Innovative treatment approaches in schizophrenia enhancing neuroplasticity: Aerobic exercise, erythropoetin and repetitive transcranial magnetic stimulation

Current Pharmaceutical Biotechnology

Volumn 13, Issue 8, 2012, Pages 1595-1605

  Wobrock, T ^a   Hasan, A ^a   Falkai, P ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Endurance training; Erythropoetin; Exercise; Neuroprotection; Repetitive transcranial magnetic stimulation (rTMS); Schizophrenia

Indexed keywords

PLACEBO; RECOMBINANT ERYTHROPOIETIN;

AEROBIC CELL CULTURE; ARTICLE; CLINICAL TRIAL; COGNITION; HUMAN; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; SAMPLE SIZE; SCHIZOPHRENIA; SYNAPTOGENESIS; TRANSCRANIAL MAGNETIC STIMULATION;

ANIMALS; ERYTHROPOIETIN; EXERCISE; HUMANS; NEURONAL PLASTICITY; SCHIZOPHRENIA; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84862626002     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920112800784763     Document Type: Article

References (112)

1. Murray, C.J.; Lopez, A.D. Evidence-based health policy-lessons from the Global Burden of Disease Study. Science, 1996, 274, 740-743.
2. Hoff, A.L.; Sakuma, M.; Wieneke, M.; Horon, R.; Kushner, M.; DeLisi, L.E. Longitudinal neuropsychological follow-up study of patients with first-episode schizophrenia. Am. J. Psychiatry, 1999, 156, 1336-1341.
3. Heinrichs, R.W.; Zakzanis, K.K. Neurocognitive deficit in schizophrenia: a quantitative review of the evidence. Neuropsychology,1998, 12, 426-445.
4. Fleischhacker, W.W.; Cetkovich-Bakmas, M.; De Hert, M.; Hennekens, C.H.; Lambert, M.; Leucht, S.; Maj, M.; McIntyre, R.S.; Naber, D.; Newcomer, J.W.; Olfson, M.; Osby, U.; Sartorius, N.; Lieberman, J.A. Comorbid somatic illnesses in patients with severe mental disorders: clinical, policy, and research challenges. J. Clin. Psychiatry, 2008, 69, 514-519.
5. Falkai, P.; Wobrock, T.; Lieberman, J.; Glenthoj, B.; Gattaz, W.F.; Möller, H.J. World Federation of Societies of Biological Psychiatry (WFSBP) guidelines for biological treatment of schizophrenia, Part 1: acute treatment of schizophrenia. World J. Biol. Psychiatry, 2005, 6, 132-191.
6. Falkai, P.; Wobrock, T.; Lieberman, J.; Glenthoj, B.; Gattaz, W.F.; Möller, H.J. World Federation of Societies of Biological Psychiatry (WFSBP) guidelines for biological treatment of schizophrenia, part 2: long-term treatment of schizophrenia. World J. Biol. Psychiatry, 2006, 7, 5-40.
7. Seeman, P.; Guan, H.C. Phencyclidine and glutamate agonist LY379268 stimulate dopamine D2High receptors: D2 basis for schizophrenia. Synapse, 2008, 62, 819-828.
8. Delay, J.; Deniker, P. Neuroplegics in psychiatric therapy. Therapie, 1953, 8, 347-364.
9. Keefe, R.S. Cognitive deficits in patients with schizophrenia: effects and treatment. J. Clin. Psychiatry, 2007, 68(Suppl. 14), 8-13.
10. Falkai, P.; Schneider-Axmann, T.; Honer, W.G.; Vogeley, K.; Schönell, H.; Pfeiffer, U.; Scherk, H.; Block, W.; Träber, F.; Schild, H.H.; Maier, W.; Tepest, R. Influence of genetic loading, obstetric complications and premorbid adjustment on brain morphology in schizophrenia: a MRI study. Eur. Arch. Psychiatry Clin. Neurosci., 2003, 253, 92-99.
11. Wright, I.C.; Rabe-Hesketh, S.; Woodruff, P.W.; David, A.S.; Murray, R.M.; Bullmore, E.T. Meta-analysis of regional brain volumes in schizophrenia. Am. J. Psychiatry, 2000, 157, 16-25.
12. Ebner, F.; Tepest, R.; Dani, I., Pfeiffer, U.; Schulze, T.G.; Rietschel, M.; Maier, W.; Träber, F.; Block, W.; Schild, H.H.; Wagner, M.; Steinmetz, H.; Gaebel, W.; Honer, W.G.; Schneider-Axmann, T.; Falkai, P. The hippocampus in families with schizophrenia in relation to obstetric complications. Schizophr. Res., 2008, 104, 71-78.
13. Seidman, L.J.; Faraone, S.V.; Goldstein, J.M.; Kremen, W.S.; Horton, N.J.; Makris, N.; Toomey, R.; Kennedy, D.; Caviness, V.S.; Tsuang, M.T. Left hippocampal volume as a vulnerability indicator for schizophrenia: a magnetic resonance imaging morphometric study of nonpsychotic first-degree relatives. Arch. Gen. Psychiatry, 2002, 59, 839-849.
14. Harrison, P.J.; Weinberger, D.R. Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol. Psychiatry, 2005, 10, 40-68.
15. Schmitt, A.; Fendt, M.; Zink, M.; Ebert, U.; Starke, M.; Berthold, M.; Herb, A.; Petroianu, G.; Falkai, P.; Henn, F.A. Altered NMDA receptor expression and behavior following postnatal hypoxia: potential relevance to schizophrenia. J. Neural. Transm., 2007, 114, 239-248.
16. Wobrock, T.; Scherk, H.; Falkai, P. Magnetic resonance spectroscopy in schizophrenia. Possibilities and limitations. Radiologe, 2005, 45, 124-130.
17. Cahn, W.; Hulshoff Pol, H.E.; Bongers, M.; Schnack, H.G.; Mandl, R.C.; Van Haren, N.E.; Durston, S.; Koning, H. Van Der Linden, J.A.; Kahn, R.S. Brain morphology in antipsychotic-naïve schizophrenia: a study of multiple brain structures. Br. J. Psychiatry Suppl., 2002, 43, 66-72.
18. Cahn, W.; van Haren, N.E.; Hulshoff Pol, H.E.; Schnack, H.G.; Caspers, E.; Laponder, D.A.; Kahn, R.S. Brain volume changes in the first year of illness and 5-year outcome of schizophrenia. Br. J. Psychiatry, 2006, 189, 381-382.
19. Reif, A.; Fritzen, S.; Finger, M.; Strobel, A.; Lauer, M.; Schmitt, A.; Lesch, K.P. Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol. Psychiatry, 2006, 11, 514-522.
20. Arnold, S.E. Contributions of neuropathology to understanding schizophrenia in late life. Harv. Rev. Psychiatry, 2001, 9, 69-76.
21. Pereira, A.C.; Huddleston, D.E.; Brickman, A.M.; Sosunov, A.A.; Hen, R.; McKhann, G.M.; Sloan, R.; Gage, F.H.; Brown, T.R.; Small, S.A. An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. USA, 2007, 104, 5638-5643.
22. Krebs, M.; Leopold, K.; Hinzpeter, A.; Schaefer, M. Current schizophrenia drugs: efficacy and side effects. Expert Opin. Pharmacother., 2006, 7, 1005-1016.
23. Driemeyer, J.; Boyke, J.; Gaser, C.; Buchel, C.; May, A. Changesin gray matter induced by learning--revisited. PLoS One, 2008, 3, e2669.
24. Pascual-Leone, A.; MAmedi, A.; Fregni, F.; Merabet, L.B. The plastic human brain cortex. Ann. Rev. Neurosci., 2005, 28, 377-401.
25. Heckers, S.; Konradi, C. Hippocampal neurons in schizophrenia. J. Neural. Transm., 2002, 109, 891-905.
26. Sawada, K.; Barr, A.M.; Nakamura, M.; Arima, K.; Young, C.E.; Dwork, A.J.; Falkai, P.; Phillips, A.G.; Honer, W.G. Hippocampal complexin proteins and cognitive dysfunction in schizophrenia. Arch. Gen. Psychiatry, 2005, 62, 263-272.
27. Toni, N.; Teng, E.M.; Bushong, E.A.; Aimone, J.B.; Zhao, C.; Consiglio, A.; van Praag, H.; Martone, M.E.; Ellisman, M.H.; Gage, F.H. Synapse formation on neurons born in the adult hippocampus. Nat. Neurosci., 2007, 10, 727-734.
28. Reif, A.; Schmitt, A.; Fritzen, S.; Lesch, K.P. Neurogenesis and schizophrenia: dividing neurons in a divided mind? Eur. Arch. Psychiatry Clin. Neurosci., 2007, 257, 290-299.
29. Barr, A.M. Y.C.; Sawada, K.; Honer, W.G. Relevance of presynaptic proteins to neuropsychiatric disorders. In: Molecular Mechanism of Synaptogenesis; Dityatev, A., El-Husseini, A., Eds.; Springer: Berlin, 2006; pp. 391-408.
30. Ding, Q.; Vaynman, S.; Souda, P.; Whitelegge, J.P.; Gomez-Pinilla, F. Exercise affects energy metabolism and neural plasticityrelated proteins in the hippocampus as revealed by proteomic analysis. Eur. J. Neurosci., 2006, 24, 1265-1276.
31. Fabel, K.; Kempermann, G. Physical activity and the regulation of neurogenesis in the adult and aging brain. Neuromol. Med., 2008, 10, 59-66.
32. Colcombe, S.J.; Kramer, A.F.; Erickson, K.I.; Scalf, P.; McAuley, E.; Cohen, N.J.; Webb, A.; Jerome, G.J.; Marquez, D.X.; Elavsky, S. Cardiovascular fitness, cortical plasticity, and aging. Proc. Natl. Acad. Sci. USA, 2004, 101, 3316-3321.
33. Draganski, B.; Gaser, C.; Busch, V.; Schuierer, G.; Bogdahn, U.; May, A. Neuroplasticity: changes in grey matter induced by training. Nature, 2004, 427, 311-312.
34. May, A.; Hajak, G.; Ganssbauer, S.; Steffens, T.; Langguth, B.; Kleinjung, T.; Eichhammer, P. Structural brain alterations following 5 days of intervention: dynamic aspects of neuroplasticity. Cereb. Cortex, 2007, 17, 205-210.
35. Gaser, C.; Schlaug, G. Gray matter differences between musicians and nonmusicians. Ann. N. Y. Acad. Sci., 2003, 999, 514-517.
36. Pajonk, F.G.; Wobrock, T.; Gruber, O.; Scherk, H.; Berner, D.; Kaizl, I.; Kierer, A.; Müller, S.; Oest, M.; Meyer, T.; Backens, M.; Schneider-Axmann, T.; Thornton, A.E.; Honer, W.G.; Falkai, P. Hippocampal plasticity in response to exercise in schizophrenia. Arch. Gen. Psychiatry 2010, 67, 133-143.
37. Bannerman, D.M.; Rawlins, J.N.; McHugh, S.B.; Deacon, R.M.; Yee, B.K.; Bast, T.; Zhang, W.N.; Pothuizen, H.H.; Feldon, J. Regional dissociations within the hippocampus--memory and anxiety. Neurosci. Biobehav. Rev., 2004, 28, 273-283.
38. McEwen, B.S. Possible mechanisms for atrophy of the human hippocampus. Mol. Psychiatry, 1997, 2, 255-262.
39. Masuda, S.; Okano, M.; Yamagishi, K.; Nagao, M.; Ueda, M.; Sasaki, R. A novel site of erythropoietin production. Oxygendependent production in cultured rat astrocytes. J. Biol. Chem., 1994, 269, 19488-19493.
40. Knabe, W.; Knerlich, F.; Washausen, S.; Kietzmann, T.; Sirén, A.L.; Brunnett, G.; Kuhn, H.J.; Ehrenreich, H. Expression patterns of erythropoietin and its receptor in the developing midbrain. Anat. Embryol. (Berl.), 2004, 207, 503-512.
41. Ehrenreich, H.; Degner, D.; Meller, J.; Brines, M.; Béhé, M.; Hasselblatt, M.; Woldt, H.; Falkai, P.; Knerlich, F.; Jacob, S.; von Ahsen, N.; Maier, W.; Brück, W.; Rüther, E.; Cerami, A.; Becker, W.; Sirén, A.L. Erythropoietin: a candidate compound for neuroprotection in schizophrenia. Mol. Psychiatry, 2004, 9, 42-54.
42. Jelkmann, W. Erythropoietin after a century of research: younger than ever. Eur. J. Haematol., 2007, 78, 183-205.
43. Byts, N.; Samoylenko, A.; Woldt, H.; Ehrenreich, H.; Siren, A.L. Cell type specific signalling by hematopoietic growth factors in neural cells. Neurochem. Res., 2006, 31, 1219-1230.
44. Park, M.H.; Lee, S.M.; Lee, J.W.; Son, D.J.; Moon, D.C.; Yoon, D.Y.; Hong, J.T. ERK-mediated production of neurotrophic factors by astrocytes promotes neuronal stem cell differentiation by erythropoietin. Biochem. Biophys. Res. Commun., 2006, 339, 1021-1028.
45. Ehrenreich, H.; Hinze-Selch, D.; Stawicki, S.; Aust, C.; Knolle- Veentjer, S.; Wilms, S.; Heinz, G.; Erdag, S.; Jahn, H.; Degner, D.; Ritzen, M.; Mohr, A.; Wagner, M.; Schneider, U.; Bohn, M.; Huber, M.; Czernik, A.; Pollmächer, T.; Maier, W.; Sirén, A.L.; Klosterkötter, J.; Falkai, P.; Rüther, E.; Aldenhoff, J.B.; Krampe, H. Improvement of cognitive functions in chronic schizophrenic patients by recombinant human erythropoietin. Mol. Psychiatry, 2007, 12, 206-220.
46. Cooke, S.F.; Bliss, T.V. Plasticity in the human central nervous system. Brain, 2006, 129, 1659-1673.
47. Chen, F.; Madsen, T.M.; Wegener, G.; Nyengaard, J.R. Repeated electroconvulsive seizures increase the total number of synapses in adult male rat hippocampus. Eur. Neuropsychopharmacol., 2009, 19, 329-338.
48. Tharyan, P.; Adams, C.E. Electroconvulsive Therapy for Schizophrenia (Cochrane Review). John Wiley & Sons, Ltd: Chichester, UK, 2004.
49. Haraldsson, H.M.; Ferrarelli, F.; Kalin, N.H.; Tononi, G. Transcranial Magnetic Stimulation in the investigation and treatment of schizophrenia: a review. Schizophr Res., 2004, 71, 1-16.
50. Burt, T.; Lisanby, S.H.; Sackeim, H.A. Neuropsychiatric applications of transcranial magnetic stimulation: a meta analysis. Int. J. Neuropsychopharmacol., 2002, 5, 73-103.
51. Wassermann, E.M. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation; June 5-7, 1996. Electroencephalogr. Clin. Neurophysiol., 1998, 108, 1-16.
52. George, M.S; Lisanby, S.H.; Sackeim, H.A. Transcranial magnetic stimulation: applications in neuropsychiatry. Arch. Gen. Psychiatry, 1999, 56, 300-311.
53. Post, A.; Muller, M.B.; Engelmann, M.; Keck, M.E. Repetitive transcranial magnetic stimulation in rats: evidence for a neuroprotective effect in vitro and in vivo. Eur. J. Neurosci., 1999, 11, 3247-3254.
54. Fujiki, M.; Steward, O. High frequency transcranial magnetic stimulation mimics the effects of ECS in upregulating astroglial gene expression in the murine CNS. Brain Res. Mol. Brain Res., 1997, 44, 301-308.
55. Steward, O.; Kelley, M.S.; Torre, E.R. The process of reinnervation in the dentate gyrus of adult rats: temporal relationship between changes in the levels of glial fibrillary acidic protein (GFAP) and GFAP mRNA in reactive astrocytes. Exp. Neurol., 1993, 124, 167-183.
56. Post, A.; Keck, M.E. Transcranial magnetic stimulation as a therapeutic tool in psychiatry: what do we know about the neurobiological mechanisms? J. Psychiatr. Res., 2001, 35, 193-215.
57. Muller, M.B.; Toschi, N.; Kresse, A.E.; Post, A.; Keck, M.E. Longterm repetitive transcranial magnetic stimulation increases the expression of brain-derived neurotrophic factor and cholecystokinin mRNA, but not neuropeptide tyrosine mRNA in specific areas of rat brain. Neuropsychopharmacology, 2000, 23, 205-215.
58. Zetterstrom, T.S.; Pei, Q.; Grahame-Smith, D.G. Repeated electroconvulsive shock extends the duration of enhanced gene expression for BDNF in rat brain compared with a single administration. Brain Res. Mol. Brain Res., 1998, 57, 106-110.
59. Zetterstrom, T.S.; Pei, Q.; Madhav, T.R.; Coppell, A.L.; Lewis, L.; Grahame-Smith, D.G. Manipulations of brain 5-HT levels affect gene expression for BDNF in rat brain. Neuropharmacology, 1999, 38, 1063-1073.
60. Czeh, B.; Welt, T.; Fischer, A.K.; Erhardt, A.; Schmitt, W.; Müller, M.B.; Toschi, N.; Fuchs, E.; Keck, M.E. Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol. Psychiatry, 2002, 52, 1057-1065.
61. Shergill, S.S.; Murray, R.M.; McGuire, P.K. Auditory hallucinations: a review of psychological treatments. Schizophr. Res., 1998, 32, 137-150.
62. Shergill, S.S.; Brammer, M.J.; Williams, S.C.; Murray, R.M.; McGuire, P.K. Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Arch. Gen. Psychiatry, 2000, 57, 1033-1038.
63. Hoffman, R.E.; Boutros, N.N.; Berman, R.M.; Roessler, E.; Belger, A.; Krystal, J.H.; Charney, D.S. Transcranial magnetic stimulation of left temporoparietal cortex in three patients reporting hallucinated voices. Biol. Psychiatry, 1999, 46, 130-132.
64. Freitas, C.; Fregni, F.; Pascual-Leone, A. Meta-analysis of the effects of repetitive transcranial magnetic stimulation (rTMS) on negative and positive symptoms in schizophrenia. Schizophr. Res., 2009, 108, 11-24.
65. Dolan, R.J.; Bench, C.J.; Liddle, P.F.; Friston, K.J.; Frith, C.D.; Grasby, P.M.; Frackowiak, R.S. Dorsolateral prefrontal cortex dysfunction in the major psychoses; symptom or disease specificity? J. Neurol. Neurosurg. Psychiatry, 1993, 56, 1290-1294.
66. Dlabac-de Lange, J.J.; Knegtering, R.; Aleman, A. Repetitive transcranial magnetic stimulation for negative symptoms of schizophrenia: review and meta-analysis. J. Clin. Psychiatry, 2010, 71(4), 411-418.
67. Cordes, J.; Falkai, P.; Guse, B.; Hasan, A.; Schneider-Axmann, T.; Arends, M.; Winterer, G.; Wölwer, W.; Ben Sliman, E.; Ramacher, M.; Schmidt-Kraepelin, C.; Ohmann, C.; Langguth, B.; Landgrebe, M.; Eichhammer, P.; Frank, E.; Burger, J.; Hajak, G.; Rietschel, M.; Wobrock, T. Repetitive transcranial magnetic stimulation for the treatment of negative symptoms in residual schizophrenia: rationale and design of a sham-controlled, randomized multicenter study. Eur. Arch. Psychiatry Clin. Neurosci., 2009, 259(Suppl. 2), S189-S197.
68. Huang, Y.Z.; Edwards, M.J.; Rounis, E.; Bhatia, K.P.; Rothwell, J.C. Theta burst stimulation of the human motor cortex. Neuron, 2005, 45, 201-206.
69. Huang, Y.Z.; Rothwell, J.C.; Chen, R.S.; Lu, C.S.; Chuang, W.L. The theoretical model of theta burst form of repetitive transcranial magnetic stimulation. Clin. Neurophysiol., 2011, 122(5), 1011-1018.
70. Demirtas-Tatlidede, A.; Freitas, C.; Cromer, J.R.; Safar, L.; Ongur, D.; Stone, W.S.; Seidman, L.J.; Schmahmann, J.D.; Pascual-Leone, A. Safety and proof of principle study of cerebellar vermal theta burst stimulation in refractory schizophrenia. Schizophr. Res., 2010, 124(1/3), 91-100.
71. Bor, J.; Brunelin, J.; Rivet, A.; d'Amato, T.; Poulet, E.; Saoud, M.; Padberg, F. Effects of theta burst stimulation on glutamate levels in a patient with negative symptoms of schizophrenia. Schizophr. Res., 2009, 111, 196-197.
72. Eberle, M.C.; Wildgruber, D.; Wasserka, B.; Fallgatter, A.J.; Plewnia, C. Relief From Chronic Intractable Auditory Hallucinations After Long-Term Bilateral Theta Burst Stimulation. Am. J. Psychiatry, 2010, 167, 1410.
73. Sidhoumi, D.; Braha, S.; Bouaziz, N.; Brunelin, J.; Benadhira, R.; Januel, D. Evaluation of the therapeutic effect of theta burst stimulation on drug-resistant auditory hallucinations in a schizophrenic patient and its impact on cognitive function and neuronal excitability: a case study. Clin. Neurophysiol., 2010, 121, 802.
74. Edelmuth, R.C.; Nitsche, M.A.; Battistella, L.; Fregni, F. Why do some promising brain-stimulation devices fail the next steps of clinical development? Expert. Rev. Med. Devices, 2010, 7, 67-97.
75. Zhao, C.; Deng, W.; Gage, F.H. Mechanisms and functional implications of adult neurogenesis. Cell, 2008, 132, 645-660.
76. Leuner, B.; Gould, E. Structural plasticity and hippocampal function. Annu. Rev. Psychol., 2010, 61, 111-140.
77. van Praag, H.; Shubert, T.; Zhao, C.; Gage, F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci., 2005, 25, 8680-8685.
78. Klempin, F.; Kempermann, G. Adult hippocampal neurogenesis and aging. Eur. Arch. Psychiatry Clin. Neurosci., 2007, 257, 271-280.
79. Song, H.; Stevens, C.F.; Gage, F.H. Astroglia induce neurogenesis from adult neural stem cells. Nature, 2002, 417, 39-44.
80. Duan, X.; Chang, J.H.; Ge, S.; Faulkner, R.L.; Kim, J.Y.; Kitabatake, Y.; Liu, X.B.; Yang, C.H.; Jordan, J.D.; Ma, D.K.; Liu, C.Y.; Ganesan, S.; Cheng, H.J.; Ming, G.L.; Lu, B.; Song, H. Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell, 2007, 130, 1146-1158.
81. Gong, C.; Wang, T.W.; Huang, H.S.; Parent, J.M. Reelin regulates neuronal progenitor migration in intact and epileptic hippocampus. J. Neurosci., 2007, 27, 1803-1811.
82. Ge, S.; Yang, C.H.; Hsu, K.S.; Ming, G.L.; Song, H. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron, 2007, 54, 559-566.
83. Kee, N.; Teixeira, C.M.; Wang, A.H.; Frankland, P.W. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci., 2007, 10, 355-362.
84. Tashiro, A.; Sandler, V.M.; Toni, N.; Zhao, C.; Gage, F.H. NMDAreceptor- mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature, 2006, 442, 929-933.
85. Olson, A.K.; Eadie, B.D.; Ernst, C.; Christie, B.R. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus, 2006, 16, 250-260.
86. Dobrossy, M.D.; Drapeau, E.; Aurousseau, C.; Le Moal, M.; Piazza, P.V.; Abrous, D.N. Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date. Mol. Psychiatry, 2003, 8, 974-982.
87. Gilbert, P.E.; Kesner, R.P.; Lee, I. Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1. Hippocampus, 2001, 11, 626-636.
88. McHugh, T.J.; Jones, M.W.; Quinn, J.J.; Balthasar, N.; Coppari, R.; Elmquist, J.K.; Lowell, B.B.; Fanselow, M.S.; Wilson, M.A.; Tonegawa, S. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science, 2007, 317, 94-99.
89. Wiskott, L.; Rasch, M.J.; Kempermann, G. A functional hypothesis for adult hippocampal neurogenesis: avoidance of catastrophic interference in the dentate gyrus. Hippocampus, 2006, 16, 329-343.
90. Dietrich, M.O.; Andrews, Z.B.; Horvath, T.L. Exercise-induced synaptogenesis in the hippocampus is dependent on UCP2-regulated mitochondrial adaptation. J. Neurosci., 2008, 28, 10766-10771.
91. Esser, S.K.; Huber, R.; Massimini, M.; Peterson, M.J.; Ferrarelli, F.; Tononi, G. A direct demonstration of cortical LTP in humans: a combined TMS/EEG study. Brain Res. Bull., 2006, 69, 86-94.
92. Fox, P.; Ingham, R.; George, M.S.; Mayberg, H.; Ingham, J.; Roby, J.; Martin, C.; Jerabek, P. Imaging human intra-cerebral connectivity by PET during TMS. Neuroreport, 1997, 8, 2787-2791.
93. Strafella, A.P.; Paus, T.; Barrett, J.; Dagher, A. Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J. Neurosci., 2001, 21, RC157.
94. Lessmann, V.; Gottmann, K.; Malcangio, M. Neurotrophin secretion: current facts and future prospects. Prog. Neurobiol., 2003, 69, 341-374.
95. Ahmed, Z.; Wieraszko, A. Modulation of learning and hippocampal; neuronal plasticity by repetitive transcranial magnetic stimulation (rTMS). Bioelectromagnetics, 2006, 27, 288-294.
96. Vaynman, S.; Ying, Z.; Gomez-Pinilla, F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur. J. Neurosci., 2004, 20, 2580-2590.
97. Melloni, R.H.; Jr., Apostolides, P.J.; Hamos, J.E.; DeGennaro, L.J. Dynamics of synapsin I gene expression during the establishment and restoration of functional synapses in the rat hippocampus. Neuroscience, 1994, 58, 683-703.
98. Barbacid, M. The Trk family of neurotrophin receptors. J. Neurobiol., 1994, 25, 1386-1403.
99. Garcia, C.C.; Blair, H.J.; Seager, M.; Coulthard, A.; Tennant, S.; Buddles, M.; Curtis, A.; Goodship, J.A. Identification of a mutation in synapsin I; a synaptic vesicle protein; in a family with epilepsy. J. Med. Genet., 2004, 41, 183-186.
100. Pieribone, V.A.; Shupliakov, O.; Brodin, L.; Hilfiker-Rothenfluh, S.; Czernik, A.J.; Greengard, P. Distinct pools of synaptic vesicles in neurotransmitter release. Nature, 1995, 375, 493-497.
101. Blanquet, P.R.; Lamour, Y. Brain-derived neurotrophic factor increases Ca2+/calmodulin-dependent protein kinase 2 activity in hippocampus. J. Biol. Chem., 1997, 272, 24133-24136.
102. Greengard, P.; Valtorta, F.; Czernik, A.J.; Benfenati, F. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science, 1993, 259, 780-785.
103. Jovanovic, J.N.; Czernik, A.J.; Fienberg, A.A.; Greengard, P.; Sihra, T.S. Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat. Neurosci., 2000, 3, 323-329.
104. Duman, R.S.; Monteggia, L.M. A neurotrophic model for stressrelated mood disorders. Biol. Psychiatry, 2006, 59, 1116-1127.
105. Cheeran, B.; Talelli, P.; Mori, F.; Koch, G.; Suppa, A.; Edwards, M.; Houlden, H.; Bhatia, K.; Greenwood, R.; Rothwell, J.C. A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. J. Physiol., 2008, 586, 5717-5725.
106. Antal, A.; Chaieb, L.; Moliadze, V.; Monte-Silva, K.; Poreisz, C.; Thirugnanasambandam, N.; Nitsche, M.A.; Shoukier, M.; Ludwig, H.; Paulus, W. Brain-derived neurotrophic factor (BDNF) gene polymorphisms shape cortical plasticity in humans. Brain Stimul., 2010, 3, 230-237.
107. Ehrenreich, H.; Siren, A.L. Neuroprotection--what does it mean?-- What means do we have? Eur. Arch. Psychiatry Clin. Neurosci., 2001, 251, 149-151.
108. Sack, A.T.; Linden, D.E. Combining transcranial magnetic stimulation and functional imaging in cognitive brain research: possibilities and limitations. Brain Res. Brain Res. Rev., 2003, 43, 41-56.
109. Ridding, M.C.; Rothwell, J.C. Is there a future for therapeutic use of transcranial magnetic stimulation? Nat. Rev. Neurosci., 2007, 8, 559-567.
110. Guse, B.; Falkai, P.; Wobrock, T. Cognitive effects of highfrequency repetitive transcranial magnetic stimulation: a systematic review. J. Neural. Transm., 2010, 117, 105-122.
111. Mittrach, M.; Thunker, J.; Winterer, G.; Agelink, M.W.; Regenbrecht, G.; Arends, M.; Mobascher, A.; Kim, S.J.; Wölwer, W.; Brinkmeyer, J.; Gaebel, W.; Cordes, J. The Tolerability of rTMS Treatment in Schizophrenia with Respect to Cognitive Function. Pharmacopsychiatry, 2010, 43(3), 110-117.
112. Manganas, L.N.; Zhang, X.; Li, Y.; Hazel, R.D.; Smith, S.D.; Wagshul, M.E.; Henn, F.; Benveniste, H.; Djuric, P.M.; Enikolopov, G.; Maletic-Savatic, M. Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain. Science, 2007, 318, 980-985.