Midbrain raphe stimulation improves behavioral and anatomical recovery from fluid-percussion brain injury

Journal of Neurotrauma

Volumn 30, Issue 2, 2013, Pages 119-130

  Gonzalez, Melissa M Carballos ^a   Blaya, Meghan O ^a   Alonso, Ofelia F ^a   Bramlett, Helen M ^a,b   Hentall, Ian D ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

cAMP; deep brain stimulation; forebrain trauma; forelimb reaching; neuroanatomical volume; water maze

Indexed keywords

CYCLIC AMP;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN SIZE; CONTROLLED STUDY; CORPUS CALLOSUM; DORSAL RAPHE NUCLEUS; EXTERNAL CAPSULE; FLUID PERCUSSION BRAIN INJURY; HISTOPATHOLOGY; LIMB MOVEMENT; MALE; MAZE TEST; MEDIAN RAPHE NUCLEUS; NEUROANATOMY; NEUROPHYSIOLOGY; NONHUMAN; OCCIPITAL CORTEX; PARIETAL CORTEX; RAT; TRAUMATIC BRAIN INJURY; WHITE MATTER; WORKING MEMORY;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN INJURIES; CYCLIC AMP; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION THERAPY; ENZYME-LINKED IMMUNOSORBENT ASSAY; MALE; MAZE LEARNING; MICE; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION;

EID: 84872155350     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2499     Document Type: Article

References (61)

1. Jang, S.H. (2009). Review of motor recovery in patients with traumatic brain injury. NeuroRehabilitation 24, 349-353.
2. Wagner, A.K. and Zitelli, K.T. (2012). A Rehabilomics focused perspective on molecular mechanisms underlying neurological injury, complications, and recovery after severe TBI. Pathophysiology Mar.E-pub ahead of print.
3. Garcia, A.N., Shah, M.A., Dixon, C.E., Wagner, A.K., and Kline, A.E. (2011). Biologic and plastic effects of experimental traumatic brain injury treatment paradigms and their relevance to clinical rehabilitation. PM. R. 3, Suppl. 1, S18-S27.
4. Liepert, J. (2008). Pharmacotherapy in restorative neurology. Curr. Opin. Neurol. 21, 639-643.
5. Richardson, R.M., Singh, A., Sun, D., Fillmore, H.L., Dietrich, D.W., 3rd, and Bullock, M.R. (2010). Stem cell biology in traumatic brain injury: effects of injury and strategies for repair. J. Neurosurg. 112, 1125-1138.
6. Xiong, Y., Mahmood, A., and Chopp, M. (2010). Neurorestorative treatments for traumatic brain injury. Discov. Med. 10, 434-442.
7. Bramlett, H.M., and Dietrich, W.D. (2007). Progressive damage after brain and spinal cord injury: pathomechanisms and treatment strategies. Prog. Brain Res. 161, 125-141. (Pubitemid 47017402)
8. Avramescu, S., and Timofeev, I. (2008). Synaptic strength modulation after cortical trauma: a role in epileptogenesis. J. Neurosci. 28, 6760-6772.
9. Prince, D.A., Parada, I., Scalise, K., Graber, K., Jin, X., and Shen, F. (2009). Epilepsy following cortical injury: cellular and molecular mechanisms as targets for potential prophylaxis. Epilepsia 50, Suppl 2, 30-40.
10. Lenzlinger, P.M., Morganti-Kossmann, M.C., Laurer, H.L., and Mc-Intosh, T.K. (2001). The duality of the inflammatory response to traumatic brain injury. Mol Neurobiol 24, 169-181. (Pubitemid 34066684)
11. Ziebell, J.M., and Morganti-Kossmann, M.C. (2010). Involvement of pro-and anti-inflammatory cytokines and chemokines in the pathophysiology of traumatic brain injury. Neurotherapeutics 7, 22-30.
12. Cunningham, E.T., Jr., Wada, E., Carter, D.B., Tracey, D.E., Battey, J.F., and De Souza, E.B. (1992). In situ histochemical localization of type I interleukin-1 receptor messenger RNA in the central nervous system, pituitary, and adrenal gland of the mouse. J. Neurosci. 12, 1101-1114.
13. Kanjhan, R., Housley, G.D., Burton, L.D., Christie, D.L., Kippenberger, A., Thorne, P.R., Luo, L., and Ryan, A.F. (1999). Distribution of the P2X2 receptor subunit of the ATP-gated ion channels in the rat central nervous system. J. Comp. Neurol. 407, 11-32. (Pubitemid 29161990)
14. Langhans, W. (2007). Signals generating anorexia during acute illness. Proc Nutr Soc 66, 321-330.
15. Nakamura, K., Li, Y.Q., Kaneko, T., Katoh, H., and Negishi, M. (2001). Prostaglandin EP3 receptor protein in serotonin and catecholamine cell groups: a double immunofluorescence study in the rat brain. Neuroscience 103, 763-775. (Pubitemid 32239340)
16. Molliver, M.E. (1987). Serotonergic neuronal systems: what their anatomic organization tells us about function. J. Clin. Psychopharmacol. 7, Suppl., 3S-23S. (Pubitemid 18014272)
17. Vertes, R.P., Fortin, W.J., and Crane, A.M. (1999). Projections of the median raphe nucleus in the rat. J. Comp. Neurol. 407, 555-582. (Pubitemid 29196671)
18. Azmitia, E.C. (2007). Serotonin and brain: evolution, neuroplasticity, and homeostasis. Int. Rev. Neurobiol. 77, 31-56.
19. Berger, M., Gray, J.A., and Roth, B.L. (2009). The expanded biology of serotonin. Annu. Rev. Med. 60, 355-366.
20. Turlejski, K. (1996). Evolutionary ancient roles of serotonin: longlasting regulation of activity and development. Acta Neurobiol. Exp. (Wars) 56, 619-636. (Pubitemid 26179691)
21. Hobson, S.A., Bacon, A., Elliot-Hunt, C.R., Holmes, F.E., Kerr, N.C., Pope, R., Vanderplank, P. and Wynick, D. (2010). Galanin acts as a trophic factor to the central and peripheral nervous systems. EXS. 102, 25-38.
22. Hökfelt, T., Xu, Z.Q., Shi, T.J., Holmberg, K., and Zhang, X. (1998). Galanin in ascending systems. Focus on coexistence with 5-hydroxytryptamine and noradrenaline. Ann. N. Y. Acad. Sci. 863, 252-263. (Pubitemid 29047780)
23. Hentall, I.D., and Burns, S.B. (2009). Restorative effects of stimulating medullary raphe after spinal cord injury. J. Rehabil. Res. Dev. 46, 109-122.
24. Hentall, I.D., and Gonzalez, M.M. (2012). Promotion of recovery from thoracic spinal cord contusion in rats by stimulation of medullary raphe or its midbrain input. Neurorehabil. Neural. Repair 26, 374-384.
25. Bramlett, H.M., Green, E.J., and Dietrich, W.D. (1997). Hippocampally dependent and independent chronic spatial navigational deficits following parasagittal fluid percussion brain injury in the rat. Brain Res. 762, 195-202. (Pubitemid 27315949)
26. Thompson, H.J., Lifshitz, J., Marklund, N., Grady, M.S., Graham, D.I., Hovda, D.A., and McIntosh, T.K. (2005). Lateral fluid percussion brain injury: a 15-year review and evaluation. J. Neurotrauma 22, 42-75.
27. Sanders, M.J., Dietrich, W.D., and Green, E.J. (1999). Cognitive function following traumatic brain injury: effects of injury severity and recovery period in a parasagittal fluid-percussive injury model. J. Neurotrauma 16, 915-925. (Pubitemid 29491763)
28. D'Hooge, R., and De Deyn, P.P. (2001). Applications of the Morris water maze in the study of learning and memory. Brain Res. Brain Res. Rev. 36, 60-90. (Pubitemid 32763130)
29. Hamm, R.J., Temple, M.D., Pike, B.R., O'Dell, D.M., Buck, D.L., and Lyeth, B.G. (1996). Working memory deficits following traumatic brain injury in the rat. J. Neurotrauma 13, 317-323. (Pubitemid 26279353)
30. Schallert, T., Fleming, S.M., Leasure, J.L., Tillerson, J.L., and Bland, S.T. (2000). CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39, 777-787. (Pubitemid 30103682)
31. Vazey, E.M., Chen, K., Hughes, S.M., and Connor, B. (2006). Transplanted adult neural progenitor cells survive, differentiate and reduce motor function impairment in a rodent model of Huntington's disease. Exp. Neurol. 199, 384-396. (Pubitemid 43928967)
32. Dietrich, W.D., Ginsberg, M.D., and Busto, R. (1986). Effect of transient cerebral ischemia on metabolic activation of a somatosensory circuit. J. Cereb. Blood Flow Metab. 6, 405-413. (Pubitemid 16010623)
33. Passineau, M.J., Zhao, W., Busto, R., Dietrich, W.D., Alonso, O., Loor, J.Y., Bramlett, H.M., and Ginsberg, M.D. (2000). Chronic metabolic sequelae of traumatic brain injury: prolonged suppression of somatosensory activation. Am. J. Physiol. Heart Circ. Physiol. 279, H924-931.
34. Hentall, I.D., Zorman, G., Kansky, S., and Fields, H.L. (1984). Relations among threshold, spike height, electrode distance, and conduction velocity in electrical stimulation of certain medullospinal neurons. J. Neurophysiol. 51, 968-977. (Pubitemid 14104221)
35. Ranck, J.B., Jr. (1975). Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res. 98, 417-440.
36. Shannon, R.V., Moore, J.K., McCreery, D.B., and Portillo, F. (1997). Threshold-distance measures from electrical stimulation of human brainstem. IEEE Trans Rehabil Eng 5, 70-74. (Pubitemid 27186459)
37. Allers, K.A., and Sharp, T. (2003). Neurochemical and anatomical identification of fast-and slow-firing neurones in the rat dorsal raphe nucleus using juxtacellular labelling methods in vivo. Neuroscience 122, 193-204. (Pubitemid 37329958)
38. Kocsis, B., Varga, V., Dahan, L., and Sik, A. (2006). Serotonergic neuron diversity: identification of raphe neurons with discharges timelocked to the hippocampal theta rhythm. Proc. Natl. Acad. Sci. U. S. A. 103, 1059-1064. (Pubitemid 43212221)
39. Hentall, I.D., Pinzon, A., and Noga, B.R. (2006). Spatial and temporal patterns of serotonin release in the rat's lumbar spinal cord following electrical stimulation of the nucleus raphe magnus. Neuroscience 142, 893-903. (Pubitemid 44508710)
40. Jacobs, B.L., and Azmitia, E.C. (1992). Structure and function of the brain serotonin system. Physiol. Rev. 72, 165-229.
41. Vertes, R.P. (1991). A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J. Comp. Neurol. 313, 643-668.
42. Vertes, R.P., and Kocsis, B. (1994). Projections of the dorsal raphe nucleus to the brainstem: PHA-L analysis in the rat. J. Comp. Neurol. 340, 11-26. (Pubitemid 24036456)
43. Morris, R.G., Garrud, P., Rawlins, J.N., and O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683. (Pubitemid 12096189)
44. Sutherland, R.J., McDonald, R.J., Hill, C.R., and Rudy, J.W. (1989). Damage to the hippocampal formation in rats selectively impairs the ability to learn cue relationships. Behav. Neural Biology. 52, 331-356. (Pubitemid 20018614)
45. Whishaw, I.Q., and Kolb, B. (1984). Decortication abolishes place but not cue learning in rats. Behav. Brain Res. 11, 123-134. (Pubitemid 14190221)
46. Mokler, D.J., Dugal, J.R., Hoffman, J.M., and Morgane, P.J. (2009). Functional interrelations between nucleus raphe dorsalis and nucleus raphe medianus: a dual probe microdialysis study of glutamate-stimulated serotonin release. Brain Res. Bull. 78, 132-138.
47. Jackson, J., Dickson, C.T., and Bland, B.H. (2008). Median raphe stimulation disrupts hippocampal theta via rapid inhibition and statedependent phase reset of theta-related neural circuitry. J. Neurophysiol. 99, 3009-3026.
48. Williams, J.M., and Givens, B. (2003). Stimulation-induced reset of hippocampal theta in the freely performing rat. Hippocampus 13, 109-116. (Pubitemid 36305401)
49. Trulson, M.E., and Jacobs, B.L. (1979). Raphe unit activity in freely moving cats: correlation with level of behavioral arousal. Brain Res. 163, 135-150. (Pubitemid 9111292)
50. Urbain, N., Creamer, K., and Debonnel, G. (2006). Electrophysiological diversity of the dorsal raphe cells across the sleep-wake cycle of the rat. J. Physiol. 573, 679-695. (Pubitemid 43842510)
51. Meyer-Bernstein, E.L., and Morin, L.P. (1999). Electrical stimulation of the median or dorsal raphe nuclei reduces light-induced FOS protein in the suprachiasmatic nucleus and causes circadian activity rhythm phase shifts. Neuroscience 92, 267-279. (Pubitemid 29249037)
52. Mathias, J.L., and Alvaro, P.K. (2012). Prevalence of sleep disturbances, disorders, and problems following traumatic brain injury: A meta-analysis. Sleep Med. 13, 898-905.
53. Spencer, T., and Filbin, M.T. (2004). A role for cAMP in regeneration of the adult mammalian CNS. J. Anat. 204, 49-55. (Pubitemid 38128574)
54. Kitson, S.L. (2007). 5-hydroxytryptamine (5-HT) receptor ligands. Curr. Pharm. Des. 13, 2621-2637. (Pubitemid 47430438)
55. Raymond, J.R., Mukhin, Y.V., Gelasco, A., Turner, J., Collinsworth, G., Gettys, T.W., Grewal, J.S., and Garnovskaya, M.N. (2001). Multiplicity of mechanisms of serotonin receptor signal transduction. Pharmacol. Ther. 92, 179-212. (Pubitemid 34251133)
56. Atkins, C.M., Oliva, A.A., Jr., Alonso, O.F., Pearse, D.D., Bramlett, H.M., and Dietrich, W.D. (2007). Modulation of the cAMP signaling pathway after traumatic brain injury. Exp. Neurol. 208, 145-158. (Pubitemid 47600157)
57. Schiff, N.D., Giacino, J.T., Kalmar, K., Victor, J.D., Baker, K., Gerber, M., Fritz, B., Eisenberg, B., Biondi, T.,O'Connor, J., Kobylarz, E.J., Farris, S., Machado, A., McCagg, C., Plum, F., Fins, J.J., and Rezai, A.R. (2007). Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 448, 600-603. (Pubitemid 47206940)
58. Yamamoto, T., and Katayama, Y. (2005). Deep brain stimulation therapy for the vegetative state. Neuropsychol. Rehabil. 15, 406-413. (Pubitemid 41248346)
59. Adkins-Muir, D.L., and Jones, T.A. (2003). Cortical electrical stimulation combined with rehabilitative training: enhanced functional recovery and dendritic plasticity following focal cortical ischemia in rats. Neurol. Res. 25, 780-788. (Pubitemid 37499711)
60. Jackson, A., Mavoori, J., and Fetz, E.E. (2006). Long-term motor cortex plasticity induced by an electronic neural implant. Nature 444, 56-60. (Pubitemid 44684753)
61. Kringelbach, M.L., Jenkinson, N., Owen, S.L., and Aziz, T.Z. (2007). Translational principles of deep brain stimulation. Nat. Rev. Neurosci. 8, 623-635. (Pubitemid 47093935)