Alterations in Hippocampal Network Activity after In Vitro Traumatic Brain Injury

Journal of Neurotrauma

Volumn 32, Issue 13, 2015, Pages 1011-1019

  Kang, Woo Hyeun ^a   Cao, Wenzhe ^b   Graudejus, Oliver ^b,c   Patel, Tapan P ^d   Wagner, Sigurd ^b   Meaney, David F ^d   Morrison, Barclay ^a  

^a Department of Earth and Environmental Sciences   (United States)

^b Princeton University   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

electrophysiology; hippocampus; network synchronization; traumatic brain injury

Indexed keywords

BICUCULLINE; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; FOLLOW UP; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL NETWORK ACTIVITY; HIPPOCAMPUS; IN VITRO STUDY; MECHANICAL STIMULATION; MICROARRAY ANALYSIS; NERVE CELL NECROSIS; NERVE CELL NETWORK; NONHUMAN; RAT; SLICE CULTURE; STRETCHABLE MICROELECTRODE ARRAY; TRAUMATIC BRAIN INJURY; ANIMAL; BRAIN INJURY; DRUG EFFECTS; ELECTROPHYSIOLOGY; MICROELECTRODE; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BICUCULLINE; BRAIN INJURIES; ELECTROPHYSIOLOGICAL PROCESSES; GABA-A RECEPTOR ANTAGONISTS; HIPPOCAMPUS; IN VITRO TECHNIQUES; MICROELECTRODES; NERVE NET; NEURONS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84932610307     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2014.3667     Document Type: Article

References (58)

1. Gean, A.D., and Fischbein, N.J. (2010). Head trauma. Neuroimaging Clin. N. Am. 20, 527-556.
2. Hyder, A.A., Wunderlich, C.A., Puvanachandra, P., Gururaj, G., and Kobusingye, O.C. (2007). The impact of traumatic brain injuries: a global perspective. NeuroRehabilitation 22, 341-353.
3. Faul, M., Xu, L., Wald, M.M., Coronado, V., and Dellinger, A.M. (2010). Traumatic Brain Injury in the United States: National Estimates of Prevalence and Incidence, 2002-2006. Injury Prev. 16, A268-A268.
4. Kinnunen, K.M., Greenwood, R., Powell, J.H., Leech, R., Hawkins, P.C., Bonnelle, V., Patel, M.C., Counsell, S.J., and Sharp, D.J. (2011). White matter damage and cognitive impairment after traumatic brain injury. Brain 134, 449-463.
5. Christidi, F., Bigler, E.D., McCauley, S.R., Schnelle, K.P., Merkley, T.L., Mors, M.B., Li, X., Macleod, M., Chu, Z., Hunter, J.V., Levin, H.S., Clifton, G.L., and Wilde, E.A. (2011). Diffusion tensor imaging of the perforant pathway zone and its relation to memory function in patients with severe traumatic brain injury. J. Neurotrauma 28, 711-725.
6. Ommaya, A.K., and Gennarelli, T.A. (1974). Cerebral concussion and traumatic unconsciousness. Correlation of experimental and clinical observations of blunt head injuries. Brain 97, 633-654.
7. Fujimoto, S.T., Longhi, L., Saatman, K.E., Conte, V., Stocchetti, N., and McIntosh, T.K. (2004). Motor and cognitive function evaluation following experimental traumatic brain injury. Neurosci. Biobehav. Rev. 28, 365-378.
8. Margulies, S.S., and Thibault, L.E. (1989). An analytical model of traumatic diffuse brain injury. J. Biomech. Eng. 111, 241-249.
9. Asikainen, I., Kaste, M., and Sarna, S. (1999). Early and late post-traumatic seizures in traumatic brain injury rehabilitation patients: brain injury factors causing late seizures and influence of seizures on long-term outcome. Epilepsia 40, 584-589.
10. Sosin, D.M., Sniezek, J.E., and Waxweiler, R.J. (1995). Trends in death associated with traumatic brain injury, 1979 through 1992. Success and failure. JAMA 273, 1778-1780.
11. Hoskison, M.M., Moore, A.N., Hu, B., Orsi, S., Kobori, N., and Dash, P.K. (2009). Persistent working memory dysfunction following traumatic brain injury: evidence for a time-dependent mechanism. Neuroscience 159, 483-491.
12. Wang, X.J. (2001). Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci. 24, 455-463.
13. Buzsaki, G. (1989). Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 31, 551-570.
14. Kobori, N., and Dash, P.K. (2006). Reversal of brain injury-induced prefrontal glutamic acid decarboxylase expression and working memory deficits by D1 receptor antagonism. J. Neurosci. 26, 4236-4246.
15. Levin, H.S., Hanten, G., Chang, C.C., Zhang, L., Schachar, R., Ewing- Cobbs, L., and Max, J.E. (2002). Working memory after traumatic brain injury in children. Ann. Neurol. 52, 82-88.
16. McAllister, T.W., Saykin, A.J., Flashman, L.A., Sparling, M.B., Johnson, S.C., Guerin, S.J., Mamourian, A.C., Weaver, J.B., and Yanofsky, N. (1999). Brain activation during working memory 1 month after mild traumatic brain injury: a functional MRI study. Neurology 53, 1300-1308.
17. Yu, Z., and Morrison, B. 3rd. (2010). Experimental mild traumatic brain injury induces functional alteration of the developing hippo-campus. J. Neurophysiol. 103, 499-510.
18. Elkin, B.S., and Morrison, B. 3rd. (2007). Region-specific tolerance criteria for the living brain. Stapp Car Crash J. 51, 127-138.
19. Cater, H.L., Sundstrom, L.E., and Morrison, B. 3rd. (2006). Temporal development of hippocampal cell death is dependent on tissue strain but not strain rate. J. Biomech. 39, 2810-2818.
20. Viano, D.C., Casson, I.R., Pellman, E.J., Zhang, L., King, A.I., and Yang, K.H. (2005). Concussion in professional football: brain responses by finite element analysis: part 9. Neurosurgery 57, 891-916; discussion, 891-916.
21. Kleiven, S. (2007). Predictors for traumatic brain injuries evaluated through accident reconstructions. Stapp Car Crash J. 51, 81-114.
22. Hardy, W.N., Mason, M.J., Foster, C.D., Shah, C.S., Kopacz, J.M., Yang, K.H., King, A.I., Bishop, J., Bey, M., Anderst, W., and Tashman, S. (2007). A study of the response of the human cadaver head to impact. Stapp Car Crash J. 51, 17-80.
23. Bayly, P.V., Cohen, T.S., Leister, E.P., Ajo, D., Leuthardt, E.C., and Genin, G.M. (2005). Deformation of the human brain induced by mild acceleration. J. Neurotrauma 22, 845-856.
24. Bayly, P.V., Black, E.E., Pedersen, R.C., Leister, E.P., and Genin, G.M. (2006). In vivo imaging of rapid deformation and strain in an animal model of traumatic brain injury. J. Biomech. 39, 1086-1095.
25. Morrison, B. 3rd, Elkin, B.S., Dolle, J.P., and Yarmush, M.L. (2011). In vitro models of traumatic brain injury. Annu. Rev. Biomed. Eng. 13, 91-126.
26. Morrison, B. 3rd, Saatman, K.E., Meaney, D.F., and McIntosh, T.K. (1998). In vitro central nervous system models of mechanically induced trauma: a review. J. Neurotrauma 15, 911-928.
27. Beggs, J.M., and Plenz, D. (2004). Neuronal avalanches are diverse and precise activity patterns that are stable for many hours in cortical slice cultures. J. Neurosci. 24, 5216-5229.
28. Arnold, F.J., Hofmann, F., Bengtson, C.P., Wittmann, M., Vanhoutte, P., and Bading, H. (2005). Microelectrode array recordings of cultured hippocampal networks reveal a simple model for transcription and protein synthesis-dependent plasticity. J. Physiol. 564, 3-19.
29. Kralik, J.D., Dimitrov, D.F., Krupa, D.J., Katz, D.B., Cohen, D., and Nicolelis, M.A. (2001). Techniques for long-term multisite neuronal ensemble recordings in behaving animals. Methods 25, 121-150.
30. Doetsch, G.S. (2000). Patterns in the brain. Neuronal population coding in the somatosensory system. Physiol. Behav. 69, 187-201.
31. Yu, Z., Graudejus, O., Tsay, C., Lacour, S.P., Wagner, S., and Morrison, B. 3rd. (2009). Monitoring hippocampus electrical activity in vitro on an elastically deformable microelectrode array. J. Neurotrauma 26, 1135-1145.
32. Matsuyama, S., Taniguchi, T., Kadoyama, K., and Matsumoto, A. (2008). Long-term potentiation-like facilitation through GABAA receptor blockade in the mouse dentate gyrus in vivo. Neuroreport 19, 1809-1813.
33. Sloviter, R.S. (1994). On the relationship between neuropathology and pathophysiology in the epileptic hippocampus of humans and experimental animals. Hippocampus 4, 250-253.
34. De Curtis, M., Biella, G., Forti, M., and Panzica, F. (1994). Multifocal spontaneous epileptic activity induced by restricted bicuculline ejection in the piriform cortex of the isolated guinea pig brain. J. Neurophysiol. 71, 2463-2476.
35. Li, X., Zhou, W., Zeng, S., Liu, M., and Luo, Q. (2007). Long-term recording on multi-electrode array reveals degraded inhibitory connection in neuronal network development. Biosens. Bioelectron. 22, 1538-1543.
36. Sundstrom, L., Morrison, B. 3rd, Bradley, M. and Pringle, A. (2005). Organotypic cultures as tools for functional screening in the CNS. Drug Discov. Today 10, 993-1000.
37. Lacour, S.P., Wagner, S., Huang, Z.Y., and Suo, Z. (2003). Stretchable gold conductors on elastomeric substrates. Appl. Phys. Lett. 82, 2404-2406.
38. Graudejus, O., Morrison, B., Goletiani, C., Yu, Z., and Wagner, S. (2012). Encapsulating elastically stretchable neural interfaces: yield, resolution, and recording/stimulation of neural activity. Adv. Funct. Mater. 22, 640-651.
39. Tsay, C., Lacour, S.P., Wagner, S., and Morrison, B. (2005). Architecture, fabrication, and properties of stretchable micro-electrode arrays. Proc. 4th IEEE Conf. Sensors, 1169-1172.
40. Graudejus, O., Yu, Z., Jones, J., Morrison, B., and Wagner, S. (2009). Characterization of an elastically stretchable microelectrode array and its application to neural field potential recordings. J. Electrochem. Soc. 156, P85-P94.
41. Morrison, B. 3rd, Cater, H.L., Benham, C.D., and Sundstrom, L.E. (2006). An in vitro model of traumatic brain injury utilising two-dimensional stretch of organotypic hippocampal slice cultures. J. Neurosci. Methods 150, 192-201.
42. Egert, U., and Meyer, T. (2005). Heart on a chip-extracellular multielectrode recordings from cardiac myocytes in vitro, in: Practical Methods in Cardiovascular Research. S. Dhein, F. Mohr, and M. Delmar (eds). Springer: Berlin; Heidelberg, pps. 432-453.
43. Effgen, G.B., Hue, C.D., Vogel, E. 3rd, Panzer, M.B., Meaney, D.F., Bass, C.R. and Morrison, B. 3rd. (2012). A multiscale approach to blast neurotrauma modeling: part II: methodology for inducing blast injury to in vitro models. Front. Neurol. 3, 23.
44. Morrison, B. 3rd, Cater, H.L., Wang, C.C., Thomas, F.C., Hung, C.T., Ateshian, G.A., and Sundstrom, L.E. (2003). A tissue level tolerance criterion for living brain developed with an in vitro model of traumatic mechanical loading. Stapp Car Crash J. 47, 93-105.
45. Novak, J.L., and Wheeler, B.C. (1988). Multisite hippocampal slice recording and stimulation using a 32 element microelectrode array. J. Neurosci. Methods 23, 149-159.
46. Choi, J.H., Jung, H.K., and Kim, T. (2006). A new action potential detector using the MTEO and its effects on spike sorting systems at low signal-to-noise ratios. IEEE Trans. Biomed. Eng. 53, 738-746.
47. Pimashkin, A., Kastalskiy, I., Simonov, A., Koryagina, E., Mukhina, I., and Kazantsev, V. (2011). Spiking signatures of spontaneous activity bursts in hippocampal cultures. Front. Comput Neurosci. 5, 46.
48. Li, X., Cui, D., Jiruska, P., Fox, J.E., Yao, X., and Jefferys, J.G. (2007). Synchronization measurement of multiple neuronal populations. J. Neurophysiol. 98, 3341-3348.
49. Li, X., Ouyang, G., Usami, A., Ikegaya, Y., and Sik, A. (2010). Scalefree topology of the CA3 hippocampal network: a novel method to analyze functional neuronal assemblies. Biophys. J. 98, 1733-1741.
50. Patel, T.P., Ventre, S.C., and Meaney, D.F. (2012). Dynamic changes in neural circuit topology following mild mechanical injury in vitro. Ann. Biomed. Eng. 40, 23-36.
51. Bahner, F., Weiss, E.K., Birke, G., Maier, N., Schmitz, D., Rudolph, U., Frotscher, M., Traub, R.D., Both, M., and Draguhn, A. (2011). Cellular correlate of assembly formation in oscillating hippocampal networks in vitro. Proc. Natl. Acad. Sci. U. S. A. 108, E607-E616.
52. Sharp, D.J., Scott, G., and Leech, R. (2014). Network dysfunction after traumatic brain injury. Nat. Rev. Neurol. 10, 156-166.
53. Tsirka, V., Simos, P.G., Vakis, A., Kanatsouli, K., Vourkas, M., Erimaki, S., Pachou, E., Stam, C.J., and Micheloyannis, S. (2011). Mild traumatic brain injury: graph-model characterization of brain networks for episodic memory. Int. J. Psychophysiol. 79, 89-96.
54. Stam, C.J., Jones, B.F., Nolte, G., Breakspear, M., and Scheltens, P. (2007). Small-world networks and functional connectivity in Alzheimer's disease. Cereb. Cortex 17, 92-99.
55. Stam, C.J., de Haan, W., Daffertshofer, A., Jones, B.F., Manshanden, I., van Cappellen van Walsum, A.M., Montez, T., Verbunt, J.P., de Munck, J.C., van Dijk, B.W., Berendse, H.W., and Scheltens, P. (2009). Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease. Brain 132, 213-224.
56. Bonislawski, D.P., Schwarzbach, E.P., and Cohen, A.S. (2007). Brain injury impairs dentate gyrus inhibitory efficacy. Neurobiol. Dis. 25, 163-169.
57. Wang, W., and Xu, T.L. (2006). Chloride homeostasis differentially affects GABA(A) receptor- and glycine receptor-mediated effects on spontaneous circuit activity in hippocampal cell culture. Neurosci. Lett. 406, 11-16.
58. Leinekugel, X., Khalilov, I., McLean, H., Caillard, O., Gaiarsa, J.L., Ben-Ari, Y., and Khazipov, R. (1999). GABA is the principal fastacting excitatory transmitter in the neonatal brain. Adv. Neurol. 79, 189-201.