Dendritic morphology of neurons in medial prefrontal cortex, hippocampus, and nucleus accumbens in adult SH rats

Synapse

Volumn 65, Issue 3, 2011, Pages 198-206

  Sánchez, Fremioth ^a,b   Gómez Villalobos, María de Jesús ^a   Juarez, Ismael ^a   Quevedo, Lucía ^b   Flores, Gonzalo ^a  

^a BENEMÉRITA UNIVERSIDAD AUTÓNOMA DE PUEBLA   (Mexico)

^b INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

Author keywords

Dendrites; Golgi Cox stain; Hippocampus; Hypertension; Medial prefrontal cortex; Medium spiny neurons; Nucleus accumbens; Pyramidal neurons

Indexed keywords

ARTERIAL PRESSURE; ARTICLE; BLOOD PRESSURE; CELL STRUCTURE; CONTROLLED STUDY; DENDRITIC CELL; GOLGI STAIN; HIPPOCAMPUS; LOCOMOTION; MALE; NERVE CELL; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SPONTANEOUSLY HYPERTENSIVE RAT;

EID: 78650655953     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20837     Document Type: Article

References (86)

1. 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.
2. Alvarez VA, Sabatini BL. 2007. Anatomical and physiological plasticity of dendritic spines. Annu Rev Neurosci 30: 79-97.
3. Amenta F, Mignini F, Rabbia F, Tomassoni D, Veglio F. 2002. Protective effect of anti-hypertensive treatment on cognitive function in essential hypertension: Analysis of published clinical data. J Neurol Sci 204: 147-151.
4. Amenta F, Di Tullio MA, Tomassoni D. 2003. Arterial hypertension and brain damage evidence from animal models (review). Clin Exp Hypertens 25: 359-380.
5. Arnsten AF. 2009. Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 10: 410-422.
6. Audesirk T, Cabell L, Kern M, Audesirk G. 2003. Enhancement of dendritic branching in cultured hippocampal neurons by 17-β-estradiol is mediated by nitric oxide. Int J Dev Neurosci 21: 225-233.
7. Chen HI, Hu CT. 1997. Endogenous nitric oxide on arterial hemodynamics: A comparison between normotensive and hypertensive rats. Am J Physiol 273: H1816-H1823.
8. Conrad CD. 2006. What is the functional significance of chronic stress-induced CA3 dendritic retraction within the hippocampus? Behav Cogn Neurosci Rev 5: 41-60.
9. Cook SC, Wellman CL. 2004. Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 60: 236-248.
10. Diaz Heijtz R, Castellanos FX. 2006. Differential effects of a selective dopamine D1-like receptor agonist on motor activity and c-fos expression in the frontal-striatal circuitry of SHR and Wistar-Kyoto rats. Behav Brain Funct 2: 18.
11. Erkinjuntti T, Gauthier S. 2009. The concept of vascular cognitive impairment. Front Neurol Neurosci 24: 79-85.
12. Farkas E, De Vos RA, Jansen Steur EN, Luiten PG. 2000. Are Alzheimer's disease, hypertension, and cerebrocapillary damage related? Neurobiol Aging 21: 235-243.
13. Fernandez-Espejo E. 2000. How does the nucleus accumbens function? Rev Neurol 30: 845-849.
14. 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.
15. 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.
16. Floresco SB, Todd CL, Grace AA. 2001. Glutamatergic afferents from the hippocampus to the nucleus accumbens regulate activity of ventral tegmental area dopamine neurons. J Neurosci 21: 4915-4922.
17. French SJ, Totterdell S. 2003. Individual nucleus accumbens-projection neurons receive both basolateral amygdala and ventral subicular afferents in rats. Neuroscience 119: 19-31.
18. Frishman WH. 2002. Are antihypertensive agents protective against dementia? A review of clinical and preclinical data. Heart Dis 4: 380-386.
19. Gattu M, Pauly JR, Boss KL, Summers JB, Buccafusco JJ. 1997. Cognitive impairment in spontaneously hypertensive rats: Role of central nicotinic receptors I. Brain Res 771: 89-103.
20. Gattu M, Terry AV, Pauly JR, Buccafusco JJ. 1997. Cognitive impairment in spontaneously hypertensive rats: Role of central nicotinic receptors II. Brain Res 771: 104-114.
21. Gibb R, Kolb B. 1998. A method for vibratome sectioning of Golgi-Cox stained whole rat brain. J Neurosci Methods 79: 1-4.
22. Gómez F, Lahmame A, de Kloet ER, Armario A. 1996. Hypothalamic-pituitary-adrenal response to chronic stress in five inbred rat strains: Differential responses are mainly located at the adrenocortical level. Neuroendocrinology 63: 327-337.
23. Goto Y, O'Donnell P. 2001. Synchronous activity in the hippocampus and nucleus accumbens in vivo. J Neurosci 21(RC131): 1-5.
24. Goto Y, Grace AA. 2008. Dopamine modulation of hippocampal-prefrontal cortical interaction drives memory-guided behavior. Cereb Cortex 18: 1407-1414.
25. Groenewegen HJ, Wright CI, Beijer AV, Voorn P. 1999. Convergence and segregation of ventral striatal inputs and outputs. Ann NY Acad Sci 877: 49-63.
26. Hannesdottir K, Nitkunan A, Charlton RA, Barrick TR, MacGregor GA, Markus HS. 2009. Cognitive impairment and white matter damage in hypertension: A pilot study. Acta Neurol Scand 119: 261-268.
27. Hård E, Carlsson SG, Jern S, Larsson K, Lindh AS, Svensson L. 1985. Behavioral reactivity in spontaneously hypertensive rats Physiol Behav 35: 487-492.
28. Heal DJ, Smith SL, Kulkarni RS, Rowley HL. 2008. New perspectives from microdialysis studies in freely-moving, spontaneously hypertensive rats on the pharmacology of drugs for the treatment of ADHD. Pharmacol Biochem Behav 90: 184-197.
29. Heidbreder CA, Weiss IC, Domeney AM, Pryce C, Homberg J, Hedou G, Feldon J, Moran MC, Nelson P. 2000. Behavioral, neurochemical and endocrinological characterization of the early social isolation syndrome. Neuroscience 100: 749-768.
30. Hernandez CM, Høifødt H, Terry AVJr. 2003. Spontaneously hypertensive rats: Further evaluation of age-related memory performance and cholinergic marker expression. J Psychiatry Neurosci 28: 197-209.
31. Hoffmann P, Friberg P, Ely D, Thorén P. 1987. Effect of spontaneous running on blood pressure, heart rate and cardiac dimensions in developing and established spontaneous hypertension in rats. Acta Physiol Scand 129: 535-542.
32. Horch HW, Kruttgen A, Portbury SD, Katz LC. 1999. Destabilization of cortical dendrites and spines by BDNF. Neuron 23: 353-364.
33. Huttenlocher PR. 1984. Synapse elimination and plasticity in developing human cerebral cortex. Am J Ment Defici 88: 488-496.
34. Jackson ME, Moghaddam B. 2001. Amygdala regulation of nucleus accumbens dopamine output is governed by the prefrontal cortex. J Neurosci 21: 676-681.
35. Jay TM, Witter MP. 1991. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 313: 574-586.
36. Juárez I, Gratton A, Flores G. 2008. Ontogeny of altered dendritic morphology in the rat prefrontal cortex, hippocampus and nucleus accumbens following Cesarean delivery and birth anoxia. J Comp Neurol 507: 1734-1747.
37. Kolb B, Forgie M, Gibb R, Gorny G, Rowntree S. 1998. Age, experience and the changing brain. Neurosci Biobehav Rev 22: 143-159.
38. Laroche S, Davis S, Jay TM. 2000. Plasticity at hippocampal to prefrontal cortex synapses: Dual roles in working memory and consolidation. Hippocampus 10: 438-446.
39. Lee TH, Yang JT, Kato H, Wu JH. 2006. Hypertension downregulates the expression of brain-derived neurotrophic factor in the ischemia-vulnerable hippocampal CA1 and cortical areas after carotid artery occlusion. Brain Res 1116: 31-38.
40. Lewis DA, Anderson SA. 1995. The functional architecture of the prefrontal cortex and schizophrenia. Psychol Med 25: 887-894.
41. Linz W, Jessen T, Becker BA, Schoelkens BA, Wiemer G.Longterm ACE. 1997. Inhibition doubles lifespan of hypertensive rats. Circulation 96: 3164-3172.
42. Linz W, Wohlfart P, Schoelkens BA, Becker RHA, Malinski T, Wiemer G. 1999. Late treatment with ramipril increases survival in old spontaneously hypertensive rats. Hypertension 34: 291-295.
43. Manolio TA, Olson J, Longstreth WT. 2003. Hypertensive and cognitive function: Pathophysiologic effects of hypertension on the brain. Curr Hypertens Rep 5: 255-261.
44. Martínez-Tellez R, Gómez-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.
45. 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.
46. McAllister AK. 2000. Cellular and molecular mechanisms of dendrite growth. Cereb Cortex 10: 963-973.
47. McAllister AK, Lo DC, Katz LC. 1995. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15: 791-803.
48. Mignini F, Vitaioli L, Sabbatini M, Tomassoni D, Amenta F. 2004. The cerebral cortex of spontaneously hypertensive rats: A quantitative microanatomical study. Clin Exp Hypertens 26: 287-303.
49. Morales-Medina JC, Mejorada A, Romero-Curiel A, Flores G. 2007. Alterations in dendritic morphology of hippocampal neurons in adult rats after neonatal administration of N-omega-nitro-L-arginine. Synapse 61: 785-789.
50. 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.
51. Mori S, Kato M, Fujishima M. 1995. Impaired maze learning and cerebral glucose utilization in aged hypertensive rats. Hypertension 25: 545-553.
52. Nakamura-Palacios EM, Caldas CK, Fiorini A, Chagas KD, Chagas KD, Vasquez ED. 1996. Deficits of spatial learning and working memory in spontaneously hypertensive rats. Behav Brain Res 74: 217-221.
53. Nikonenko I, Jourdain P, Muller D. 2003. Presynaptic remodeling contributes to activity-dependent synaptogenesis. J Neurosci 23: 8498-8505.
54. Nikonenko I, Boda B, Steen S, Knott G, Welker E, Muller D. 2008. PSD-95 promotes synaptogenesis and multiinnervated spine formation through nitric oxide signaling J Cell Biol 183: 1115-1127.
55. O'Donnell P, Grace AA. 1995. Synaptic interactions among excitatory afferents to nucleus accumbens neurons: Hippocampal gating of prefrontal cortical input. J Neurosci 15: 3622-3639.
56. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates, 2nd ed. New York: Academic Press.
57. Radley JJ, Morrison JH. 2005. Repeated stress and structural plasticity in the brain. Ageing Res Rev 4: 271-287.
58. Robinson TE, Kolb B. 1997. Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J Neurosci 17: 8491-8497.
59. Robinson TE, Kolb B. 1999. Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. Eur J Neurosci 11: 1598-1564.
60. Roman O, Seres J, Pometlova M, Jurcovicova J. 2004. Neuroendocrine or behavioral effects of acute or chronic emotional stress in Wistar Kyoto (WKY) and spontaneously hypertensive (SHR) rats. Endocr Regul 38: 151-155.
61. Russell VA. 2002. Hypodopaminergic and hypernoradrenergic activity in prefrontal cortex slices of an animal model for attention-deficit hyperactivity disorder-The spontaneously hypertensive rat. Behav Brain Res 130: 191-196.
62. Sabbatini M, Strocchi P, Vitaioli L, Amenta F. 2000. The hippocampus in spontaneously hypertensive rats: A quantitative microanatomical study. Neuroscience 100: 251-258.
63. Sabbatini M, Catalani A, Consoli C, Marletta N, Tomassoni D, Avola R. 2002. The hippocampus in spontaneously hypertensive rats: An animal model of vascular dementia? Mech Ageing Dev 123: 547-559.
64. Seib LM, Wellman CL. 2003. Daily injections alter spine density in rat medial prefrontal cortex. Neurosci Lett 337: 29-32.
65. Seress L, Abraham H, Lin H, Totterdell S. 2002. Nitric oxide-containing pyramidal neurons of the subiculum innervate the CA1 area. Exp Brain Res 147: 38-44.
66. Sesack SR, Pickel VM. 1992. Prefrontal cortical efferents in the rat synapse on unlabeled neurons of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J Comp Neurol 320: 145-160.
67. Sholl DA. 1953. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87: 387-406.
68. 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.
69. Solis O, Limón DI, Flores-Hernández J, Flores G. 2007. Alterations in dendritic morphology of the prefrontal cortical and striatum neurons in the unilateral 6-OHDA-rat model of Parkinson's disease. Synapse 61: 450-458.
70. Solis 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.
71. Spieker LE, Flammer AJ, Lüscher TF. 2006. The vascular endothelium in hypertension. Handb Exp Pharmacol 176: 249-283.
72. Sutterer JR, Perry J, Devito W. 1980. Two-way shuttlebox avoidance in the spontaneously hypertensive and normotensive rat. J Comp Physiol Psychol 94: 155-163.
73. Sutterer JR, Devito WJ, Rykaszewski I. 1981. Developmental aspect of 2-way shuttle box avoidance in the spontaneously hypertensive rat and normotensive rat. Dev Psychobiol 14: 405-414.
74. Suzuki WA. 2009. Perception and the medial temporal lobe: Evaluating the current evidence. Neuron 61: 657-666.
75. Tayebati SK, Di Tullio MA, Tomassoni D, Amenta F. 2009. Neuroprotective effect of treatment with galantamine and choline alphoscerate on brain microanatomy in spontaneously hypertensive rats. J Neurol Sci 283: 187-194.
76. Terry AV, Hernandez CM, Buccafusco JJ, Gattu M. 2000. Deficits in spatial learning and nicotinic-acetylcholine receptors in older, spontaneously hypertensive rats. Neurosci 101: 357-368.
77. Tomassoni D, Avola R, Di Tullio MA, Sabbatini M, Vitaioli L, Amenta F. 2004. Increased expression of glial fibrillary acidic protein in the brain of spontaneously hypertensive rats. Clin Exp Hypertens 26: 335-350.
78. Tongiorgi E, Domenici L, Simonato M. 2006. What is the biological significance of BDNF mRNA targeting in the dendrites? Clues from epilepsy and cortical development. Mol Neurobiol 33: 17-32.
79. Török J. 2008. Participation of nitric oxide in different models of experimental hypertension. Physiol Res 57: 813-825.
80. Török J, Kristek F. 2001. Functional and morphological pattern of vascular responses in two models of experimental hypertension. Exp Clin Cardiol 6: 142-148.
81. 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.
82. Vertes RP. 2006. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142: 1-20.
83. Vanhoutte PM, Lüscher TF, Gräser T. 1991. Endothelium-dependent contractions. Blood Vessels 28: 74-83.
84. Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S. 2002. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22: 6810-6818.
85. Wu CC, Yen MH. 1999. Higher level of plasma nitric oxide in spontaneously hypertensive rats. Am J Hypertens 12: 476-482.
86. Wyss JM, Fisk G, van Groen T. 1992. Impaired learning and memory in mature spontaneously hypertensive rats. Brain Res 592: 135-140.