Prenatal protein malnutrition alters the proportion but not numbers of parvalbuminimmunoreactive interneurons in the hippocampus of the adult sprague-Dawley rat

Nutritional Neuroscience

Volumn 14, Issue 4, 2011, Pages 165-178

  Lister, James P ^a   Blatt, Gene J ^a   Kemper, Thomas L ^a   Tonkiss, John ^a   Debassio, William A ^a   Galler, Janina R ^b   Rosene, Douglas L ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

CA1 subfield; CA3 subfield; Hemispheric asymmetry; Inhibition; Stereology; Undernutrition

Indexed keywords

PARVALBUMIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ASYMMETRY; CELL COUNT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENTATE HILUS; FEMALE; GABAERGIC SYSTEM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; IMMUNOREACTIVITY; INTERNEURON; LEFT HEMISPHERE; MALE; MATERNAL NUTRITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MALNUTRITION; RAT; RIGHT HEMISPHERE; STEREOLOGY; STRATUM PYRAMIDALE; SUBICULUM;

ANIMALS; DENTATE GYRUS; FEMALE; INTERNEURONS; MALE; NEURONS; PARVALBUMINS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROTEIN-ENERGY MALNUTRITION; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 84856482152     PISSN: 1028415X     EISSN: 14768305     Source Type: Journal    
DOI: 10.1179/147683011X13009738172396     Document Type: Article

References (54)

1. Lister JP, Tonkiss J, Blatt GJ, Kemper TL, Debassio WA, Galler JR, et al. Asymmetry of neuron numbers in the hippocampal formation of prenatally malnourished and normally nourished rats: a stereological investigation. Hippocampus 2006;16(11):946-58.
2. Galler JR, Shumsky JS, Morgane PJ. Malnutrition and brain development. In: Walker W, Watkins J, (eds.) Nutrition in pediatrics. Neuilly-sur-Seine, France: B.C. Decker, Inc.; 1996. p. 196-212.
3. Morgane PJ, Mokler DJ, Galler JR. Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci Biobehav Rev 2002;26(4):471-83.
4. Tonkiss J, Galler J, Morgane PJ, Bronzino JD, Austin-LaFrance RJ. Prenatal protein malnutrition and postnatal brain function. Ann N Y Acad Sci 1993;678:215-27.
5. Austin KB, Bronzino J, Morgane PJ. Prenatal protein malnutrition affects synaptic potentiation in the dentate gyrus of rats in adulthood. Brain Res 1986;394(2):267-73.
6. Bronzino JD, Austin-LaFrance RJ, Mokler D, Morgane PJ. Effects of prenatal protein malnutrition on hippocampal longterm potentiation in freely moving rats. Exp Neurol 1997; 148(1):317-23.
7. Zhang Y, Li N, Yang Z. Perinatal food restriction impaired spatial learning and memory behavior and decreased the density of nitric oxide synthase neurons in the hippocampus of adult male rat offspring. Toxicology Letters 2010;193(2):167-72.
8. Tonkiss J, Galler JR, Formica RN, Shukitt-Hale B, Timm RR. Fetal protein malnutrition impairs acquisition of a DRL task in adult rats. Physiol Behav 1990;48(1):73-7.
9. Tonkiss J, Shultz PL, Shumsky JS, Fiacco TA, Vincitore M, Rosene DL, et al. Chlordiazepoxide-induced spatial learning deficits: dose-dependent differences following prenatal malnutrition. Pharmacol Biochem Behav 2000;65(1):105-16.
10. Tonkiss J, Trzcinska M, Shultz PL, Vincitore M, Galler JR. Prenatally protein malnourished rats are less sensitive to the amnestic effects of medial septal infusions of chlordiazepoxide. Behav Pharmacol 2000;11(6):437-46.
11. Austin-LaFrance RJ, Morgane PJ, Bronzino JD. Prenatal protein malnutrition and hippocampal functioning: rapid kindling. Brain Res Bull 1991;27(6):815-8.
12. Bronzino JD, Austin-LaFrance RJ, Morgane PJ, Galler JR. Effects of prenatal protein malnutrition on kindling-induced alterations in dentate granule cell excitability. II. Paired-pulse measures. Exp Neurol 1991;112(2):216-23.
13. Austin KB, Beiswanger C, Bronzino JD, Austin-LaFrance RJ, Galler JR, Morgane PJ. Prenatal protein malnutrition alters behavioral state modulation of inhibition and facilitation in the dentate gyrus. Brain Res Bull 1992;28(2):245-55.
14. Bronzino JD, Blaise JH, Mokler DJ, Galler JR, Morgane PJ. Modulation of paired-pulse responses in the dentate gyrus: effects of prenatal protein malnutrition. Brain Res 1999; 849(1-2):45-57.
15. Luebke J, St John J, Galler JR. Prenatal protein malnutrition results in increased frequency of miniature inhibitory synaptic currents in rat CA1 pyramidal cells. Synapse 2000;37(1):23-31.
16. Chang YM, Galler JR, Luebke JI. Prenatal protein malnutrition results in increased frequency of miniature inhibitory postsynaptic currents in rat CA3 interneurons. Nutr Neurosci 2003; 6(4):263-7.
17. Cintra L, Aguilar A, Granados L, Galvan A, Kemper T, DeBassio W, et al. Effects of prenatal protein malnutrition on hippocampal CA1 pyramidal cells in rats of four age groups. Hippocampus 1997;7(2):192-203.
18. Cintra L, Diaz-Cintra S, Galvan A, Kemper T, Morgane PJ. Effects of protein undernutrition on the dentate gyrus in rats of three age groups. Brain Res 1990;532(1-2):271-7.
19. Diaz-Cintra S, Cintra L, Galvan A, Aguilar A, Kemper T, Morgane PJ. Effects of prenatal protein deprivation on postnatal development of granule cells in the fascia dentata. J Comp Neurol 1991;310(3):356-64.
20. Freund TF, Buzsaki G. Interneurons of the hippocampus. Hippocampus 1996;6(4):347-470.
21. Klausberger T. GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus. Eur J Neurosci. 2009;30(6):947-57.
22. Díaz-Cintra S, González-Maciel A, Morales MA, Aguilar A, Cintra L, Prado-Alcalá RA. Protein malnutrition differentially alters the number of glutamic acid decarboxylase-67 interneurons in dentate gyrus and CA1-3 subfields of the dorsal hippocampus. Exp Neurol 2007;208(1):47-53.
23. Baude A, Bleasdale C, Dalezios Y, Somogyi P, Klausberger T. Immunoreactivity for the GABAA receptor alpha1 subunit, somatostatin and connexin36 distinguishes axoaxonic, basket, and bistratified interneurons of the rat hippocampus. Cereb Cortex 2007;17:2094-107.
24. Lister JP, Blatt GJ, Debassio WA, Kemper TL, Tonkiss J, Galler JR, et al. Effect of prenatal protein malnutrition on numbers of neurons in the principal cell layers of the adult rat hippocampal formation. Hippocampus 2005;15(3):393-403.
25. Rosene DL, Roy NJ, Davis BJ. A cryoprotection method that facilitates cutting frozen sections of whole monkey brains for histological and histochemical processing without freezing artifact. J Histochem Cytochem 1986;34(10):1301-15.
26. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991;231(4):482-97.
27. Katsumaru H, Kosaka T, Heizmann CW, Hama K. Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Exp Brain Res 1988;72(2):347-62.
28. Kosaka T, Katsumaru H, Hama K, Wu JY, Heizmann CW. GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 1987;419(1-2):119-30.
29. Sloviter RS. Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 1989;280(2):183-96.
30. Amaral DG, Witter MP. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 1989;31(3):571-91.
31. Rosene DL, Van Hoesen GW. The hippocampal formation of the primate brain. A review of some comparative aspects of cytoarchitecture and connections. In: Jones EG, Peters A, (eds.) Cerebral cortex. Vol. 7. New York: Plenum Publishing Corporation; 1987. p. 345-456.
32. Gundersen HJ, Jensen EB, Kieu K, Nielsen J. The efficiency of systematic sampling in stereology-reconsidered. J Microsc 1999; 193(Pt 3):199-211.
33. Gellerman LW. Chance orders of alternating stimuli in visual discrimination experiments. J Genet Psychol 1933;42:207-8.
34. Mouton PR. Principles and practices of unbiased stereology: an introduction for bioscientists. Baltimore: Johns Hopkins University Press; 2002.
35. Hedreen JC. Lost caps in histological counting methods. Anat Rec 1998;250(3):366-72.
36. Gundersen HJ. Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R, Thompson. J. Microsc 1986;143(Pt 1):3-45.
37. Sik A, Penttonen M, Ylinen A, Buzsaki G. Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci 1995;15(10):6651-65.
38. Kosaka T. Axon initial segments of the granule cell in the rat dentate gyrus: synaptic contacts on bundles of axon initial segments. Brain Res 1983;274(1):129-34.
39. Ramon Y, Cajal S. Estructura del asta de Ammon y fascia dentata. Ann Soc Esp Hist Nat 1893;22:53-114.
40. Soriano E, Frotscher M. A GABAergic axo-axonic cell in the fascia dentata controls the main excitatory hippocampal pathway. Brain Res 1989;503(1):170-4.
41. Szentagothai J, Arbib MA. Conceptual models of neural organization. Neurosci Res Program Bull 1974;12(3):305-510.
42. Li XG, Somogyi P, Tepper JM, Buzsaki G. Axonal and dendritic arborization of an intracellularly labeled chandelier cell in the CA1 region of rat hippocampus. Exp Brain Res 1992;90(3): 519-25.
43. Gilbert ME, Sui L, Walker MJ, Anderson W, Thomas S, Smoller SN, et al. Thyroid hormone insufficiency during brain development reduces parvalbumin immunoreactivity and inhibitory function in the hippocampus. Endocrinology 2007;148(1): 92-102.
44. Nomura T, Fukuda T, Aika Y, Heizmann CW, Emson PC, Kobayashi T, et al. Distribution of nonprincipal neurons in the rat hippocampus, with special reference to their dorsoventral difference. Brain Res 1997;751(1):64-80.
45. Nomura T, Fukuda T, Aika Y, Heizmann CW, Emson PC, Kobayashi T, et al. Laminar distribution of non-principal neurons in the rat hippocampus, with special reference to their compositional difference among layers. Brain Res 1997; 764(1-2):197-204.
46. Buckmaster PS, Dudek FE. Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J Comp Neurol 1997;385(3): 385-404.
47. Dinocourt C, Petanjek Z, Freund TF, Ben-Ari Y, Esclapez M. Loss of interneurons innervating pyramidal cell dendrites and axon initial segments in the CA1 region of the hippocampus following pilocarpine-induced seizures. J Comp Neurol 2003; 459(4):407-25.
48. Diamond MC, Murphy GM, Akiyama K, Johnson RE. Morphologic hippocampal asymmetry in male and female rats. Exp Neurol 1982;76(3):553-65.
49. Diamond MC, Johnson RE, Young D, Singh SS. Age-related morphologic differences in the rat cerebral cortex and hippocampus: male-female; right-left. Exp Neurol 1983;81(1):1-13.
50. Ragbetli MC, Aydinlioglu A, Kaplan S. Sex differences and right-left asymmetries in rat hippocampal components. Int J Neurosci 2002;112(1):81-95.
51. Toga AW, Thompson PM. Mapping brain asymmetry. Nat Rev Neurosci 2003;4(1):37-48.
52. Tang AC. A hippocampal theory of cerebral lateralization. In: Hugdahl K, Davidson RJ (eds.) The asymmetrical brain. Cambridge, MA: MIT Press; 2003. p. 37-68.
53. Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA. Origins of cortical interneuron subtypes. J Neurosci 2004; 24(11):2612-22.
54. Freund TF. Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 2003;26(9):489-95.