Early malnutrition results in long-lasting impairments in pattern-separation for overlapping novel object and novel location memories and reduced hippocampal neurogenesis

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Pérez Garciá, Georgina ^a   Guzmán Quevedo, Omar ^a   Da Silva Aragaõ, Raquel ^a   Bolanõs Jiménez, Francisco ^a  

^a Universite de Nantes   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN-DERIVED GROWTH FACTOR; EARLY GROWTH RESPONSE FACTOR 1; EGR1 PROTEIN, RAT;

ADVERSE EFFECTS; ANIMAL; COGNITION DISORDERS; COMPLICATION; DISEASE MODEL; FEMALE; GENE EXPRESSION; GENETICS; HIPPOCAMPUS; LEARNING DISORDERS; MALE; MALNUTRITION; MEMORY; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN RESTRICTION; RAT;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; COGNITION DISORDERS; DIET, PROTEIN-RESTRICTED; DISEASE MODELS, ANIMAL; EARLY GROWTH RESPONSE PROTEIN 1; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; LEARNING DISORDERS; MALE; MALNUTRITION; MEMORY; NEUROGENESIS; RATS;

EID: 84958787292     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep21275     Document Type: Article

References (60)

1. Daniels, M. C., Adair, L. S. Growth in Young Filipino Children Predicts Schooling Trajectories through High School. J Nutr. 134, 1439-1446 (2004).
2. Waber, D. P. et al. Neuropsychological outcomes at midlife following moderate to severe malnutrition in infancy. Neuropsychology 28, 530-540 (2014).
3. Galler, J. R. et al. Infant Malnutrition Is Associated with Persisting Attention Deficits in Middle Adulthood. J Nutr. 142, 788-794 (2012).
4. Laus, M. F., Duarte Manhas Ferreira Vales, L., Braga Costa, T. M., Sousa Almeida, S. Early Postnatal Protein-Calorie Malnutrition and Cognition: A Review of Human and Animal Studies. Int J Environ Res Public Health. 8, 590-612 (2011).
5. Walker, S. P., Chang, S. M., Powell, C. A., Grantham-McGregor, S. M. Effects of early childhood psychosocial stimulation and nutritional supplementation on cognition and education in growth-stunted Jamaican children: prospective cohort study. Lancet 366, 1804-1807 (2005).
6. Galler, J. R., Ramsey, F. C., Forde, V., Salt, P., Archer, E. Long-Term Effects of Early Kwashiorkor Compared with Marasmus. II. Intellectual Performance. J Pediatr Gastroenterol Nutr. 6, 847-854 (1987).
7. Stein, Z. S. M., Saenger, G., Marolla, F. Nutrition and mental performance. Science 178, 708-713. (1972).
8. de Groot, R. H. et al. Prenatal famine exposure and cognition at age 59 years. Int J Epidemiol. 40, 327-337 (2011).
9. Barnes, R. H. et al. Influence of Nutritional Deprivations in Early Life on Learning Behavior of Rats as Measured by Performance in a Water Maze. J Nutr. 89, 399-410 (1966).
10. Jordan, T. C., Cane, S. E., Howells, K. F. Deficits in spatial memory performance induced by early undernutrition. Dev Psychobiol. 14, 317-325 (1981).
11. Castro, C. A., Tracy, M., Rudy, J. W. Early-life undernutrition impairs the development of the learning and short-term memory processes mediating performance in a conditional-spatial discrimination task. Behav Brain Res. 32, 255-264 (1989).
12. Tonkiss, J., Galler, J. R. Prenatal protein malnutrition and working memory performance in adult rats. Behav Brain Res. 40, 95-107 (1990).
13. Wolf, C., Almli, C. R., Finger, S., Ryan, S., Morgane, P. J. Behavioral effects of severe and moderate early malnutrition. Physiol Behav. 38, 725-730(1986).
14. Campbell, L. F., Bedi, K. S. The effects of undernutrition during early life on spatial learning. Physiol Behav. 45, 883-890(1989).
15. Tonkiss, J., Shultz, P., Galler, J. R. An analysis of spatial navigation in prenatally protein malnourished rats. Physiol Behav. 55, 217-224(1994).
16. Strupp, B. J., Levitsky, D. A. Enduring Cognitive Effects of Early Malnutrition: A Theoretical Reappraisal. J Nutr. 125 (8 Suppl), 2221-2232 (1995).
17. Levitsky, D. A., Barnes, R. H. Effect of Early Malnutrition on the Reaction of Adult Rats to Aversive Stimuli. Nature 225, 468-469 (1970).
18. De Oliveira, L. M., Almeida, S. D. S. Effects of malnutrition and environment on the acquisition and extinction of avoidance behavior in rats. Physiol Behav. 34, 141-145 (1985).
19. Katz, H. B., Rosett, R. E., Ostwald, R. The compensatory role of food-motivation in the maze learning performance of lactationally undernourished rats. Dev Psychobiol. 12, 305-315 (1979).
20. Tonkiss, J., Shukitt-Hale, B., Formica, R. N., Rocco, F. J., Galler, J. R. Prenatal protein malnutrition alters response to reward in adult rats. Physiol Behav. 48, 675-680 (1990).
21. Diáz-Cintra, S. et al. Effects of prenatal protein deprivation on postnatal development of granule cells in the fascia dentata. J Comp Neurol. 310, 356-364 (1991).
22. Bedi, K. S. Effects of undernutrition during early life on granule cell numbers in the rat dentate gyrus. J Comp Neurol. 311, 425-433 (1991).
23. Deng, W., Aimone, J. B., Gage, F. H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11, 339-350 (2010).
24. Epp, J. R., Chow, C., Galea, L. A. M. Hippocampus-dependent learning influences hippocampal neurogenesis. Front Neurosci. 7, 57; doi: 10.3389/fnins.2013.00057 (2013).
25. Debassio, W. A., Kemper, T. L., Tonkiss, J., Galler, J. R. Effect of Prenatal Protein Deprivation on Postnatal Granule Cell Generation in the Hippocampal Dentate Gyrus. Brain Research Bulletin 41, 379-383 (1996).
26. King, R. S. et al. Effects of prenatal protein malnutrition and acute postnatal stress on granule cell genesis in the fascia dentata of neonatal and juvenile rats. Brain Res Dev Brain Res. 150, 9-15 (2004).
27. Coupé, B. et al. Perinatal Undernutrition Modifies Cell Proliferation and Brain-Derived Neurotrophic Factor Levels During Critical Time-Windows for Hypothalamic and Hippocampal Development in the Male Rat. J Neuroendocrinol. 21, 40-48 (2009).
28. Matos, R. J. B., Orozco-Solís, R., Lopes de Souza, S., Manhães-de-Castro, R., Bolanõs-Jiménez, F. Nutrient restriction during early life reduces cell proliferation in the hippocampus at adulthood but does not impair the neuronal differentiation process of the new generated cells. Neuroscience 196, 16-24 (2011).
29. Ennaceur, A., Delacour, J. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav Brain Res. 31, 47-59 (1988).
30. Ennaceur, A., Meliani, K. A new one-trial test for neurobiological studies of memory in rats. III. Spatial vs. non-spatial working memory. Behav Brain Res. 51, 83-92 (1992).
31. Gould, E., Beylin, A., Tanapat, P., Reeves, A., Shors, T. J. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2, 260-265 (1999).
32. Dobrossy, M. D. et al. Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date. Mol Psychiatry 8, 974-982 (2003).
33. Leuner, B. et al. Learning Enhances the Survival of New Neurons beyond the Time when the Hippocampus Is Required for Memory. J Neurosci. 24, 7477-7481 (2004).
34. Bekinschtein, P. et al. BDNF in the Dentate Gyrus Is Required for Consolidation of "Pattern-Separated" Memories. Cell Rep. 5, 759-768 (2013).
35. Bozon, B., Davis, S., Laroche, S. A Requirement for the Immediate Early Gene zif268 in Reconsolidation of Recognition Memory after Retrieval. Neuron 40, 695-701 (2003).
36. Gilbert, P. E., Brushfield, A. M. The role of the CA3 hippocampal subregion in spatial memory: A process oriented behavioral assessment. Prog Neuropsychopharmacol Biol Psychiatry. 33, 774-781 (2009).
37. Hartley, T., Lever, C., Burgess, N., O'Keefe, J. Space in the brain: how the hippocampal formation supports spatial cognition. Philos Trans R Soc Lond B Biol Sc. 369, 1365; doi: 10.1098/rstb.2012.0510 (2014).
38. Barker, G. R. I., Warburton, E. C. When Is the Hippocampus Involved in Recognition Memory? J Neurosci. 31, 10721-10731 (2011).
39. Marr, D. Simple Memory: A Theory for Archicortex. Philos Trans R Soc Lond B Biol Sc. 262, 23-81 (1971).
40. Willshaw, D. J., Dayan, P., Morris, R. G. M. Memory, modelling and Marr: a commentary on Marr (1971) 'Simple memory: a theory of archicortex'. Philos Trans R Soc Lond B Biol Sc. 370, 1666; doi: 1098/rstb.2014.0383 (2015).
41. Lever, C., Wills, T., Cacucci, F., Burgess, N., O'Keefe, J. Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416, 90-94 (2002).
42. Leutgeb, J. K., Leutgeb, S., Moser, M.-B., Moser, E. I. Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus. Science 315, 961-966(2007).
43. Gilbert, P. E., Kesner, R. P., DeCoteau, W. E. Memory for Spatial Location: Role of the Hippocampus in Mediating Spatial Pattern Separation. J Neurosci. 18, 804-810 (1998).
44. Clelland, C. D. et al. A Functional Role for Adult Hippocampal Neurogenesis in Spatial Pattern Separation. Science 325, 210-213 (2009).
45. Sahay, A. et al. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472, 466-470 (2011).
46. Hunsaker, M. R., Kesner, R. P. Evaluating the Differential Roles of the Dorsal Dentate Gyrus, Dorsal CA3, and Dorsal CA1 During a Temporal Ordering for Spatial Locations Task. Hippocampus 18, 955-964 (2008).
47. Haettig, J. et al. HDAC inhibition modulates hippocampus-dependent long-term memory for object location in a CBP-dependent manner. Learn Mem. 18, 71-79 (2011).
48. Sestakova, N. P. A., Kluknavsky, M., Bernatova, I. Determination of motor activity and anxiety-related behaviour in rodents: methodological aspects and role of nitric oxide. Interdiscip Toxicol. 6, 126-135 (2013).
49. Dudai, Y. The Neurobiology of Consolidations, Or, How Stable is the Engram? Annu Rev Psychol. 55, 51-86 (2004).
50. Besnard, A., Caboche, J., Laroche, S. Reconsolidation of memory: A decade of debate. Prog Neurobiol. 99, 61-80 (2012).
51. Lee, J. L. C., Everitt, B. J., Thomas, K. L. Independent Cellular Processes for Hippocampal Memory Consolidation and Reconsolidation. Science 304, 839-843 (2004).
52. Alonso, M. et al. BDNF-triggered events in the rat hippocampus are required for both short-and long-term memory formation. Hippocampus 12, 551-560 (2002).
53. Lonergan, M. E., Gafford, G. M., Jarome, T. J., Helmstetter, F. J. Time-Dependent Expression of Arc and Zif268 after Acquisition of Fear Conditioning. Neural Plast. 2010, 139891;doi:10.1155/2010/139891(2010).
54. Nakashiba, T. et al. Young Dentate Granule Cells Mediate Pattern Separation, whereas Old Granule Cells Facilitate Pattern Completion. Cell 149, 188-201 (2012).
55. Creer, D. J., Romberg, C., Saksida, L. M., van Praag, H., Bussey, T. J. Running enhances spatial pattern separation in mice. Proc Natl Acad Sci USA 107, 2367-2372 (2010).
56. Niibori, Y. et al. Suppression of adult neurogenesis impairs population coding of similar contexts in hippocampal CA3 region. Nat Commun 3, 1253; doi: 10.1038/ncomms2261 (2012).
57. Ong, T. P., Ozanne, S. E. Developmental programming of type 2 diabetes: early nutrition and epigenetic mechanisms. Curr Opin Clin Nutr Metab Care. 18, 354-360 (2015).
58. Jarome, T. J., Lubin, F. D. Epigenetic mechanisms of memory formation and reconsolidation. Neurobiol Learn Mem. 115, 116-127 (2014).
59. Yao, B., Jin, P. Unlocking epigenetic codes in neurogenesis. Genes Dev. 28, 1253-1271 (2014).
60. Pérez-Garciá, G., Guzmán-Quevedo, O., Da Silva Aragao, R., Manhaes de Castro, R., Bolanõs-Jiménez, F. Effects of early protein restriction on the plastic epigenetic responses associated with learning and memory. J Dev Orig Health Dis 4(Supplement 1), S21 (2013).