A comparison of neuroinflammation to implanted microelectrodes in rat and mouse models

Biomaterials

Volumn 35, Issue 22, 2014, Pages 5637-5646

  Potter Baker, Kelsey A ^a,b   Ravikumar, Madhumitha ^a,b   Burke, Alan A ^a   Meador, William D ^a   Householder, Kyle T ^a,b   Buck, Amy C ^a,b   Sunil, Smrithi ^a,b   Stewart, Wade G ^a   Anna, Jake P ^a   Tomaszewski, William H ^a   Capadona, Jeffrey R ^a,b  

^a Case Western Reserve University   (United States)

^b LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

Author keywords

Animal models; Brain; Microelectrode; Neuroinflammation

Indexed keywords

BRAIN; RATS;

ANIMAL MODEL; GENETIC ALTERATIONS; MECHANISTIC PATHWAYS; NEUROINFLAMMATION; PHYSIOLOGICAL DIFFERENCES; POST-IMPLANTATION; SURGICAL METHOD; TRANSGENIC MICE;

MICROELECTRODES;

CD68 ANTIGEN; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN G ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE COURSE; IMMUNOHISTOCHEMISTRY; IMPLANTATION; MICROELECTRODE; MOUSE; NERVE CELL; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; RAT; TRANSGENIC MOUSE; ANIMAL; ASTROCYTE; BRAIN; DISEASE MODEL; ELECTRODE IMPLANT; ENCEPHALITIS; IMMUNOLOGY; INFLAMMATION; MACROPHAGE; MICROGLIA;

ANIMALIA; MUS MUSCULUS; RATTUS;

ANIMALS; ASTROCYTES; BRAIN; DISEASE MODELS, ANIMAL; ELECTRODES, IMPLANTED; ENCEPHALITIS; INFLAMMATION; MACROPHAGES; MICE; MICROGLIA; RATS;

EID: 84899980137     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.03.076     Document Type: Article

References (62)

1. Schwartz A.B. Cortical neural prosthetics. Annu Rev Neurosci 2004, 27:487-507.
2. Cogan S.F. Neural stimulation and recording electrodes. Annu Rev Biomed Eng 2008, 10:275-309.
3. Duffau H. Brain mapping in tumors: intraoperative or extraoperative?. Epilepsia 2013, 54:79-83.
4. Oakes T.R., Pizzagalli D.A., Hendrick A.M., Horras K.A., Larson C.L., Abercrombie H.C., et al. Functional coupling of simultaneous electrical and metabolic activity in the human brain. Hum Brain Mapp 2004, 21:257-270.
5. Anderson M.L. Neural reuse: a fundamental organizational principle of the brain. Behav Brain Sci 2010, 33:245-266.
6. Carlson K.S., Xia C.Z., Wesson D.W. Encoding and representation of intranasal CO2 in the mouse olfactory cortex. JNeurosci 2013, 33:13873-13881.
7. Kim S.P., Simeral J.D., Hochberg L.R., Donoghue J.P., Black M.J. Neural control of computer cursor velocity by decoding motor cortical spiking activity in humans with tetraplegia. JNeural Eng 2008, 5:455-476.
8. Simeral J.D., Kim S.P., Black M.J., Donoghue J.P., Hochberg L.R. Neural control of cursor trajectory and click by a human with tetraplegia 1000 days after implant of an intracortical microelectrode array. JNeural Eng 2011, 8:025027.
9. Hochberg L.R., Bacher D., Jarosiewicz B., Masse N.Y., Simeral J.D., Vogel J., et al. Reach and grasp by people with tetraplegia using a neurally controlled robotic arm. Nature 2012, 485:372-375.
10. Tresco P.A., Winslow B.D. The challenge of integrating devices into the central nervous system. Crit Rev Biomed Eng 2011, 39:29-44.
11. He W., Bellamkonda R.V. Amolecular perspective on understanding and modulating the performance of chronic central nervous system (CNS) recording electrodes. Indwelling neural implants: strategies for contending with the invivo environment 2008, CRC Press. W. Reichert (Ed.).
12. Barrese J.C., Rao N., Paroo K., Triebwasser C., Vargas-Irwin C., Franquemont L., et al. Failure mode analysis of silicon-based intracortical microelectrode arrays in non-human primates. JNeural Eng 2013, 10:066014.
13. Prasad A., Xue Q.S., Sankar V., Nishida T., Shaw G., Streit W.J., et al. Comprehensive characterization and failure modes of tungsten microwire arrays in chronic neural implants. JNeural Eng 2012, 9:056015.
14. Verhagen J.V., Gabbott P.L., Rolls E.T. Asimple method for reconditioning epoxy-coated microelectrodes for extracellular single neuron recording. JNeurosci Methods 2003, 123:215-217.
15. Biran R., Martin D., Tresco P. Neuronal cell loss accompanies the brain tissue response to chronically implanted silicon microelectrode arrays. Exp Neurol 2005, 195:115-126.
16. Moshayedi P, Ng G, Kwok JCF, Yeo GSH, Bryant CE, Fawcett JW, etal. The relationship between glial cell mechanosensitivity and foreign body reactions in the central nervous system. Biomaterials.
17. Karumbaiah L., Norman S.E., Rajan N.B., Anand S., Saxena T., Betancur M., et al. The upregulation of specific interleukin (IL) receptor antagonists and paradoxical enhancement of neuronal apoptosis due to electrode induced strain and brain micromotion. Biomaterials 2012, 33:5983-5996.
18. Skousen J., Bolick K., Bridge M., Tresco P. Apredictive model of the foreign body response to devices implanted chronically in the central nervous system 2012, IFESS, Banff, Alberta, Canada.
19. Potter K.A., Buck A.C., Self W.K., Callanan M.E., Sunil S., Capadona J.R. The effect of resveratrol on neurodegeneration and blood brain barrier stability surrounding intracortical microelectrodes. Biomaterials 2013, 34:7001-7015.
20. He W., McConnell G.C., Schneider T.M., Bellamkonda R.V. Anovel anti-inflammatory surface for neural electrodes. Adv Mater 2007, 19:3529-3533.
21. Potter K.A., Buck A.C., Self W.K., Capadona J.R. Stab injury and device implantation within the brain results in inversely multiphasic neuroinflammatory and neurodegenerative responses. JNeural Eng 2012, 9:046020.
22. Mokarram N., Bellamkonda R.V. Aperspective on immunomodulation and tissue repair. Ann Biomed Eng 2013, 42:338-351.
23. Mokarram N., Bellamkonda R.V. Overcoming endogenous constraints on neuronal regeneration. IEEE Trans Biomed Eng 2010, 58:1900-1906.
24. Cramer P.E., Cirrito J.R., Wesson D.W., Lee C.Y.D., Karlo J.C., Zinn A.E., et al. ApoE-Directed therapeutics rapidly clear -amyloid and reverse deficits in AD mouse models. Science 2012, 335:1503-1506.
25. Han S., Choi J.R., Soon Shin K., Kang S.J. Resveratrol upregulated heat shock proteins and extended the survival of G93A-SOD1 mice. Brain Res 2012, 1483:112-117.
26. Murakami K., Murata N., Noda Y., Tahara S., Kaneko T., Kinoshita N., et al. SOD1 deficiency drives amyloid oligomerization and memory loss in a mouse model of Alzheimer's disease. JBiol Chem 2011, 286:44557-44568.
27. Liao B., Zhao W., Beers D.R., Henkel J.S., Appel S.H. Transformation from a neuroprotective to a neurotoxic microglial phenotype in a mouse model of ALS. Exp Neurol 2012, 237:147-152.
28. Ravikumar M., Hageman D.J., Tomaszewski W.H., Chandra G.M., Skousen J.L., Capadona J.R. The effect of residual endotoxin contamination on the neuroinflammatory response to sterilized intracortical microelectrodes. JMater Chem B 2014, 2(17):2517-2529.
29. Potter K.A., Simon J.S., Velagapudi B., Capadona J.R. Reduction of autofluorescence at the microelectrode-cortical tissue interface improves antibody detection. JNeurosci Methods 2012, 203:96-105.
30. McConnell G.C., Rees H.D., Levey A.I., Gutekunst C.-A., Gross R.E., Bellamkonda R.V. Implanted neural electrodes cause chronic, local inflammation that is correlated with local neurodegeneration. JNeural Eng 2009, 6:056003.
31. Polikov V., Tresco P., Reichert W. Response of brain tissue to chronically implanted neural electrodes. JNeurosci Methods 2005, 148:1-18.
32. Zhong Y., Bellamkonda R. Dexamethasone-coated neural probes elicit attenuated inflammatory response and neuronal loss compared to uncoated neural probes. Brain Res 2007, 1148:15-27.
33. Azemi E., Lagenaur C.F., Cui X.T. The surface immobilization of the neural adhesion molecule L1 on neural probes and its effect on neuronal density and gliosis at the probe/tissue interface. Biomaterials 2011, 32:681-692.
34. Dijkstra C., Dopp E., Joling P., Kraal G. The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 1985, 54:589-599.
35. Frampton J.P., Hynd M.R., Shuler M.L., Shain W. Effects of glial cells on electrode impedance recorded from neural prosthetic devices invitro. Ann Biomed Eng 2010, 38:1031-1047.
36. Aschner M., Sonnewald U., Tan K.H. Astrocyte modulation of neurotoxic injury. Brain Pathol 2002, 12:475-481.
37. Raff M.C., Abney E.R., Cohen J., Lindsay R., Noble M. Two types of astrocytes in cultures of developing rat white matter: differences in morphology, surface gangliosides, and growth characteristics. JNeurosci 1963, 3:1289-1300.
38. Saxena T., Karumbaiah L., Gaupp E.A., Patkar R., Patil K., Betancur M., et al. The impact of chronic blood-brain barrier breach on intracortical electrode function. Biomaterials 2013, 34:4703-4713.
39. Winslow B.D., Christensen M.B., Yang W.-K., Solzbacher F., Tresco P.A. Acomparison of the tissue response to chronically implanted Parylene-C-coated and uncoated planar silicon microelectrode arrays in rat cortex. Biomaterials 2010, 31:9163-9172.
40. Buzsáki G. Large-scale recording of neuronal ensembles. Nat Neurosci 2004, 7:446-451.
41. Mullen R.J., Buck C.R., Smith A.M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 1992, 116:201-211.
42. Rennaker R.L., Miller J., Tang H., Wilson D.A. Minocycline increases quality and longevity of chronic neural recordings. JNeural Eng 2007, 4:L1-L5.
43. Shain W., Spataro L., Dilgen J., Haverstick K., Retterer S., Isaacson M., et al. Controlling cellular reactive responses around neural prosthetic devices using peripheral and local intervention strategies. IEEE Trans Neural Syst Rehabil Eng 2003, 11:186-188.
44. Winslow B.D., Tresco P.A. Quantitative analysis of the tissue response to chronically implanted microwire electrodes in rat cortex. Biomaterials 2010, 31:1558-1567.
45. Wu J., Glimcher L.H., Aliprantis A.O. HCO3-/Cl- anion exchanger SLC4A2 is required for proper osteoclast differentiation and function. Proc Natl Acad Sci 2008, 105:16934-16939.
46. Pintado C., Revilla E., Vizuete M.L., Jiménez S., García-Cuervo L., Vitorica J., et al. Regional difference in inflammatory response to LPS-injection in the brain: role of microglia cell density. JNeuroimmunol 2011, 238:44-51.
47. Savchenko V.L., McKanna J.A., Nikonenko I.R., Skibo G.G. Microglia and astrocytes in the adult rat brain: comparative immunocytochemical analysis demonstrates the efficacy of lipocortin 1 immunoreactivity. Neuroscience 2000, 96:195-203.
48. Savchenko V.L., Nikonenko I.R., Skibo G.G., McKanna J.A. Distribution of microglia and astrocytes in different regions of the normal adult rat brain. Neurophysiology 1997, 29:343-351.
49. Ito D., Imai Y., Ohsawa K., Nakajima K., Fukuuchi Y., Kohsaka S. Microglia-specific localisation of a novel calcium binding protein, Iba1. Mol Brain Res 1998, 57:1-9.
50. DeFelipe J. The evolution of the brain, the human nature of cortical circuits, and intellectual creativity. Front Neuroanat 2011, 5:1-17.
51. Woolley A.J., Desai H.A., Otto K.J. Chronic intracortical microelectrode arrays induce non-uniform, depth-related tissue responses. JNeural Eng 2013, 10:026007.
52. Fawcett J.W., Asher R.A. The glial scar and central nervous system repair. Brain Res Bull 1999, 49:377-391.
53. Silver J., Miller J.H. Regeneration beyond the glial scar. Nat Rev Neurosci 2004, 5:146-156.
54. Sofroniew M.V. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 2009, 32:638-647.
55. Harris J.P., Capadona J.R., Miller R.H., Healy B.C., Shanmuganathan K., Rowan S.J., et al. Mechanically adaptive intracortical implants improve the proximity of neuronal cell bodies. JNeural Eng 2011, 8:066011.
56. McConnell G.C., Schneider T.M., Owens D.J., Bellamkonda R.V. Extraction force and cortical tissue reaction of silicon microelectrode arrays implanted in the rat brain. IEEE Trans Biomed Eng 2007, 54:1097-1107.
57. Abbott N.J. Inflammatory mediators and modulation of blood-brain barrier Permeability. Cell Mol Neurobiol 2000, 20:131-147.
58. Abbott N.J., Rönnbäck L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006, 7:41-53.
59. Kawano H., Kimura-Kuroda J., Komuta Y., Yoshioka N., Li H.P., Kawamura K., et al. Role of the lesion scar in the response to damage and repair of the central nervous system. Cell Tissue Res 2012, 349:169-180.
60. Aihara N., Tanno H., Hall J.J., Pitts L.H., Noble L.J. Immunocytochemical localization of immunoglobulins in the rat brain: relationship to the blood-brain barrier. JComp Neurol 1994, 342:481-496.
61. Szarowski D. Brain responses to micro-machined silicon devices. Brain Res 2003, 983:23-35.
62. Paxinos G, Watson C. The rat brain in stereotaxic coordinates: Academic Press.