larson L, Nurmikko A. Microwave communication links for brain interface applications[C]// 2016 IEEE 16th Topical Meeting on Silicon Monolithic Integrated Circuits in RF Systems (SiRF). Austin: IEEE, 2016: 73-76.
[87] Sarasola-Sanz A, López-Larraz E, Irastorza-Landa N, et al. An EEG-based brain-machine interface to control a 7-degrees of freedom exoskeleton for stroke rehabilitation[G]// Converging Clinical and Engineering Research on Neurorehabilitation II. Segovia: Springer, 2017: 1127-1131.
[88] Opie NL, Rind GS, John SE, et al. Feasibility of a chronic, minimally invasive endovascular neural interface[C]// 2016 IEEE 38th Annual International Conference of the Engineering in Medicine and Biology Society (EMBC). Orlando: IEEE, 2016: 4455-4458.
[89] Oxley TJ, Opie NL, John SE, et al. Minimally invasive endovascular stent-electrode array for high-fidelity, chronic recordings of cortical neural activity[J]. Nature Biotechnology, 2016, 34(3): 320-327.
[90] Angle MR, Cui B, Melosh NA. Nanotechnology and neurophysiology[J]. Current Opinion in Neurobiology, 2015, 32: 132-140.
[91] Angle MR, Schaefer AT. Neuronal recordings with solid-conductor intracellular nanoelectrodes (SCINEs)[J]. PLoS ONE, 2012, 7(8): 1-8.
[92] Edgington R, Sato S, Ishiyama Y, et al. Growth and electrical characterisation of δ-doped boron layers on (111) diamond surfaces[J]. Journal of Applied Physics, 2012, 111(3): 1-8.
[93] Maybeck V, Edgington R, Bongrain A, et al. Boron‐doped nanocrystalline diamond microelectrode arrays monitor cardiac action potentials[J]. Advanced Healthcare Materials, 2014, 3(2): 283-289.
[94] Almquist BD, Melosh NA. Fusion of biomimetic stealth probes into lipid bilayer cores[J]. Proceedings of the National Academy of Sciences, 2010, 107(13): 5815-5820.
[95] Dyer EL, Azar MG, Perich MG, et al. A cryptography-based approach for movement decoding[J]. Nature Biomedical Engineering, 2017, 1(12): 967-976.
[96] Ethier C, Acuna D, Solla SA, et al. Adaptive neuron-to-EMG decoder training for FES neuroprostheses[J]. Journal of Neural Engineering, 2016, 13(4): 1-16.
[97] Nurmikko AV. Approaches to large scale neural recording by chronic implants for mobile BCIs[C]// 2018 6th International Conference on Brain-Computer Interface (BCI). Ganwon: IEEE, 2018: 1-2.
[98] Yin M, Li H, Bull C, et al. An externally head-mounted wireless neural recording device for laboratory animal research and possible human clinical use[C]// 2013 35th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC). Osaka: IEEE, 2013: 3109-3114.
[99] Yin M, Borton DA, Aceros J, et al. A 100-channel hermetically sealed implantable device for chronic wireless neurosensing applications[J]. IEEE Transactions on Biomedical Circuits and Systems, 2013, 7(2): 115-128.
[100] Tsai D, John E, Chari T, et al. High-channel-count, high-density microelectrode array for closed-loop investigation of neuronal networks[C]// 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society. Milan: IEEE, 2015: 7510-7513.
[101] Wu H, Lekas M, Davies R, et al. Integrated transformers with magnetic thin films[J]. IEEE Transactions on Magnetics, 2016, 52(7): 1-4.
[102] Edrees HM, Colón-Berrios AR, De Godoy Peixoto D, et al. Monolithically Integrated CMOS-SMR Oscillator in 65 nm CMOS Using Custom MPW Die-Level Fabrication Process[J]. Journal of Microelectromechanical Systems, 2017, 26(4): 846-858.
[103] Tsai D, Yuste R, Shepard KL. Statistically reconstructed multiplexing for very dense, high-channel-count acquisition systems[J]. IEEE Transactions on Biomedical Circuits and Systems, 2018, 12(1): 13-23.
[104] Tsai D, Sawyer D, Bradd A, et al. A very large-scale microelectrode array for cellular-resolution electrophysiology[J]. Nature Communications, 2017, 8(1): 1-11.
[105] Szobota S, Gorostiza P, Del Bene F, et al. Remote control of neuronal activity with a light-gated glutamate receptor[J]. Neuron, 2007, 54(4): 535-545.
[106] Del Bene F, Wyart C, Robles E, et al. Filtering of visual information in the tectum by an identified neural circuit[J]. Science, 2010, 330(6004): 669-673.
[107] Berry MH, Holt A, Levitz J, et al. Restoration of patterned vision with an engineered photoactivatable G protein-coupled receptor[J]. Nature Communications, 2017, 8(1): 1-12.
[108] Shemesh OA, Tanese D, Zampini V, et al. Temporally precise single-cell-resolution optogenetics[J]. Nature Neuroscience, 2017, 20(12): 1796-1806.
[109] Waller L, Tian L. Computational imaging: machine learning for 3D microscopy[J]. Nature, 2015, 523(7561): 416-417.
[110] Pégard NC, Liu HY, Antipa N, et al. Compressive light-field microscopy for 3D neural activity recording[J]. Optica, 2016, 3(5): 517-524.
[111] Mardinly AR, Oldenburg IA, Pégard NC, et al. Precise multimodal optical control of neural ensemble activity[J]. Nature Neuroscience, 2018, 21(6): 881-893.
