The neurobiology of infant maternal odor learning

Brazilian Journal of Medical and Biological Research

Volumn 43, Issue 10, 2010, Pages 914-919

  Raineki, C ^a,b,c,d,e   Pickenhagen, A ^a,b,c   Roth, T L ^d,f   Babstock, D M ^g   McLean, J H ^h   Harley, C W ^g   Lucion, A B ^e   Sullivan, R M ^a,b,c,d  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NEW YORK UNIVERSITY   (United States)

^d UNIVERSITY OF OKLAHOMA   (United States)

^e FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^f UNIVERSITY OF DELAWARE   (United States)

^g MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^h MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Amygdala; Attachment; Locus coeruleus; Maternal odor; Norepinephrine; Olfactory bulb

Indexed keywords

NORADRENALIN;

AMYGDALOID NUCLEUS; BEHAVIOR; CONDITIONING; LABORATORY; LEARNING; LOCUS CERULEUS; MATERNAL ODOR; MEDICAL RESEARCH; MOTHER CHILD RELATION; NERVE CELL PLASTICITY; NERVE POTENTIAL; NEUROBIOLOGY; NONHUMAN; ODOR; OLFACTORY BULB; REVIEW;

RATTUS;

EID: 78149270817     PISSN: 0100879X     EISSN: 1414431X     Source Type: Journal    
DOI: 10.1590/S0100-879X2010007500090     Document Type: Review

References (60)

1. Hess E. Ethology: An approach to the complete analysis of behavior. In: Brown R, Galanter E, Hess E, Mendler G (Editors), New directions in psychology. New York: Holt, Rinehart and Winston; 1962. p 159-199.
2. Lorenz KZ. Companions as factors in the bird's environment. In: Lorenz KZ (Editor), Studies in animal and human behavior. Cambridge: Harvard University Press; 1970.
3. Salzen E. Imprinting and environmental learning. In: Aron-son LR, Tobach E, Lehrman DS, Rosenblatt JS (Editors), Development and evolution of behavior. San Francisco: W.H. Freeman; 1970. p 158-178.
4. Bolhuis JJ, Honey RC. Imprinting, learning and development: from behaviour to brain and back. Trends Neurosci 1998; 21: 306-311.
5. Decasper AJ, Fifer WP. Of human bonding: newborns prefer their mothers' voices. Science 1980; 208: 1174-1176.
6. Sullivan RM, Toubas P. Clinical usefulness of maternal odor in newborns: soothing and feeding preparatory responses. Biol Neonate 1998; 74: 402-408.
7. Pedersen PE, Williams CL, Blass EM. Activation and odor conditioning of suckling behavior in 3-day-old albino rats. J Exp Psychol Anim Behav Process 1982; 8: 329-341.
8. Raineki C, Moriceau S, Sullivan RM. Developing a neurobe-havioral animal model of infant attachment to an abusive caregiver. Biol Psychiatry 2010; 67: 1137-1145.
9. Hofer MA, Shair H, Singh P. Evidence that maternal ventral skin substances promote suckling in infant rats. Physiol Behav 1976; 17: 131-136.
10. Leon M. Neuroethology of olfactory preference development. J Neurobiol 1992; 23: 1557-1573.
11. Sullivan RM, Wilson DA, Wong R, Correa A, Leon M. Modi-fed behavioral and olfactory bulb responses to maternal odors in preweanling rats. Brain Res Dev Brain Res 1990; 53: 243-247.
12. Camp LL, Rudy JW. Changes in the categorization of appetitive and aversive events during postnatal development of the rat. Dev Psychobiol 1988; 21: 25-42.
13. Johanson IB, Teicher MH. Classical conditioning of an odor preference in 3-day-old rats. Behav Neural Biol 1980; 29: 132-136.
14. McLean JH, Darby-King A, Sullivan RM, King SR. Serotoner-gic infuence on olfactory learning in the neonate rat. Behav Neural Biol 1993; 60: 152-162.
15. Raineki C, Shionoya K, Sander K, Sullivan RM. Ontogeny of odor-LiCl vs. odor-shock learning: similar behaviors but divergent ages of functional amygdala emergence. Learn Mem 2009; 16: 114-121.
16. Sullivan RM, Landers M, Yeaman B, Wilson DA. Good memories of bad events in infancy. Nature 2000; 407: 38-39.
17. Yuan Q, Harley CW, Darby-King A, Neve RL, McLean JH. Early odor preference learning in the rat: bidirectional effects of CAMP response element-binding protein (CREB) and mutant CREB support a causal role for phosphorylated CREB. J Neurosci 2003; 23: 4760-4765.
18. Spear NE, Rudy JW. Tests of the ontogeny of learning and memory: Issues, methods, and results. In: Shair HN, Barr GA, Hofer MA (Editors), Developmental psychobiology: New methods and changing concepts. New York: Oxford University Press; 1991. p 84-113.
19. Campbell BA, Spear NE. Ontogeny of memory. Psychol Rev 1972; 79: 215-236.
20. Hoffmann H, Spear NE. Facilitation and impairment of conditioning in the preweanling rat after prior exposure to the conditioned stimulus. Anim Learn Behav 1989; 17: 63-69.
21. Stanton ME, Fox GD, Carter CS. Ontogeny of the conditioned eyeblink response in rats: acquisition or expression? Neuropharmacology 1998; 37: 623-632.
22. Barr R, Marrott H, Rovee-Collier C. The role of sensory preconditioning in memory retrieval by preverbal infants. Learn Behav 2003; 31: 111-123.
23. Fanselow MS, Rudy JW. Convergence of experimental and developmental approaches to animal learning and memory processes. In: Carew TJ, Menzel R, Shatz CJ (Editors), Mechanistic relationships between development and learning. New York: J. Wiley & Sons; 1998. p 15-28.
24. Rudy JW, Morledge P. Ontogeny of contextual fear conditioning in rats: implications for consolidation, infantile amnesia, and hippocampal system function. Behav Neurosci 1994; 108: 227-234.
25. Thompson JV, Sullivan RM, Wilson DA. Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity. Brain Res 2008; 1200: 58-65.
26. Verwer RW, Van Vulpen EH, Van Uum JF. Postnatal development of amygdaloid projections to the prefrontal cortex in the rat studied with retrograde and anterograde tracers. J Comp Neurol 1996; 376: 75-96.
27. Sullivan RM, Wilson DA. The role of norepinephrine in the expression of learned olfactory neurobehavioral responses in infant rats. Psychobiology 1991; 19: 308-312.
28. Wilson DA, Sullivan RM, Leon M. Single-unit analysis of postnatal olfactory learning: modifed olfactory bulb output response patterns to learned attractive odors. J Neurosci 1987; 7: 3154-3162.
29. Woo CC, Coopersmith R, Leon M. Localized changes in olfactory bulb morphology associated with early olfactory learning. J Comp Neurol 1987; 263: 113-125.
30. Yuan Q, Harley CW, McLean JH. Mitral cell beta1 and 5-HT2A receptor colocalization and cAMP coregulation: a new model of norepinephrine-induced learning in the olfactory bulb. Learn Mem 2003; 10: 5-15.
31. Roth TL, Sullivan RM. Memory of early maltreatment: neonatal behavioral and neural correlates of maternal maltreatment within the context of classical conditioning. Biol Psychiatry 2005; 57: 823-831.
32. Johnson BA, Woo CC, Duong H, Nguyen V, Leon M. A learned odor evokes an enhanced Fos-like glomerular response in the olfactory bulb of young rats. Brain Res 1995; 699: 192-200.
33. Sullivan RM, Wilson DA, Lemon C, Gerhardt GA. Bilateral 6-OHDA lesions of the locus coeruleus impair associative olfactory learning in newborn rats. Brain Res 1994; 643: 306-309.
34. Sullivan RM, Zyzak DR, Skierkowski P, Wilson DA. The role of olfactory bulb norepinephrine in early olfactory learning. Brain Res Dev Brain Res 1992; 70: 279-282.
35. Langdon PE, Harley CW, McLean JH. Increased beta adre-noceptor activation overcomes conditioned olfactory learning defcits induced by serotonin depletion. Brain Res Dev Brain Res 1997; 102: 291-293.
36. Moriceau S, Sullivan RM. Maternal presence serves as a switch between learning fear and attraction in infancy. Nat Neurosci 2006; 9: 1004-1006.
37. McLean JH, Harley CW, Darby-King A, Yuan Q. pCREB in the neonate rat olfactory bulb is selectively and transiently increased by odor preference-conditioned training. Learn Mem 1999; 6: 608-618.
38. Yuan Q, Harley CW, Bruce JC, Darby-King A, McLean JH. Isoproterenol increases CREB phosphorylation and olfactory nerve-evoked potentials in normal and 5-HT-depleted olfactory bulbs in rat pups only at doses that produce odor preference learning. Learn Mem 2000; 7: 413-421.
39. Coopersmith R, Leon M. Enhanced neural response by adult rats to odors experienced early in life. Brain Res 1986; 371: 400-403.
40. Wilson DA, Leon M. Spatial patterns of olfactory bulb single-unit responses to learned olfactory cues in young rats. J Neurophysiol 1988; 59: 1770-1782.
41. McLean JH, Shipley MT. Postnatal development of the no-radrenergic projection from locus coeruleus to the olfactory bulb in the rat. J Comp Neurol 1991; 304: 467-477.
42. Shipley MT, Halloran FJ, de la Torre J. Surprisingly rich projection from locus coeruleus to the olfactory bulb in the rat. Brain Res 1985; 329: 294-299.
43. Moriceau S, Sullivan RM. Unique neural circuitry for neonatal olfactory learning. J Neurosci 2004; 24: 1182-1189.
44. Rangel S, Leon M. Early odor preference training increases olfactory bulb norepinephrine. Brain Res Dev Brain Res 1995; 85: 187-191.
45. Sullivan RM, Stackenwalt G, Nasr F, Lemon C, Wilson DA. Association of an odor with activation of olfactory bulb no-radrenergic beta-receptors or locus coeruleus stimulation is suffcient to produce learned approach responses to that odor in neonatal rats. Behav Neurosci 2000; 114: 957-962.
46. Ferry B, Roozendaal B, McGaugh JL. Role of norepineph-rine in mediating stress hormone regulation of long-term memory storage: a critical involvement of the amygdala. Biol Psychiatry 1999; 46: 1140-1152.
47. Moffat SD, Suh EJ, Fleming AS. Noradrenergic involvement in the consolidation of maternal experience in postpartum rats. Physiol Behav 1993; 53: 805-811.
48. Nakamura S, Kimura F, Sakaguchi T. Postnatal development of electrical activity in the locus ceruleus. J Neurophysiol 1987; 58: 510-524.
49. Vankov A, Herve-Minvielle A, Sara SJ. Response to novelty and its rapid habituation in locus coeruleus neurons of the freely exploring rat. Eur J Neurosci 1995; 7: 1180-1187.
50. Kimura F, Nakamura S. Locus coeruleus neurons in the neonatal rat: electrical activity and responses to sensory stimulation. Brain Res 1985; 355: 301-305.
51. Nakamura S, Salaguchi T. Development of plasticity of the locus coeruleus. A review of recent physiological and pharmacological experimentation. Prog Neurbiol 1990; 34: 505-526.
52. Haroutunian V, Campbell BA. Emergence of interoceptive and exteroceptive control of behavior in rats. Science 1979; 205: 927-929.
53. Barr GA. Ontogeny of nociception and antinociception. NIDA Res Monogr 1995; 158: 172-201.
54. Fitzgerald M. The development of nociceptive circuits. Nat Rev Neurosci 2005; 6: 507-520.
55. Fanselow MS, Gale GD. The amygdala, fear, and memory. Ann N Y Acad Sci 2003; 985: 125-134.
56. LeDoux JE. Emotion circuits in the brain. Annu Rev Neurosci 2000; 23: 155-184.
57. Moriceau S, Wilson DA, Levine S, Sullivan RM. Dual circuitry for odor-shock conditioning during infancy: corticosterone switches between fear and attraction via amygdala. J Neu-rosci 2006; 26: 6737-6748.
58. Collier AC, Mast J, Mayer D, Jacobs C. Approach avoidance confict in preweanling rats: A developmental study. Anim Learn Beahav 1979; 7: 514-520.
59. Martin LT, Alberts JR. Taste aversions to mother's milk: the age-related role of nursing in acquisition and expression of a learned association. J Comp Physiol Psychol 1979; 93: 430-445.
60. Shionoya K, Moriceau S, Lunday L, Miner C, Roth TL, Sullivan RM. Development switch in neural circuitry underlying odor-malaise learning. Learn Mem 2006; 13: 801-808.