Differential effect of lithium on cell number in the hippocampus and prefrontal cortex in adult mice: A stereological study

Bipolar Disorders

Volumn 18, Issue 1, 2016, Pages 41-51

  Rajkowska, Grazyna ^a   Clarke, Gerard ^a,b   Mahajan, Gouri ^a   Licht, Camilla M M ^c   van de Werd, Henri J J M ^c   Yuan, Peter ^d   Stockmeier, Craig A ^a   Manji, Husseini K ^d,e   Uylings, Harry B M ^c  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^e JOHNSON AND JOHNSON   (United States)

Author keywords

Adult neurogenesis; Astrocytes; Bipolar disorder; Glia; Lithium; Neurons; Stereology

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; LITHIUM SALT; LITHIUM DERIVATIVE;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BIPOLAR DISORDER; BRAIN SIZE; CELL COUNT; CELL DENSITY; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; DRUG BLOOD LEVEL; GLIA CELL; GRAY MATTER; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MALE; MEDIAL PREFRONTAL CORTEX; MOUSE; NERVE CELL; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL; STEREOMETRY; ANIMAL; C57BL MOUSE; CYTOLOGY; DRUG EFFECTS; GLIA; ORGAN SIZE; PATHOLOGY; PREFRONTAL CORTEX;

ANIMALS; ASTROCYTES; BIPOLAR DISORDER; CELL COUNT; DENTATE GYRUS; HIPPOCAMPUS; LITHIUM COMPOUNDS; MALE; MICE; MICE, INBRED C57BL; NEUROGLIA; NEURONS; ORGAN SIZE; PREFRONTAL CORTEX;

EID: 84958637174     PISSN: 13985647     EISSN: 13995618     Source Type: Journal    
DOI: 10.1111/bdi.12364     Document Type: Article

References (61)

1. Rajkowska G, Halaris A, Selemon LD. Reductions in neuronal and glial density characterize the dorsolateral prefrontal cortex in bipolar disorder. Biol Psychiatry 2001; 49: 741-752.
2. Chana G, Landau S, Beasley C, Everall IP, Cotter D. 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 2003; 53: 1086-1098.
3. Moore GJ, Bebchuk JM, Wilds IB, Chen G, Manji HK. Lithium-induced increase in human grey matter. Lancet 2000; 356: 1241-1242. Erratum in: Lancet 2000; 356: 2104.
4. Moore GJ, Cortese BM, Glitz DA et al. A longitudinal study of the effects of lithium treatment on prefrontal and subgenual prefrontal gray matter volume in treatment-responsive bipolar disorder patients. J Clin Psychiatry 2009; 70: 699-705.
5. Bauer M, Grof P, Müller-Oerlingausen B. Lithium in neuropsychiatry: the comprehensive guide. London: Informa Healthcare, 2006.
6. Schloesser RJ, Martinowich K, Manji HK. Mood-stabilizing drugs: mechanisms of action. Trends Neurosci 2012; 35: 36-46.
7. Malhi GS, Tanious M, Das P, Coulston CM, Berk M. Potential Mechanisms of Action of Lithium in Bipolar Disorder. Current Understanding. CNS Drugs 2013; 27: 135-153.
8. Sassi RB, Nicoletti M, Brambilla P et al. Increased gray matter volume in lithium treated bipolar disorder patients. Neurosci Lett 2002; 329: 243-245.
9. Yucel K, McKinnon MC, Taylor VH, Macdonald K, Alda M, Young LT, MacQueen GM. Bilateral hippocampal volume increases after long-term lithium treatment in patients with bipolar disorder: a longitudinal MRI study. Psychopharmacology 2007; 195: 357-367.
10. Yucel K, Taylor VH, McKinnon MC et al. Bilateral hippocampal volume increase in patients with bipolar disorder and short-term lithium treatment. Neuropsychopharmacology 2008; 33: 361-367.
11. Monkul ES, Matsuo K, Nicoletti MA et al. Prefrontal gray matter increases in healthy individuals after lithium treatment: a voxel-based morphometry study. Neurosci Lett 2007; 429: 7-11.
12. Vernon AC, Natesan S, Crum WR et al. Contrasting effects of haloperidol and lithium on rodent brain structure: a magnetic resonance imaging study with postmortem confirmation. Biol Psychiatry 2012; 71: 855-863.
13. Chen G, Rajkowska G, Du F, Seraji-Bozorgzad N, Manji HK. Enhancement of hippocampal neurogenesis by lithium. J Neurochemistry 2000; 75: 1729-1734.
14. Son H, Yu IT, Hwang SJ et al. Lithium enhances long-term potentiation independently of hippocampal neurogenesis in the rat dentate gyrus. J Neurochem 2003; 85: 872-81. Erratum in: J Neurochem 2003; 85: 1624.
15. Kim JS, Chang MY, Yu IT et al. Lithium selectively increases neuronal differentiation of hippocampal neural progenitor cells both in vitro and in vivo. J Neurochem 2004; 89: 324-336.
16. Rajkowska G, Goldman-Rakic PS. Cytoarchitectonic definition of prefrontal areas in the normal human cortex: I. Remapping of areas 9 and 46 using quantitative criteria. Cereb Cortex 1995; 5: 307-322.
17. Rajkowska G, Miguel-Hidalgo JJ, Wei J et al. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry 1999; 45: 1085-1098.
18. Uylings HBM, Zilles K, Rajkowska G. Optimal staining methods for delineation of cortical areas and neuron counts in human brains. NeuroImage 1999; 9: 439-445.
19. Miguel-Hidalgo JJ, Rajkowska G. Immunohistochemistry of neural markers for the study of the laminar architecture in celloidin sections from the human cerebral cortex. J Neurosci Methods 1999; 93: 69-79.
20. Miguel-Hidalgo JJ, Baucom C, Dilley G et al. Glial fibrillary acidic protein immunoreactivity in the prefrontal cortex distinguishes younger from older adults in major depressive disorder. Biol Psychiatry 2000; 48: 861-873.
21. West MJ. Stereological studies of the hippocampus: a comparison of the hippocampal subdivisions of diverse species including hedgehogs, laboratory rodents, wild mice and men. Prog Brain Res 1990; 83: 13-36.
22. Slomianka L, West MJ. Comparative quantitative study of the hippocampal region of two closely related species of wild mice: interspecific and intraspecific variations in volumes of hippocampal components. J Comp Neurol 1989; 280: 544-552.
23. Van De Werd HJJM, Rajkowska G, Evers P, Uylings HBM. Cytoarchitectonic and chemoarchitectonic characterization of the prefrontal cortical areas in the mouse. Brain Struct Funct 2010; 214: 339-353.
24. Van De Werd HJJM, Uylings HBM. Comparison of (stereotactic) parcellations in mouse prefrontal cortex. Brain Struct Funct 2014; 219: 433-459.
25. Ling EA, Paterson JA, Privat A, Mori S, Leblond CP. Investigation of Glial Cells in Semithin Sections I. Identification of glial cells in the brain of young rats. J Comp Neurol 1973; 149: 43-72.
26. Thune JJ, Uylings HBM, Pakkenberg B. Total number of neurons in the prefrontal cortex in schizophrenics and controls. J Psychiatr Res 2001; 35: 15-21.
27. West MJ, Slomianka L, Gundersen HJG. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using optical fractionator. Anat Rec 1991; 231: 482-497.
28. Schmitz C. Variation of fractionator estimates and its prediction. Anat Embryol (Berl) 1998; 198: 371-397.
29. Glaser EM, Wilson PD. The coefficient of error of optical fractionator population size estimates: a computer simulation comparing three estimators. J Microsc 1998; 192: 163-171.
30. Uylings HBM, Malofeeva LI, Bogolepova IN, Jacobsen AM, Amunts K, Zilles K. No postnatal doubling of number of neurons in human Broca's area (BA 44 and 45)? A stereological study. Neuroscience 2005; 136: 715-728.
31. Cruz-Orive LM, Insausti AM, Insausti R, Crespo D. A case study from neuroscience involving stereology and multivariate analysis. In: Evans SM, Janson AM, Nyengaard Jr. eds. Quantitative Methods in Neuroscience. Oxford: Oxford University Press, 2004: 16-64.
32. Cruz-Orive LM. A general variance predictor for Cavalieri slices. J Microsc 2006; 222: 158-165.
33. Gundersen HJG. Stereology of arbitrary particles: a review of unbiased number and size estimators and presentation of some new ones, in memory of William R. Thompson. J Microsc 1986; 143: 3-45.
34. Rasch D, Kubinger KD, Moder K. The two-sample t test: pre-testing its assumptions does not pay off. Stat Papers 2011; 52: 219-231.
35. Uylings HBM, Van Eden CG, Hofman MA. Morphometry of size/volume variables and comparisons of their bivariate relations in the nervous system under different conditions. J Neurosci Methods 1986; 18: 19-37.
36. Gundersen HJG, Jensen EB. The efficiency of systematic sampling in stereology and its prediction. J Microsc 1987; 147: 229-263.
37. Gundersen HJG, Jensen EBV, Kiêu K, Nielsen J. The efficiency of systematic sampling in stereology: reconsidered. J Microsc 1999; 193: 199-211.
38. Slomianka L, West MJ. Estimators of the precision of stereological estimates: an example based on the CA1 pyramidal cell layer of rats. Neuroscience 2005; 136: 757-767.
39. García-Fiñana M, Cruz-Orive LM, Mackay CE, Pakkenberg B, Roberts N. Comparison of MR imaging against physical sectioning to estimate the volume of human cerebral compartments. NeuroImage 2003; 18: 505-516.
40. Stanton GB, Kohler SJ, Boklweski J, Cameron JL, Greenough WT. Cytogenesis in the adult monkey motor cortex: perivascular NG2 cells are the major adult born cell type. J Comp Neurol 2015; 523: 849-868.
41. Ookubo M, Kanai H, Aoki H, Yamada N. Antidepressants and mood stabilizers effects on histone deacetylase expression in C57BL/6 mice: brain region specific changes. J Psychiatr Res 2013; 47: 1204-1214.
42. Cho Y, Cavalli V. HDAC signaling in neuronal development and axon regeneration. Curr Opin Neurobiol 2014; 27: 118-126.
43. Kempermann G, Gage FH. Experience-dependent regulation of adult hippocampal neurogenesis: effects of long-term stimulation and stimulus withdrawal. Hippocampus 1999; 9: 321-332.
44. Kempermann G, Gage FH. Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. Eur J Neurosci 2002; 16: 129-136.
45. Fabricius K, Wörtwein G, Pakkenberg B. The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampus. Brain Struct Funct 2008; 212: 403-416.
46. Boekhoorn K, van Dis V, Goedknegt E, Sobel A, Lucassen PJ, Hoogenraad CC. The microtubule destabilizing protein stathmin controls the transition from dividing neuronal precursors to postmitotic neurons during adult hippocampal neurogenesis. Dev Neurobiol 2014; 74: 1226-1242.
47. Kimoto H, Eto R, Abe M, Kato H, Araki T. Alterations of glial cells in the mouse hippocampus during postnatal development. Cell Mol Neurobiol 2009; 29: 1181-1189.
48. Mouton PR, Long JM, Lei DL et al. Age and gender effects on microglia and astrocyte numbers in brains of mice. Brain Res 2002; 956: 30-35.
49. Seri B, García-Verdugo JM, McEwen BS, Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001; 21: 7153-60.
50. Song H, Stevens CF, Gage FH. Astroglia induce neurogenesis from adult neural stem cells. Nature 2002; 417: 39-44.
51. Uylings HBM, Van PJ. Measures for quantifying dendritic arborizations. Network: Computation in Neural Systems 2002; 13: 397-414.
52. Seong SS, Hammonds MD, Mervis RF. Four weeks lithium treatment alters neuronal dendrites in the rat hippocampus. Int J Neuropsychopharmacol 2013; 16: 1373-1382.
53. Altshuler LL, Bartzokis G, Grieder T et al. An MRI study of temporal lobe structures in men with bipolar disorder or schizophrenia. Biol Psychiatry 2000; 48: 147-162.
54. McDonald C, Zanelli J, Rabe-Hesketh S et al. Meta-analysis of magnetic resonance imaging brain morphometry studies in bipolar disorder. Biol Psychiatry 2004; 56: 411-417.
55. Strasser HC, Lilyestrom J, Ashby ER et al. Hippocampal and ventricular volumes in psychotic and nonpsychotic bipolar patients compared with schizophrenia patients and community control subjects: a pilot study. Biol Psychiatry 2005; 57: 633-639.
56. Hajek T, Cullis J, Novak T et al. Hippocampal volumes in bipolar disorders: opposing effects of illness burden and lithium treatment. Bipolar Disord 2012; 14: 261-270.
57. Hallahan B, Newell J, Soares JC et al. Structural magnetic resonance imaging in bipolar disorder: an international collaborative mega-analysis of individual adult patient data. Biol Psychiatry 2011; 69: 326-335.
58. Vita A, De Peri L, Sacchetti E. Gray matter, white matter, brain, and intracranial volumes in first-episode bipolar disorder: a meta-analysis of magnetic resonance imaging studies. Bipolar Disord 2009; 11: 807-814.
59. Cousins DA, Aribisala B. Nicol Ferrier I, Blamire AM. Lithium, gray matter, and magnetic resonance imaging signal. Biol Psychiatry 2013; 73: 652-657.
60. Lyoo IK, Dager SR, Kim JE et al. Lithium-induced gray matter volume increase as a neural correlate of treatment response in bipolar disorder: a longitudinal brain imaging study. Neuropsychopharmacology 2010; 35: 1743-1750.
61. Saul MC, Gessay GM, Gammie SC. A new mouse model for mania shares genetic correlates with human bipolar disorder. PLoS ONE 2012; 7 (6): e38128, doi:10.1371/journal.pone.0038128.