Chronic cerebrolysin administration attenuates neuronal abnormalities in the basolateral amygdala induced by neonatal ventral hippocampus lesion in the rat

Synapse

Volumn 68, Issue 1, 2014, Pages 31-38

  Vázquez Roque, Rubén Antonio ^a   Ubhi, Kiren ^b   Masliah, Eliezer ^a   Flores, Gonzalo ^a  

^a BENEMÉRITA UNIVERSIDAD AUTÓNOMA DE PUEBLA   (Mexico)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Basolateral amygdale; Cerebrolysin; Golgi Cox stain; Neonatal ventral hippocampal lesion; Schizophrenia; Stereology

Indexed keywords

CEREBROLYSIN;

ANIMAL MODEL; ARTICLE; ATTENUATION; BASOLATERAL AMYGDALA; BRAIN ATROPHY; BRAIN DAMAGE; CELL COUNT; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; DENDRITIC CELL; FEMALE; GOLGI STAIN; HIPPOCAMPUS; NEONATAL VENTRAL HIPPOCAMPAL LESION; NONHUMAN; PRIORITY JOURNAL; RAT; SPINE DISEASE; STEREOLOGY; STEREOMETRY; TREATMENT DURATION;

BASOLATERAL AMYGDALE; CEREBROLYSIN; GOLGI-COX STAIN; NEONATAL VENTRAL HIPPOCAMPAL LESION; SCHIZOPHRENIA; STEREOLOGY;

AMINO ACIDS; AMYGDALA; ANIMALS; DENDRITES; HIPPOCAMPUS; INJECTIONS, INTRAVENTRICULAR; NEUROPROTECTIVE AGENTS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84888018424     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.21718     Document Type: Article

References (72)

1. Alcántara-González F, Gamboa C, de la Cruz F, Zamudio S, Flores G. 2012. Combined administration of cerebrolyisin and donepezil induces plastic changes in medial prefrontal cortex and dentate gyrus in aged mice. Synapse 66:938-949.
2. Alquicer G, Morales-Medina JC, Quirion R, Flores G. 2008. Postweaning social isolation enhances morphological changes in the neonatal ventral hippocampal lesion rat model of psychosis. J Chem Neuroanat 35:179-187.
3. Anticevic A, Corlett PR. 2012. Cognition-emotion dysinteraction in schizophrenia. Front Psychol 3:392, doi: 10.3389/fpsyg.2012.00392.
4. 3H-thymidine radiographic analyses of neurogenesis in the rat amygdala. Bayer SA. J Comp Neurol 194:845-875.
5. Bechara A, Damasio H, Damasio AR. 2000. Emotion, decision making and the orbitofrontal cortex. Cereb Cortex 10:295-307.
6. Benes FM. 2010. Amygdalocortical circuitry in schizophrenia: From circuits to molecules. Neuropsychopharmacology 35:239-257.
7. Berdel B, Moryś J, Maciejewska B, Dziewiatkowski J. 1997. Volume and topographical changes of the basolateral complex during the development of the rat's amygdaloid body. Folia Morphol (Warsz) 56:1-11.
8. Bouwmeester H, Smits K, van Ree JM. 2002a. Neonatal development of projections to the basolateral amygdala from prefrontal and thalamic structures in rat. J Comp Neurol 450:241-255.
9. Bouwmeester H, Wolterink G, van Ree JM. 2002b. Neonatal development of projections from the basolateral amygdala to prefrontal, striatal, and thalamic structures in the rat. J Comp Neurol 442:239-249.
10. Brake WG, Sullivan RM, Flores G, Srivastava LK, Gratton A. 1999. Neonatal ventral hippocampal lesions attenuate the nucleus accumbens dopamine response to stress: An electrochemical study in the adult rat. Brain Res 831:25-32.
11. Bringas ME, Morales-Medina JC, Flores-Vivaldo Y, Negrete-Diaz JV, Aguilar-Alonso P, León-Chávez BA, Lazcano-Ortiz Z, Monroy E, Rodríguez-Moreno A, Quirion R, Flores G. 2012. Clozapine administration reverses behavioral, neuronal, and nitric oxide disturbances in the neonatal ventral hippocampus rat. Neuropharmacology 62:1848-1857.
12. Chana G, Landau S, Beasley C, Everall IP, Cotter D. 2003. Two-dimensional assessment of cytoarchitecture in the anterior cingulate cortex in major depressive disorder, bipolar disorder, and schizophrenia: Evidence for decreased neuronal somal size and increased neuronal density. Biol Psychiatry 53:1086-1098.
13. Chareyron LJ, Banta Lavenex P, Amaral DG, Lavenex P. 2011. Stereological analysis of the rat and monkey amygdala. J Comp Neurol 519:3218-3239.
14. Chareyron LJ, Lavenex PB, Lavenex P. 2012. Postnatal development of the amygdala: A stereological study in rats. J Comp Neurol 520:3745-3763
15. Chen H, Tung YC, Li B, Iqbal K, Grundke-Iqbal I. 2007. Trophic factors counteract elevated FGF-2-induced inhibition of adult neurogenesis. Neurobiol Aging 28:1148-1162.
16. Chew LJ, Fusar-Poli P, Schmitz T. Oligodendroglial alterations and the role of microglia in white matter injury: Relevance to schizophrenia. Dev Neurosci (in press).
17. Daenen EW, Wolterink G, van der Heyden JA, Kruse CG, van Ree JM. 2003. Neonatal lesions in the amygdala or ventral hippocampus disrupt prepulse inhibition of the acoustic startle response; implications for an animal model of neurodevelopmental disorders like schizophrenia. Eur Neuropsychopharmacol 13:187-197.
18. Diergaarde L, Gerrits MA, Stuy A, Spruijt BM, van Ree JM. 2004. Neonatal amygdala lesions and juvenile isolation in the rat: Differential effects on locomotor and social behavior later in life. Behav Neurosci 118:298-2305.
19. Diergaarde L, Gerrits MA, Brouwers JP, van Ree JM. 2005. Early amygdala damage disrupts performance on medial prefrontal cortex- related tasks but spares spatial learning and memory in the rat. Neuroscience 130:581-590.
20. Edwards J, Jackson HJ, Pattison PE. 2002. Emotion recognition via facial expression and affective prosody in schizophrenia: A methodological review. Clin Psychol Rev 22:789-832.
21. Everall IP, DeTeresa R, Terry R, Masliah E. 1997. Comparison of two quantitative methods for the evaluation of neuronal number in the frontal cortex in Alzheimer disease. J Neuropathol Exp Neurol 56:1202-1206.
22. Flores G, Barbeau D, Quirion R, Srivastava LK. 1996. Decreased binding of dopamine D3 receptors in limbic subregions after neonatal bilateral lesion of rat hippocampus. J Neurosci 16:2020-2026.
23. Flores G, Alquicer G, Silva-Gomez AB, Zaldivar G, Stewart J, Quirion R, Srivastava LK. 2005. Alterations in dendritic morphology of prefrontal cortical and nucleus accumbens neurons in post-pubertal rats after neonatal excitotoxic lesions of the ventral hippocampus. Neuroscience 133:463-470.
24. Gibb R, Kolb B. 1998. A method for vibratome sectioning of Golgi-Cox stained whole rat brain. J Neurosci Methods 79:1-4.
25. Giedd JN, Vaituzis AC, Hamburger SD, Lange N, Rajapakse JC, Kaysen D, Vauss YC, Rapoport JL. 1996. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4-18 years. J Comp Neurol 366:223-230.
26. Giedd JN, Castellanos FX, Rajapakse JC, Vaituzis AC, Rapoport JL. 1997. Sexual dimorphism of the developing human brain. Prog Neuropsychopharmacol Biol Psychiatry 21:1185-11201.
27. Gómez-Palacio-Schjetnan A, Escobar ML. 2013. Neurotrophins and synaptic plasticity. Curr Top Behav Neurosci 15:117-136.
28. Halpain S, Spencer K, Graber S. 2005. Dynamics and pathology of dendritic spines. Prog Brain Res 147:29-37.
29. Huang CL, Hsiao S, Hwu HG, Howng SL. 2013. Are there differential deficits in facial emotion recognition between paranoid and non-paranoid schizophrenia? A signal detection analysis. Psychiatry Res, doi: 10.1016/j.psychres.2013.03.026.
30. Juárez I, González DJ, Mena R, Flores G. 2011. The chronic administration of cerebrolysin induces plastic changes in the prefrontal cortex and dentate gyrus in aged mice. Synapse 65:1128-1135.
31. Kolb B, Forgie M, Gibb R, Gorny G, Rowntree S. 1998. Age, experience and the changing brain. Neurosci Biobehav Rev 22:143-159.
32. Kuczenski R, Everall IP, Crews L, Adame A, Grant I, Masliah E. 2007. Escalating dose-multiple binge methamphetamine exposure results in degeneration of the neocortex and limbic system in the rat. Exp Neurol 207:42-51.
33. Kuwajima M, Spacek J, Harris KM. 2013. Beyond counts and shapes: Studying pathology of dendritic spines in the context of the surrounding neuropil through serial section electron microscopy. Neuroscience 251:75-89.
34. Lee KF, Soares C, Béïque JC. 2012. Examining form and function of dendritic spines. Neural Plast 2012:704103, doi: 10.1155/2012/704103.
35. Lipska BK, Weinberger DR. 2000. To model a psychiatric disorder in animals: Schizophrenia as a reality test. Neuropsychopharmacology 23:223-239.
36. Lipska BK, Jaskiw GE, Weinberger DR. 1993. Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: A potential animal model of schizophrenia. Neuropsychopharmacology 9:67-75.
37. Lipska BK, Khaing ZZ, Weickert CS, Weinberger DR. 2001. BDNF mRNA expression in rat hippocampus and prefrontal cortex: Effects of neonatal ventral hippocampal damage and antipsychotic drugs. Eur J Neurosci 14:135-144.
38. Liu H, Tang Y, Womer F, Fan G, Lu T, Driesen N, Ren L, Wang Y, He Y, Blumberg HP, Xu K, Wang F. 2013. Differentiating patterns of amygdala-frontal functional connectivity in schizophrenia and bipolar disorder. Schizophr Bull, doi: 10.1093/schbul/sbt044.
39. Mahon PB, Eldridge H, Crocker B, Notes L, Gindes H, Postell E, King S, Potash JB, Ratnanather JT, Barta PE. 2012. An MRI study of amygdala in schizophrenia and psychotic bipolar disorder. Schizophr Res 138:188-191.
40. Marcotte ER, Pearson DM, Srivastava LK. 2001. Animal models of schizophrenia: A critical review. J Psychiatry Neurosci 26:395-410.
41. Martinez-Tellez R, Gomez-Villalobos MJ, Flores G. 2005. Alteration in dendritic morphology of cortical neurons in rats with diabetes mellitus induced by streptozotocin. Brain Res 1048:108-115.
42. Martínez-Téllez RI, Hernández-Torres E, Gamboa C, Flores G. 2009. Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse 63:794-804.
43. Masliah E, Díez-Tejedor E. 2012. The pharmacology of neurotrophic treatment with cerebrolysin: Brain protection and repair to counteract pathologies of acute and chronic neurological disorders. Drugs Today (Barc) 48 (Suppl A):3-24.
44. Menon PK, Muresanu DF, Sharma A, Mössler H, Sharma HS. 2012. Cerebrolysin, a mixture of neurotrophic factors induces marked neuroprotection in spinal cord injury following intoxication of engineered nanoparticles from metals. CNS Neurol Disord Drug Targets 11:40-49.
45. Mizukami S, Nishizuka M, Arai Y. 1983. Sexual difference in nuclear volume and its ontogeny in the rat amygdala. Exp Neurol 79:569-575.
46. Molteni R, Lipska BK, Weinberger DR, Racagni G, Riva MA. 2001. Developmental and stress-related changes of neurotrophic factor gene expression in an animal model of schizophrenia. Mol Psychiatry 6:285-292.
47. Morales-Medina JC, Sanchez F, Flores G, Dumont Y, Quirion R. 2009. Morphological reorganization after repeated corticosterone administration in the hippocampus, nucleus accumbens and amygdala in the rat. J Chem Neuroanat 38:266-272.
48. Nave K A. 2010. Myelination and support of axonal integrity by glia. Nature 468:244-252.
49. Negrete-Diaz JV, Baltazar-Gaytan E, Bringas ME, Vazquez-Roque RA, Newton S, Aguilar-Alonso P, Leon-Chavez BA, Flores G. 2010. Neonatal ventral hippocampus lesion induces increase in no levels which is attenuated by subchronic haloperidol treatment. Synapse 64:941-947.
50. Ostby Y, Tamnes CK, Fjell AM, Westlye LT, Due-Tønnessen P, Walhovd KB. 2009. Heterogeneity in subcortical brain development: A structural magnetic resonance imaging study of brain maturation from 8 to 30 years. J Neurosci 29:11772-11782.
51. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. New York: Academic Press.
52. Qiu A, Gan SC, Wang Y, Sim K. 2012. Amygdala-hippocampal shape and cortical thickness abnormalities in first-episode schizophrenia and mania. Psychol Med 43:1353-1363.
53. Robinson TJ, Kolb B. 1997. Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J Neurosci 17:8491-8497.
54. Schumann CM, Hamstra J, Goodlin-Jones BL, Lotspeich LJ, Kwon H, Buonocore MH, Lammers CR, Reiss AL, Amaral DG. 2004. The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J Neurosci 24:6392-6340.
55. Schumann CM, Bauman MD, Amaral DG. 2011. Abnormal structure or function of the amygdala is a common component of neurodevelopmental disorders. Neuropsychologia 49:745-759.
56. Schumann CM, Bauman MD, Amaral DG. 2011. Abnormal structure or function of the amygdala is a common component of neurodevelopmental disorders. Neuropsychologia 49:745-759.
57. Schulz C, Mothes-Lasch M, Straube T. 2013. Automatic neural processing of disorderrelated stimuli in social anxiety disorder: Faces and more. Front Psychol 4:282, doi: 10.3389/fpsyg.2013.00282.
58. Shepherd AM, Laurens KR, Matheson SL, Carr VJ, Green MJ. 2012. Systematic meta-review and quality assessment of the structural brain alterations in schizophrenia. Neurosci Biobehav Rev 36:1342-1356.
59. Sholl DA. 1953. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87:387-406.
60. Sierra A, Camacho-Abrego I, Negrete-Díaz V, Rodríguez-Sosa L, Escamilla C, Flores G. 2009. Economical body platform for neonatal rats stereotaxic surgery. Rev Neurol 48:141-146.
61. Silva-Gomez AB, Rojas D, Juarez I, Flores G. 2003. Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res 983:128-136.
62. Solís O, Vázquez-Roque RA, Camacho-Abrego I, Gamboa C, De La Cruz F, Zamudio S, Flores G. 2009. Decreased dendritic spine density of neurons of the prefrontal cortex and nucleus accumbens and enhanced amphetamine sensitivity in postpubertal rats after a neonatal amygdala lesion. Synapse 63:1143-1153.
63. Tesli M, Skatun KC, Ousdal OT, Brown AA, Thoresen C, Agartz I, Melle I, Djurovic S, Jensen J, Andreassen OA. 2013. CACNA1C risk variant and amygdala activity in bipolar disorder, schizophrenia and healthy controls. PLoS One 8:e56970.
64. Torres-García ME, Solis O, Patricio A, Rodríguez-Moreno A, Camacho-Abrego I, Limón ID, Flores G. 2012. Dendritic morphology changes in neurons from the prefrontal cortex, hippocampus and nucleus accumbens in rats after lesion of the thalamic reticular nucleus. Neuroscience 223:429-438.
65. Tseng KY, Chambers RA, Lipska BK. 2009. The neonatal ventral hippocampal lesion as a heuristic neurodevelopmental model of schizophrenia. Behav Brain Res 204:295-305.
66. Tsui CF, Huang J, Lui SS, Au AC, Leung MM, Cheung EF, Chan RC. 2013. Facial emotion perception abnormality in patients with early schizophrenia. Schizophr Res 147:230-235.
67. Ubhi K, Rockenstein E, Vazquez-Roque R, Mante M, Inglis C, Patrick C, Adame A, Fahnestock M, Doppler E, Novak P, Moessler H, Masliah E. 2013. Cerebrolysin modulates pronerve growth factor/nerve growth factor ratio and ameliorates the cholinergic deficit in a transgenic model of Alzheimer's disease. J Neurosci Res 91:167-177.
68. Vazquez-Roque R, Ramos B, Tecuatl C, Juárez I, Adame A, De la Cruz F, Zamudio S, Mena R, Rockenstein E, Masliah E, Flores G. 2012a. Chronic administration of the neurotrophic agent cerebrolysin ameliorates the behavioral and morphological changes induced by neonatal ventral hippocampus lesion in a rat model of schizophrenia. J Neurosci Res 90:288-306.
69. Vázquez-Roque RA, Solís O, Camacho-Abrego I, Rodríguez-Moreno A, Fidel de la Cruz, Zamudio S, Flores G. 2012b. Dendritic morphology of neurons in prefrontal cortex and ventral hippocampus of rats with neonatal amygdala lesion. Synapse 66:373-382.
70. Vega E, Gomez-Villalobos MJ, Flores G. 2004. Alteration in dendritic morphology of pyramidal neurons from the prefrontal cortex of rats with renovascular hypertension. Brain Res 1021:112-118.
71. Watson DR, Bai F, Barrett SL, Turkington A, Rushe TM, Mulholland CC, Cooper SJ. 2012. Structural changes in the hippocampus and amygdala at first episode of psychosis. Brain Imaging Behav 6:49-60.
72. Xiao S, Xue H, Li G, Yuan C, Li X, Chen C, Wu HZ, Mitchell P, Zhang M. 2012. Therapeutic effects of cerebrolysin added to risperidone in patients with schizophrenia dominated by negative symptoms. Aust NZ J Psychiatry 46:153-160.