Infantile amnesia reflects a developmental critical period for hippocampal learning

Nature Neuroscience

Volumn 19, Issue 9, 2016, Pages 1225-1233

  Travaglia, Alessio ^a   Bisaz, Reto ^a   Sweet, Eric S ^b   Blitzer, Robert D ^b   Alberini, Cristina M ^a  

^a NEW YORK UNIVERSITY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; METABOTROPIC RECEPTOR 5; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ADULT; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; EPISODIC MEMORY; HIPPOCAMPUS; INFANT DISEASE; INFANTILE AMNESIA; LATENT PERIOD; LEARNING; LONG TERM MEMORY; MEMORY CONSOLIDATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ANIMAL; FEMALE; GROWTH, DEVELOPMENT AND AGING; LONG EVANS RAT; MALE; MEMORY; METABOLISM; NERVE CELL NETWORK; PATHOPHYSIOLOGY; PHYSIOLOGY;

AMNESIA; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; FEMALE; HIPPOCAMPUS; LEARNING; MALE; MEMORY; NERVE NET; RATS, LONG-EVANS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84978771828     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4348     Document Type: Article

References (50)

1. Campbell B.A, & Spear N.E. Ontogeny of memory. Psychol. Rev. 79, 215-236 (1972).
2. Hayne H. Infant memory development: implications for childhood amnesia. Dev. Rev. 24, 33-73 (2004).
3. Rovee-Collier C. The development of infant memory. Curr. Dir. Psychol. Sci. 8, 80-85 (1999).
4. Heim C, & Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 49, 1023-1039 (2001).
5. Dumas T.C, & Rudy J.W. Development of the hippocampal memory system: creating networks and modifiable synapses. in Oxford Handbook of Developmental Behavioral Neuroscience (eds. Blumberg M.S, Freeman J.H, & Robinson S.R.) (Oxford, 2010).
6. Nelson C.A. Neural plasticity in human development: the role of early experience in sculpting memory systems. Dev. Sci. 3, 115-136 (2000).
7. Akers K.G, et al. Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science 344, 598-602 (2014).
8. Callaghan B.L, Li S, & Richardson R. The elusive engram: what can infantile amnesia tell us about memory?. Trends Neurosci. 37, 47-53 (2014).
9. Kim J.H, McNally G, & Richardson R. Recovery of fear memories in rats: role of gamma-Amino butyric acid (GABA) in infantile amnesia. Behav. Neurosci. 120, 40-48 (2006).
10. Campbell B.A, & Jaynes J. Reinstatement. Psychol. Rev. 73, 478-480 (1966).
11. Spear N.E, & Parsons P.J. Analysis of a reactivation treatment: ontogenetic determinants of alleviated forgetting. in Processes in Animal Memory (eds. Medin D.L, Roberts W.A, & Davis R.T.) 135-165 (Lawrence Erlbaum Associates, 1976).
12. Haroutunian V, & Riccio D.C. Effect of arousal conditions during reinstatement treatment upon learned fear in young rats. Dev. Psychobiol. 10, 25-32 (1977).
13. Davis J.M, & Rovee-Collier C.K. Alleviated forgetting of a learned contingency in 8-week-old infants. Dev. Psychol. 19, 353-365 (1983).
14. Campbell B.A, & Campbell E.H. Retention and extinction of learned fear in infant and adult rats. J. Comp. Physiol. Psychol. 55, 1-8 (1962).
15. Rudy J.W, & Morledge P. Ontogeny of contextual fear conditioning in rats: implications for consolidation, infantile amnesia, and hippocampal system function. Behav. Neurosci. 108, 227-234 (1994).
16. Squire L.R, Wixted J.T, & Clark R.E. Recognition memory and the medial temporal lobe: a new perspective. Nat. Rev. Neurosci. 8, 872-883 (2007).
17. Chen D.Y, Bambah-Mukku D, Pollonini G, & Alberini C.M. Glucocorticoid receptors recruit the CaMKII?-BDNF-CREB pathways to mediate memory consolidation. Nat. Neurosci. 15, 1707-1714 (2012).
18. Raineki C, et al. Functional emergence of the hippocampus in context fear learning in infant rats. Hippocampus 20, 1037-1046 (2010).
19. Foster J.A, & Burman M.A. Evidence for hippocampus-dependent contextual learning at postnatal day 17 in the rat. Learn. Mem. 17, 259-266 (2010).
20. Robinson-Drummer P.A, & Stanton M.E. Using the context preexposure facilitation effect to study long-Term context memory in preweanling, juvenile, adolescent, and adult rats. Physiol. Behav. 148, 22-28 (2015).
21. Minichiello L. TrkB signaling pathways in LTP and learning. Nat. Rev. Neurosci. 10, 850-860 (2009).
22. Morris R.G, Anderson E, Lynch G.S, & Baudry M. Selective impairment of learning and blockade of long-Term potentiation by an N-methyl-D-Aspartate receptor antagonist, AP5. Nature 319, 774-776 (1986).
23. Tsien J.Z, Huerta P.T, & Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87, 1327-1338 (1996).
24. Constantine-Paton M, Cline H.T, & Debski E. Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annu. Rev. Neurosci. 13, 129-154 (1990).
25. Sans N, et al. A developmental change in NMDA receptor-Associated proteins at hippocampal synapses. J. Neurosci. 20, 1260-1271 (2000).
26. Paoletti P, Bellone C, & Zhou Q. NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat. Rev. Neurosci. 14, 383-400 (2013).
27. Hensch T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6, 877-888 (2005).
28. Bellone C, & Nicoll R.A. Rapid bidirectional switching of synaptic NMDA receptors. Neuron 55, 779-785 (2007).
29. Carmignoto G, & Vicini S. Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258, 1007-1011 (1992).
30. Quinlan E.M, Philpot B.D, Huganir R.L, & Bear M.F. Rapid, experiencedependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat. Neurosci. 2, 352-357 (1999).
31. Philpot B.D, Sekhar A.K, Shouval H.Z, & Bear M.F. Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex. Neuron 29, 157-169 (2001).
32. Caldeira M.V, et al. BDNF regulates the expression and traffic of NMDA receptors in cultured hippocampal neurons. Mol. Cell. Neurosci. 35, 208-219 (2007).
33. Liu L, et al. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304, 1021-1024 (2004).
34. Yashiro K, & Philpot B.D. Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology 55, 1081-1094 (2008).
35. Matta J.A, Ashby M.C, Sanz-Clemente A, Roche K.W, & Isaac J.T. mGluR5 and NMDA receptors drive the experience- And activity-dependent NMDA receptor NR2B to NR2A subunit switch. Neuron 70, 339-351 (2011).
36. Huang Z.J, et al. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98, 739-755 (1999).
37. Gianfranceschi L, et al. Visual cortex is rescued from the effects of dark rearing by overexpression of BDNF. Proc. Natl. Acad. Sci. USA 100, 12486-12491 (2003).
38. Schulenburg C.J, Riccio D.C, & Stikes E.R. Acquisition and retention of a passiveavoidance response as a function of age in rats. J. Comp. Physiol. Psychol. 74, 75-83 (1971).
39. Balsam P.D, Drew M.R, & Gallistel C.R. Time and associative learning. Comp. Cogn. Behav. Rev. 5, 1-22 (2010).
40. Cull-Candy S, Brickley S, & Farrant M. NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol. 11, 327-335 (2001).
41. Gambrill A.C, & Barria A. NMDA receptor subunit composition controls synaptogenesis and synapse stabilization. Proc. Natl. Acad. Sci. USA 108, 5855-5860 (2011).
42. Dumas T.C. Developmental regulation of cognitive abilities: modified composition of a molecular switch turns on associative learning. Prog. Neurobiol. 76, 189-211 (2005).
43. Berardi N, Pizzorusso T, & Maffei L. Critical periods during sensory development. Curr. Opin. Neurobiol. 10, 138-145 (2000).
44. Castrén M.L, & Castrén E. BDNF in fragile X syndrome. Neuropharmacology 76, 729-736 (2014).
45. Greenough W.T, Black J.E, & Wallace C.S. Experience and brain development. Child Dev. 58, 539-559 (1987).
46. Nelson C.A. III et al. Cognitive recovery in socially deprived young children: the Bucharest Early Intervention Project. Science 318, 1937-1940 (2007).
47. Anand K.J, Coskun V, Thrivikraman K.V, Nemeroff C.B, & Plotsky P.M. Longterm behavioral effects of repetitive pain in neonatal rat pups. Physiol. Behav. 66, 627-637 (1999).
48. Zhao M.G, et al. Roles of NMDA NR2B subtype receptor in prefrontal long-Term potentiation and contextual fear memory. Neuron 47, 859-872 (2005).
49. Qi C, et al. mGluR5 in the nucleus accumbens shell regulates morphine-Associated contextual memory through reactive oxygen species signaling. Addict. Biol. 20, 927-940 (2015).
50. Rudy J.W, & Matus-Amat P. DHPG activation of group 1 mGluRs in BLA enhances fear conditioning. Learn. Mem. 16, 421-425 (2009).