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Developmental Neurobiology of the Rat Attachment System and Its Modulation by Stress

DOI: 10.3390/bs2020079

Keywords: stress, trauma, rat, pup, attachment, maternal odor, fear, amygdala, corticosterone, norepinephrine, locus coeruleus

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Abstract:

Stress is a powerful modulator of brain structure and function. While stress is beneficial for survival, inappropriate stress dramatically increases the risk of physical and mental health problems, particularly when experienced during early developmental periods. Here we focus on the neurobiology of the infant rat’s odor learning system that enables neonates to learn and approach the maternal odor and describe the unique role of the stress hormone corticosterone in modulating this odor approach learning across development. During the first nine postnatal days, this odor approach learning of infant rats is supported by a wide range of sensory stimuli and ensures attachment to the mother’s odor, even when interactions with her are occasionally associated with pain. With maturation and the emergence of a stress- or pain-induced corticosterone response, this odor approach learning terminates and a more adult-like amygdala-dependent fear/avoidance learning emerges. Strikingly, the odor approach and attenuated fear learning of older pups can be re-established by the presence of the mother, due to her ability to suppress her pups’ corticosterone release and amygdala activity. This suggests that developmental changes in stress responsiveness and the stimuli that produce a stress response might be critically involved in optimally adapting the pup’s attachment system to its respective ecological niche.

References

[1]  Kim, J.J.; Diamond, D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 2002, 3, 453–462, doi:10.1038/nrm832.
[2]  McEwen, B.S. Sex, stress and the hippocampus: Allostasis, allostatic load and the aging proces. Neurobiol. Aging 2002, 23, 921–939, doi:10.1016/S0197-4580(02)00027-1.
[3]  De Kloet, E.R.; Joels, M.; Holsboer, F. Stress and the brain: From adaptation to disease. Nat. Rev. Neurosci. 2005, 6, 463–475.
[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 2001, 49, 1023–1039.
[5]  McEwen, B.S. Stressed or stressed out: What is the difference? J. Psychiatry Neurosci. 2005, 30, 315–318.
[6]  Sandi, C.; Bisaz, R. A model for the involvement of neural cell adhesion molecules in stress-related mood disorders. Neuroendocrinology 2007, 85, 158–176, doi:10.1159/000101535.
[7]  Teicher, M.H.; Andersen, S.L.; Polcari, A.; Anderson, C.M.; Navalta, C.P. Developmental neurobiology of childhood stress and trauma. Psychiatr. Clin. North Am. 2002, 25, 397–426, doi:10.1016/S0193-953X(01)00003-X.
[8]  Caspi, A.; Sugden, K.; Moffitt, T.E.; Taylor, A.; Craig, I.W.; Harrington, H.; McClay, J.; Mill, J.; Martin, J.; Braithwaite, A.; et al. Influence of life stress on depression: Moderation by a polymorphism in the 5-HTT gene. Science 2003, 301, 386–389.
[9]  Sanchez, M.M.; Ladd, C.O.; Plotsky, P.M. Early adverse experience as a developmental risk factor for later psychopathology: Evidence from rodent and primate models. Dev. Psychopathol. 2001, 13, 419–449, doi:10.1017/S0954579401003029.
[10]  Levine, S. Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 2005, 30, 939–946, doi:10.1016/j.psyneuen.2005.03.013.
[11]  Bowlby, J. Attachment; Basic Books: New York, NY, USA, 1965.
[12]  Bowlby, J. Attachment and Loss; Basic Books: New York, NY, USA, 1969; Volume 1.
[13]  Rutter, M. Clinical implications of attachment concepts: Retrospect and prospect. J. Child Psychol. Psychiatry 1995, 36, 549–571.
[14]  Hofer, M.A.; Sullivan, S.M. Towards a neurobiology of attachment. In Handbook of Developmental Cognitive Neuroscience; Nelson, C.A., Luciana, M., Eds.; MIT Press: Cambridge, MA, USA, 2001; pp. 599–616.
[15]  Sullivan, R.M.; Holman, P.J. Transitions in sensitive period attachment learning in infancy: The role of corticosterone. Neurosci. Biobehav. Rev. 2010, 34, 835–844, doi:10.1016/j.neubiorev.2009.11.010.
[16]  Sullivan, R.M.; Toubas, P. Clinical usefulness of maternal odor in newborns: Soothing and feeding preparatory responses. Biol. Neonate 1998, 74, 402–408, doi:10.1159/000014061.
[17]  Pedersen, P.E.; Blass, E.M. Prenatal and postnatal determinants of the 1st suckling episode in albino rats. Dev. Psychobiol. 1982, 15, 349–355, doi:10.1002/dev.420150407.
[18]  Hofer, M.A.; Shair, H.; Singh, P. Evidence that maternal ventral skin substances promote suckling in infant rats. Physiol. Behav. 1976, 17, 131–136, doi:10.1016/0031-9384(76)90279-1.
[19]  Teicher, M.H.; Blass, E.M. First suckling response of the newborn albino rat: The roles of olfaction and amniotic fluid. Science 1977, 198, 635–636.
[20]  Hill, D.L.; Almli, C.R. Olfactory bulbectomy in infant rats: Survival, growth and ingestive behaviors. Physiol. Behav. 1981, 27, 811–817, doi:10.1016/0031-9384(81)90047-0.
[21]  Singh, P.J.; Tobach, E. Olfactory bulbectomy and nursing behavior in rat pups (Wistar DAB). Dev. Psychobiol. 1975, 8, 151–164, doi:10.1002/dev.420080207.
[22]  Singh, P.J.; Tucker, A.M.; Hofer, M.A. Effects of nasal ZnSO4 irrigation and olfactory bulbectomy on rat pups. Physiol. Behav. 1976, 17, 373–382, doi:10.1016/0031-9384(76)90094-9.
[23]  Leon, M.; Coopersmith, R.; Lee, S.; Sullivan, R.M.; Wilson, D.A.; Woo, C. Neural and Behavioral Plasticity Induced by Early Olfactory Learning; Academic Press: New York, NY, USA, 1987; p. 23.
[24]  Lev, R.; Orlic, D. Protein absorption by the intestine of the fetal rat in utero. Science 1972, 177, 522–524.
[25]  Narayanan, C.H.; Fox, M.W.; Hamburger, V. Prenatal development of spontaneous and evoked activity in the rat (Rattus norvegicus albinus). Behaviour 1971, 40, 100–134, doi:10.1163/156853971X00357.
[26]  Hepper, P.G.; Cleland, J. Developmental aspects of kin recognition. Genetica 1998, 104, 199–205, doi:10.1023/A:1026477724836.
[27]  Smotherman, W.P. Odor aversion learning by the rat fetus. Physiol. Behav. 1982, 29, 769–771, doi:10.1016/0031-9384(82)90322-5.
[28]  Smotherman, W.P.; Robinson, S.R. Prenatal expression of species-typical action patterns in the rat fetus (Rattus norvegicus). J. Comp. Psychol. 1987, 101, 190–196, doi:10.1037/0735-7036.101.2.190.
[29]  Smotherman, W.P.; Robinson, S.R. Prenatal influences on development: Behavior is not a trivial aspect of fetal life. J. Dev. Behav. Pediatr. 1987, 8, 171–176.
[30]  Miller, S.S.; Spear, N.E. Olfactory learning in the rat immediately after birth: Unique salience of first odors. Dev. Psychobiol. 2009, 51, 488–504, doi:10.1002/dev.20388.
[31]  Blass, E.M.; Teicher, M.H. Suckling. Science 1980, 210, 15–22.
[32]  Youngentob, S.L.; Kent, P.F.; Sheehe, P.R.; Molina, J.C.; Spear, N.E.; Youngentob, L.M. Experience-induced fetal plasticity: The effect of gestational ethanol exposure on the behavioral and neurophysiologic olfactory response to ethanol odor in early postnatal and adult rats. Behav. Neurosci. 2007, 121, 1293–1305, doi:10.1037/0735-7044.121.6.1293.
[33]  Alberts, J.R.; May, B. Nonnutritive, thermotactile induction of filial huddling in rat pups. Dev. Psychobiol. 1984, 17, 161–181, doi:10.1002/dev.420170207.
[34]  Galef, B.G., Jr.; Kaner, H.C. Establishment and maintenance of preference for natural and artificial olfactory stimuli in juvenile rats. J. Comp. Physiol. Psychol. 1980, 94, 588–595, doi:10.1037/h0077693.
[35]  Sullivan, R.M.; Wilson, D.A.; Wong, R.; Correa, A.; Leon, M. Modified behavioral and olfactory bulb responses to maternal odors in preweanling rats. Brain Res. Dev. Brain Res. 1990, 53, 243–247.
[36]  Brake, S.C. Suckling infant rats learn a preference for a novel olfactory stimulus paired with milk delivery. Science 1981, 211, 506–508.
[37]  Galef, B.G., Jr.; Sherry, D.F. Mother’s milk: A medium for transmission of cues reflecting the flavor of mother’s diet. J. Comp. Physiol. Psychol. 1973, 83, 374–378, doi:10.1037/h0034665.
[38]  Johanson, I.B.; Teicher, M.H. Classical conditioning of an odor preference in 3-day-old rats. Behav. Neural Biol. 1980, 29, 132–136, doi:10.1016/S0163-1047(80)92596-0.
[39]  McLean, J.H.; Darby-King, A.; Sullivan, R.M.; King, S.R. Serotonergic influence on olfactory learning in the neonate rat. Behav. Neural Biol. 1993, 60, 152–162, doi:10.1016/0163-1047(93)90257-I.
[40]  Sullivan, R.M.; Wilson, D.A. Neural correlates of conditioned odor avoidance in infant rats. Behav. Neurosci. 1991, 105, 307–312, doi:10.1037/0735-7044.105.2.307.
[41]  Wilson, D.A.; Sullivan, R.M. Neurobiology of associative learning in the neonate: Early olfactory learning. Behav. Neural Biol. 1994, 61, 1–18, doi:10.1016/S0163-1047(05)80039-1.
[42]  Weldon, D.A.; Travis, M.L.; Kennedy, D.A. Posttraining D1 receptor blockade impairs odor conditioning in neonatal rats. Behav. Neurosci. 1991, 105, 450–458.
[43]  Leon, M. Dietary control of maternal pheromone in the lactating rat. Physiol. Behav. 1975, 14, 311–319, doi:10.1016/0031-9384(75)90039-6.
[44]  Leon, M. The neurobiology of filial learning. Annu. Rev. Psychol. 1992, 43, 377–398, doi:10.1146/annurev.ps.43.020192.002113.
[45]  Hofer, M.; Sullivan, R. Towards a neurobiology of attachmen. In Handbook of Developmental Cognitive Neuroscience; Nelson, C.A., Luciana, M., Eds.; MIT Press: Cambridge, MA, USA, 2008; pp. 787–806.
[46]  Campbell, B.A.; Spear, N.E. Ontogeny of memory. Psychol. Rev. 1972, 79, 215–236, doi:10.1037/h0032690.
[47]  Rescorla, R.A. Behavioral studies of Pavlovian conditioning. Annu. Rev. Neurosci. 1988, 11, 329–352, doi:10.1146/annurev.ne.11.030188.001553.
[48]  Rescorla, R.A. Inhibition of delay in Pavlovian fear conditioning. J. Comp. Physiol. Psychol. 1967, 64, 114–120, doi:10.1037/h0024810.
[49]  Rush, A.N.; Robinette, B.L.; Stanton, M.E. Ontogenetic differences in the effects of unpaired stimulus preexposure on eyeblink conditioning in the rat. Dev. Psychobiol. 2001, 39, 8–18, doi:10.1002/dev.1023.
[50]  Stanton, M.E. Multiple memory systems, development and conditioning. Behav. Brain Res. 2000, 110, 25–37, doi:10.1016/S0166-4328(99)00182-5.
[51]  Stanton, M.E.; Fox, G.D.; Carter, C.S. Ontogeny of the conditioned eyeblink response in rats: Acquisition or expression? Neuropharmacology 1998, 37, 623–632, doi:10.1016/S0028-3908(98)00072-0.
[52]  Hoffmann, H.; Spear, N.E. Ontogenetic differences in conditioning of an aversion to a gustatory CS with a peripheral US. Behav. Neural Biol. 1988, 50, 16–23, doi:10.1016/S0163-1047(88)90732-7.
[53]  Raineki, C.; Shionoya, K.; Sander, K.; Sullivan, R.M. Ontogeny of odor-LiCl vs. odor-shock learning: Similar behaviors but divergent ages of functional amygdala emergence. Learn. Mem. 2009, 16, 114–121, doi:10.1101/lm.977909.
[54]  Camp, L.L.; Rudy, J.W. Changes in the categorization of appetitive and aversive events during postnatal development of the rat. Dev. Psychobiol. 1988, 21, 25–42, doi:10.1002/dev.420210103.
[55]  Moriceau, S.; Wilson, D.A.; Levine, S.; Sullivan, R.M. Dual circuitry for odor-shock conditioning during infancy: Corticosterone switches between fear and attraction via amygdala. J. Neurosci. 2006, 26, 6737–6748.
[56]  Sullivan, R.M.; Landers, M.; Yeaman, B.; Wilson, D.A. Good memories of bad events in infancy. Nature 2000, 407, 38–39.
[57]  Sullivan, R.M.; Hofer, M.A.; Brake, S.C. Olfactory-guided orientation in neonatal rats is enhanced by a conditioned change in behavioral state. Dev. Psychobiol. 1986, 19, 615–623, doi:10.1002/dev.420190612.
[58]  Raineki, C.; Pickenhagen, A.; Roth, T.L.; Babstock, D.M.; McLean, J.H.; Harley, C.W.; Lucion, A.B.; Sullivan, R.M. The neurobiology of infant maternal odor learning. Braz. J. Med. Biol. Res. 2010, 43, 914–919, doi:10.1590/S0100-879X2010007500090.
[59]  De Medeiros, C.B.; Fleming, A.S.; Johnston, C.C.; Walker, C.D. Artificial rearing of rat pups reveals the beneficial effects of mother care on neonatal inflammation and adult sensitivity to pain. Pediatr. Res. 2009, 66, 272–277, doi:10.1203/PDR.0b013e3181b1be06.
[60]  Roth, T.L.; Sullivan, R.M. Memory of early maltreatment: Neonatal behavioral and neural correlates of maternal maltreatment within the context of classical conditioning. Biol. Psychiatry 2005, 57, 823–831, doi:10.1016/j.biopsych.2005.01.032.
[61]  Sullivan, R.M.; Stackenwalt, G.; Nasr, F.; Lemon, C.; Wilson, D.A. Association of an odor with activation of olfactory bulb noradrenergic beta-receptors or locus coeruleus stimulation is sufficient to produce learned approach responses to that odor in neonatal rats. Behav. Neurosci. 2000, 114, 957–962, doi:10.1037/0735-7044.114.5.957.
[62]  Blozovski, D.; Cudennec, A. Passive avoidence learning in the young rat. Dev. Psychobiol. 1980, 13, 513–518, doi:10.1002/dev.420130510.
[63]  Collier, A.C.; Mast, J. Alleviation of avoidance deficits by approach alternatives in 10-day old rats. Physiol. Behav. 1979, 23, 615–618, doi:10.1016/0031-9384(79)90068-4.
[64]  Myslivecek, J. Inhibitory learning and memory in newborn rats. Prog. Neurobiol. 1997, 53, 399–430, doi:10.1016/S0301-0082(97)00036-1.
[65]  Barr, G.A. Ontogeny of nociception and antinociception. NIDA Res. Monogr. 1995, 158, 172–201.
[66]  Collier, A.C.; Bolles, R.C. The ontogenesis of defensive reactions to shock in preweanling rats. Dev. Psychobiol. 1980, 13, 141–150, doi:10.1002/dev.420130206.
[67]  Emerich, D.F.; Scalzo, F.M.; Enters, E.K.; Spear, N.E.; Spear, L.P. Effects of 6-hydroxydopamine-induced catecholamine depletion on shock-precipitated wall climbing of infant rat pups. Dev. Psychobiol. 1985, 18, 215–227, doi:10.1002/dev.420180303.
[68]  Fitzgerald, M. The development of nociceptive circuits. Nat. Rev. Neurosci. 2005, 6, 507–520, doi:10.1038/nrn1701.
[69]  Hess, E.H. Ethology: An approach to the complete analysis of behavior. In New Directions in Psychology; Brown, R., Galanter, E., Hess, E.H., Mendler, G., Eds.; Holt, Rinehart and Winston: New York, NY, USA, 1962; pp. 157–266.
[70]  Salzen, E.A. Imprinting and environmental learning. In Development and Evolution of Behavior; Aronson, L.R., Tobach, E., Lehrman, D.S., Rosensbaltt, J., Eds.; W H Freeman: San Francisco, CA, USA, 1970; pp. 158–178.
[71]  Rajecki, D.W.; Lamb, M.E.; Obmascher, P. Toward a general theory of infantile attachment: A comparative review of aspects of the social bond. Behav. Brain Sci. 1978, 3, 417–464.
[72]  Harlow, H.F.; Harlow, M.K. The effect of rearing conditions on behavior. Int. J. Psychiatry 1965, 1, 43–51.
[73]  Suomi, S.J. Gene-environment interactions and the neurobiology of social conflict. Ann. N. Y. Acad. Sci. 2003, 1008, 132–139, doi:10.1196/annals.1301.014.
[74]  Carlson, V.; Cicchetti, D.; Barnett, D.; Braunwald, K. Finding order in disorganization: Lessons from research on maltreated infants’ attachments to their caregivers. In Child Maltreatment: The Theory and Research on the Causes and Consequences of Child Abuse and Neglect; Cicchetti, D., Carlson, V., Eds.; Cambridge University Press: New York, NY, USA, 1990; pp. 494–528.
[75]  Kojima, S.; Alberts, J.R. Maternal care can rapidly induce an odor-guided huddling preference in rat pups. Dev. Psychobiol. 2009, 51, 95–105, doi:10.1002/dev.20349.
[76]  Kojima, S.; Alberts, J.R. Warmth from skin-to-skin contact with mother is essential for the acquisition of filial huddling preference in preweanling rats. Dev. Psychobiol. 2011, 53, 813–827, doi:10.1002/dev.20565.
[77]  Panksepp, J.; De Eskinazi, F.G. Opiates and homing. J. Comp. Physiol. Psychol. 1980, 94, 650–663, doi:10.1037/h0077708.
[78]  Sigling, H.O.; Wolterink-Donselaar, I.G.; Spruijt, B.M. Home seeking behavior in rat pups: Attachment vs. kin selection, oxytocin vs. vasopressin. Eur. J. Pharmacol. 2009, 612, 48–53, doi:10.1016/j.ejphar.2009.03.070.
[79]  Hoffman, C.M.; Flory, G.S.; Alberts, J.R. Neonatal thermotaxis improves reversal of a thermally reinforced operant response. Dev. Psychobiol. 1999, 34, 87–99, doi:10.1002/(SICI)1098-2302(199903)34:2<87::AID-DEV2>3.0.CO;2-W.
[80]  Johnson, B.A.; Woo, C.C.; 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, doi:10.1016/0006-8993(95)00896-X.
[81]  Moriceau, S.; Sullivan, R.M. Unique neural circuitry for neonatal olfactory learning. J. Neurosci. 2004, 24, 1182–1189, doi:10.1523/JNEUROSCI.4578-03.2004.
[82]  Moriceau, S.; Sullivan, R.M. Maternal presence serves as a switch between learning fear and attraction in infancy. Nat. Neurosci. 2006, 9, 1004–1006, doi:10.1038/nn1733.
[83]  Sullivan, R.M.; Leon, M. Early olfactory learning induces an enhanced olfactory bulb response in young rats. Brain Res. 1986, 392, 278–282.
[84]  Wilson, D.A.; Leon, M. Early appearance of inhibition in the neonatal rat olfactory bulb. Brain Res. 1986, 391, 289–292.
[85]  Wilson, D.A.; Sullivan, R.M. Olfactory associative conditioning in infant rats with brain stimulation as reward. I. Neurobehavioral consequences. Brain Res. Dev. Brain Res. 1990, 53, 215–221.
[86]  Wilson, D.A.; Sullivan, R.M. Olfactory associative conditioning in infant rats with brain stimulation as reward: II. Norepinephrine mediates a specific component of the bulb response to reward. Behav. Neurosci. 1991, 105, 843–849, doi:10.1037/0735-7044.105.6.843.
[87]  Wilson, D.A.; Sullivan, R.M.; Leon, M. Single-unit analysis of postnatal olfactory learning: Modified olfactory bulb output response patterns to learned attractive odors. J. Neurosci. 1987, 7, 3154–3162.
[88]  Woo, C.C.; Coopersmith, R.; Leon, M. Localized changes in olfactory bulb morphology associated with early olfactory learning. J. Comp. Neurol. 1987, 263, 113–125, doi:10.1002/cne.902630110.
[89]  Woo, C.C.; Oshita, M.H.; Leon, M. A learned odor decreases the number of Fos-immunopositive granule cells in the olfactory bulb of young rats. Brain Res. 1996, 716, 149–156, doi:10.1016/0006-8993(96)00037-6.
[90]  Raineki, C.; Moriceau, S.; Sullivan, R.M. Developing a neurobehavioral animal model of infant attachment to an abusive caregiver. Biol. Psychiatry 2010, 67, 1137–1145, doi:10.1016/j.biopsych.2009.12.019.
[91]  Yuan, Q.; Harley, C.W.; Bruce, J.C.; Darby-King, A.; McLean, J.H. 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, doi:10.1101/lm.35900.
[92]  Yuan, Q.; Harley, C.W.; McLean, J.H.; Knopfel, T. Optical imaging of odor preference memory in the rat olfactory bulb. J. Neurophysiol. 2002, 87, 3156–3159.
[93]  Sevelinges, Y.; Moriceau, S.; Holman, P.; Miner, C.; Muzny, K.; Gervais, R.; Mouly, A.M.; Sullivan, R.M. Enduring effects of infant memories: Infant odor-shock conditioning attenuates amygdala activity and adult fear conditioning. Biol. Psychiatry 2007, 62, 1070–1079, doi:10.1016/j.biopsych.2007.04.025.
[94]  Sevelinges, Y.; Sullivan, R.M.; Messaoudi, B.; Mouly, A.M. Neonatal odor-shock conditioning alters the neural network involved in odor fear learning at adulthood. Learn. Mem. 2008, 15, 649–656, doi:10.1101/lm.998508.
[95]  Sevelinges, Y.; Mouly, A.M.; Raineki, C.; Moriceau, S.; Forest, C.; Sullivan, R.M. Adult depression-like behavior, amygdala and olfactory cortex functions are restored by odor previously paired with shock during infant’s sensitive period attachment learning. Dev. Cogn. Neurosci. 2011, 1, 77–87, doi:10.1016/j.dcn.2010.07.005.
[96]  Langdon, P.E.; Harley, C.W.; McLean, J.H. Increased beta adrenoceptor activation overcomes conditioned olfactory learning deficits induced by serotonin depletion. Brain Res. Dev. Brain Res. 1997, 102, 291–293.
[97]  Sullivan, R.M.; Wilson, D.A.; Lemon, C.; Gerhardt, G.A. Bilateral 6-OHDA lesions of the locus coeruleus impair associative olfactory learning in newborn rats. Brain Res. 1994, 643, 306–309, doi:10.1016/0006-8993(94)90038-8.
[98]  Sullivan, R.M.; Zyzak, D.R.; Skierkowski, P.; Wilson, D.A. The role of olfactory bulb norepinephrine in early olfactory learning. Brain Res. Dev. Brain Res. 1992, 70, 279–282.
[99]  McLean, J.H.; Shipley, M.T. Postnatal development of the noradrenergic projection from locus coeruleus to the olfactory bulb in the rat. J. Comp. Neurol. 1991, 304, 467–477, doi:10.1002/cne.903040310.
[100]  Nakamura, S.; Kimura, F.; Sakaguchi, T. Postnatal development of electrical activity in the locus ceruleus. J. Neurophysiol. 1987, 58, 510–524.
[101]  Nakamura, S.; Sakaguchi, T. Development and plasticity of the locus coeruleus: A review of recent physiological and pharmacological experimentation. Prog. Neurobiol. 1990, 34, 505–526, doi:10.1016/0301-0082(90)90018-C.
[102]  Wilson, D.A.; Sullivan, R.M.; Leon, M. Odor familiarity alters mitral cell response in the olfactory bulb of neonatal rats. Brain Res. 1985, 354, 314–317.
[103]  Okutani, F.; Zhang, J.J.; Otsuka, T.; Yagi, F.; Kaba, H. Modulation of olfactory learning in young rats through intrabulbar GABA(B) receptors. Eur. J. Neurosci. 2003, 18, 2031–2036, doi:10.1046/j.1460-9568.2003.02894.x.
[104]  Sullivan, R.M.; Wilson, D.A. Molecular biology of early olfactory memory. Learn. Mem. 2003, 10, 1–4, doi:10.1101/lm.58203.
[105]  Price, T.L.; Darby-King, A.; Harley, C.W.; McLean, J.H. Serotonin plays a permissive role in conditioned olfactory learning induced by norepinephrine in the neonate rat. Behav. Neurosci. 1998, 112, 1430–1437, doi:10.1037/0735-7044.112.6.1430.
[106]  Okutani, F.; Zhang, J.J.; Yagi, F.; Kaba, H. Non-specific olfactory aversion induced by intrabulbar infusion of the GABA(A) receptor antagonist bicuculline in young rats. Neuroscience 2002, 112, 901–906, doi:10.1016/S0306-4522(02)00117-3.
[107]  Kehoe, P.; Blass, E.M. Behaviorally functional opioid systems in infant rats: I. Evidence for olfactory and gustatory classical conditioning. Behav. Neurosci. 1986, 100, 359–367, doi:10.1037/0735-7044.100.3.359.
[108]  Roth, T.L.; Sullivan, R.M. Endogenous opioids and their role in odor preference acquisition and consolidation following odor-shock conditioning in infant rats. Dev. Psychobiol. 2001, 39, 188–198, doi:10.1002/dev.1044.
[109]  Nelson, E.; Panksepp, J. Oxytocin mediates acquisition of maternally associated odor preferences in preweanling rat pups. Behav. Neurosci. 1996, 110, 583–592, doi:10.1037/0735-7044.110.3.583.
[110]  Scheinin, M.; Lomasney, J.W.; Hayden-Hixson, D.M.; Schambra, U.B.; Caron, M.G.; Lefkowitz, R.J.; Fremeau, R.T., Jr. Distribution of alpha 2-adrenergic receptor subtype gene expression in rat brain. Brain Res. Mol. Brain Res. 1994, 21, 133–149.
[111]  Pieribone, V.A.; Nicholas, A.P.; Dagerlind, A.; Hokfelt, T. Distribution of alpha 1 adrenoceptors in rat brain revealed by in situ hybridization experiments utilizing subtype-specific probes. J. Neurosci. 1994, 14, 4252–4268.
[112]  Rangel, S.; Leon, M. Early odor preference training increases olfactory bulb norepinephrine. Brain Res. Dev. Brain Res. 1995, 85, 187–191, doi:10.1016/0165-3806(94)00211-H.
[113]  Moriceau, S.; Shionoya, K.; Jakubs, K.; Sullivan, R.M. Early-life stress disrupts attachment learning: The role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine. J. Neurosci. 2009, 29, 15745–15755, doi:10.1523/JNEUROSCI.4106-09.2009.
[114]  Winzer-Serhan, U.H.; Raymon, H.K.; Broide, R.S.; Chen, Y.; Leslie, F.M. Expression of alpha 2 adrenoceptors during rat brain development—II. Alpha 2C messenger RNA expression and [3H]rauwolscine binding. Neuroscience 1997, 76, 261–272.
[115]  Roozendaal, B.; Okuda, S.; van der Zee, E.A.; McGaugh, J.L. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc. Natl. Acad. Sci. USA 2006, 103, 6741–6746.
[116]  Ferry, B.; McGaugh, J.L. Role of amygdala norepinephrine in mediating stress hormone regulation of memory storage. Acta Pharmacol. Sin. 2000, 21, 481–493.
[117]  McGaugh, J.L. Make mild moments memorable: Add a little arousal. Trends Cogn. Sci. 2006, 10, 345–347, doi:10.1016/j.tics.2006.06.001.
[118]  Haberly, L.B. Parallel-distributed processing in olfactory cortex: New insights from morphological and physiological analysis of neuronal circuitry. Chem. Senses 2001, 26, 551–576, doi:10.1093/chemse/26.5.551.
[119]  Schwob, J.E.; Price, J.L. The development of axonal connections in the central olfactory system of rats. J. Comp. Neurol. 1984, 223, 177–202, doi:10.1002/cne.902230204.
[120]  Wilson, D.A.; Sullivan, R.M. Cortical processing of odor objects. Neuron 2011, 72, 506–519, doi:10.1016/j.neuron.2011.10.027.
[121]  Zinyuk, L.E.; Datiche, F.; Cattarelli, M. Cell activity in the anterior piriform cortex during an olfactory learning in the rat. Behav. Brain Res. 2001, 124, 29–32, doi:10.1016/S0166-4328(01)00212-1.
[122]  Majak, K.; Ronkko, S.; Kemppainen, S.; Pitkanen, A. Projections from the amygdaloid complex to the piriform cortex: A PHA-L study in the rat. J. Comp. Neurol. 2004, 476, 414–428, doi:10.1002/cne.20233.
[123]  Swanson, L.W.; Petrovich, G.D. What is the amygdala? Trends Neurosci. 1998, 21, 323–331, doi:10.1016/S0166-2236(98)01265-X.
[124]  Wilson, D.A.; Stevenson, R.J. Olfactory perceptual learning: The critical role of memory in odor discrimination. Neurosci. Biobehav. Rev. 2003, 27, 307–328, doi:10.1016/S0149-7634(03)00050-2.
[125]  Davis, M.; Whalen, P.J. The amygdala: Vigilance and emotion. Mol. Psychiatry 2001, 6, 13–34, doi:10.1038/sj.mp.4000812.
[126]  Schwartz, C.E.; Wright, C.I.; Shin, L.M.; Kagan, J.; Whalen, P.J.; McMullin, K.G.; Rauch, S.L. Differential amygdalar response to novel versus newly familiar neutral faces: A functional MRI probe developed for studying inhibited temperament. Biol. Psychiatry 2003, 53, 854–862, doi:10.1016/S0006-3223(02)01906-6.
[127]  LeDoux, J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 2000, 23, 155–184, doi:10.1146/annurev.neuro.23.1.155.
[128]  Blanchard, D.C.; Blanchard, R.J. Innate and conditioned reactions to threat in rats with amygdaloid lesions. J. Comp. Physiol. Psychol. 1972, 81, 281–290, doi:10.1037/h0033521.
[129]  Maren, S. Neurotoxic basolateral amygdala lesions impair learning and memory but not the performance of conditional fear in rats. J. Neurosci. 1999, 19, 8696–8703.
[130]  Sah, P.; Faber, E.S.; Lopez de Armentia, M.; Power, J. The amygdaloid complex: Anatomy and physiology. Physiol. Rev. 2003, 83, 803–834.
[131]  Davis, M. The role of the amygdala in fear and anxiety. Annu. Rev. Neurosci. 1992, 15, 353–375, doi:10.1146/annurev.ne.15.030192.002033.
[132]  Cahill, L.; Weinberger, N.M.; Roozendaal, B.; McGaugh, J.L. Is the amygdala a locus of “conditioned fear”? Some questions and caveats. Neuron 1999, 23, 227–228, doi:10.1016/S0896-6273(00)80774-6.
[133]  Debiec, J.; LeDoux, J.E. Noradrenergic signaling in the amygdala contributes to the reconsolidation of fear memory: Treatment implications for PTSD. Ann. N. Y. Acad. Sci. 1071, 521–524.
[134]  Fanselow, M.S.; Gale, G.D. The amygdala, fear, and memory. Ann. N. Y. Acad. Sci. 2003, 985, 125–134, doi:10.1111/j.1749-6632.2003.tb07077.x.
[135]  Fanselow, M.S.; LeDoux, J.E. Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 1999, 23, 229–232, doi:10.1016/S0896-6273(00)80775-8.
[136]  Goosens, K.A.; Maren, S. Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learn. Mem. 2001, 8, 148–155, doi:10.1101/lm.37601.
[137]  Maren, S. The amygdala, synaptic plasticity, and fear memory. Ann. N. Y. Acad. Sci. 2003, 985, 106–113, doi:10.1111/j.1749-6632.2003.tb07075.x.
[138]  Sigurdsson, T.; Doyere, V.; Cain, C.K.; LeDoux, J.E. Long-term potentiation in the amygdala: A cellular mechanism of fear learning and memory. Neuropharmacology 2007, 52, 215–227, doi:10.1016/j.neuropharm.2006.06.022.
[139]  Phelps, E.A.; LeDoux, J.E. Contributions of the amygdala to emotion processing: From animal models to human behavior. Neuron 2005, 48, 175–187, doi:10.1016/j.neuron.2005.09.025.
[140]  Sullivan, R.M. Developing a sense of safety: The neurobiology of neonatal attachment. Ann. N. Y. Acad. Sci. 1008, 122–131.
[141]  Sullivan, R.M.; Wilson, D.A. Role of the amygdala complex in early olfactory associative learning. Behav. Neurosci. 1993, 107, 254–263, doi:10.1037/0735-7044.107.2.254.
[142]  Thompson, J.; Sullivan, R.M.; Wilson, D.A. Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity. Brain Res. 2008, 1200, 58–65.
[143]  Zhang, J.H.; Sato, M.; Tohyama, M. Region-specific expression of the mRNAs encoding beta subunits (beta 1, beta 2, and beta 3) of GABAA receptor in the rat brain. J. Comp. Neurol. 1991, 303, 637–657, doi:10.1002/cne.903030409.
[144]  Stork, O.; Ji, F.Y.; Kaneko, K.; Stork, S.; Yoshinobu, Y.; Moriya, T.; Shibata, S.; Obata, K. Postnatal development of a GABA deficit and disturbance of neural functions in mice lacking GAD65. Brain Res. 2000, 865, 45–58, doi:10.1016/S0006-8993(00)02206-X.
[145]  Duvarci, S.; Pare, D. Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J. Neurosci. 2007, 27, 4482–4491, doi:10.1523/JNEUROSCI.0680-07.2007.
[146]  Barr, G.A.; Moriceau, S.; Shionoya, K.; Muzny, K.; Gao, P.; Wang, S.; Sullivan, R.M. Transitions in infant learning are modulated by dopamine in the amygdala. Nat. Neurosci. 2009, 12, 1367–1369.
[147]  Walker, C.D.; Perrin, M.; Vale, W.; Rivier, C. Ontogeny of the stress response in the rat: Role of the pituitary and the hypothalamus. Endocrinology 1986, 118, 1445–1451, doi:10.1210/endo-118-4-1445.
[148]  Rosenfeld, P.; Ekstrand, J.; Olson, E.; Suchecki, D.; Levine, S. Maternal regulation of adrenocortical activity in the infant rat: Effects of feeding. Dev. Psychobiol. 1993, 26, 261–277, doi:10.1002/dev.420260504.
[149]  Walker, C.D.; Scribner, K.A.; Cascio, C.S.; Dallman, M.F. The pituitary-adrenocortical system of neonatal rats is responsive to stress throughout development in a time-dependent and stressor-specific fashion. Endocrinology 1991, 128, 1385–1395, doi:10.1210/endo-128-3-1385.
[150]  Dallman, M.F. Moments in time—The neonatal rat hypothalamo-pituitary-adrenal axis. Endocrinology 2000, 141, 1590–1592, doi:10.1210/en.141.5.1590.
[151]  Levine, S. Primary social relationships influence the development of the hypothalamic-pituitary-adrenal axis in the rat. Physiol. Behav. 2001, 73, 255–260, doi:10.1016/S0031-9384(01)00496-6.
[152]  Rosenfeld, P.; Suchecki, D.; Levine, S. Multifactorial regulation of the hypothalamic-pituitary-adrenal axis during development. Neurosci. Biobehav. Rev. 1992, 16, 553–568, doi:10.1016/S0149-7634(05)80196-4.
[153]  Grino, M.; Paulmyer-Lacroix, O.; Faudon, M.; Renard, M.; Anglade, G. Blockade of alpha 2-adrenoceptors stimulates basal and stress-induced adrenocorticotropin secretion in the developing rat through a central mechanism independent from corticotropin-releasing factor and arginine vasopressin. Endocrinology 1994, 135, 2549–2557, doi:10.1210/en.135.6.2549.
[154]  Gould, E.; Cameron, H.A. Early NMDA receptor blockade impairs defensive behavior and increases cell proliferation in the dentate gyrus of developing rats. Behav. Neurosci. 1997, 111, 49–56, doi:10.1037/0735-7044.111.1.49.
[155]  Takahashi, L.K. Stimulus control of behavioral inhibition in the preweanling rat. Physiol. Behav. 1994, 55, 717–721, doi:10.1016/0031-9384(94)90050-7.
[156]  Wiedenmayer, C.P.; Barr, G.A. Developmental changes in c-fos expression to an age-specific social stressor in infant rats. Behav. Brain Res. 2001, 126, 147–157, doi:10.1016/S0166-4328(01)00260-1.
[157]  Wiedenmayer, C.P.; Magarinos, A.M.; McEwen, B.S.; Barr, G.A. Age-specific threats induce CRF expression in the paraventricular nucleus of the hypothalamus and hippocampus of young rats. Horm. Behav. 2005, 47, 139–150, doi:10.1016/j.yhbeh.2004.09.001.
[158]  Upton, K.J.; Sullivan, R.M. Defining age limits of the sensitive period for attachment learning in rat pups. Dev. Psychobiol. 2010, 52, 453–464, doi:10.1002/dev.20448.
[159]  Takahashi, L.K.; Rubin, W.W. Corticosteroid induction of threat-induced behavioral inhibition in preweanling rats. Behav. Neurosci. 1993, 107, 860–866, doi:10.1037/0735-7044.107.5.860.
[160]  Rosenfeld, P.; van Eekelen, J.A.; Levine, S.; de Kloet, E.R. Ontogeny of corticosteroid receptors in the brain. Cell. Mol. Neurobiol. 1993, 13, 295–319, doi:10.1007/BF00711575.
[161]  Diorio, D.; Viau, V.; Meaney, M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J. Neurosci. 1993, 13, 3839–3847.
[162]  Alexis, M.N.; Kitraki, E.; Spanou, K.; Stylianopoulou, F.; Sekeris, C.E. Ontogeny of the glucocorticoid receptor in the rat brain. Adv. Exp. Med. Biol. 1990, 265, 269–276.
[163]  Kitraki, E.; Alexis, M.N.; Papalopoulou, M.; Stylianopoulou, F. Glucocorticoid receptor gene expression in the embryonic rat brain. Neuroendocrinology 1996, 63, 305–317, doi:10.1159/000126971.
[164]  Stutzmann, G.E.; McEwen, B.S.; LeDoux, J.E. Serotonin modulation of sensory inputs to the lateral amygdala: Dependency on corticosterone. J. Neurosci. 1998, 18, 9529–9538.
[165]  McGaugh, J.L.; Roozendaal, B. Role of adrenal stress hormones in forming lasting memories in the brain. Curr. Opin. Neurobiol. 2002, 12, 205–210, doi:10.1016/S0959-4388(02)00306-9.
[166]  Wiedenmayer, C.P.; Magarinos, A.M.; McEwen, B.S.; Barr, G.A. Mother lowers glucocorticoid levels of preweaning rats after acute threat. Ann. N. Y. Acad. Sci. 2003, 1008, 304–307.
[167]  Stanton, M.E.; Levine, S. Inhibition of infant glucocorticoid stress response: Specific role of maternal cues. Dev. Psychobiol. 1990, 23, 411–426, doi:10.1002/dev.420230504.
[168]  Suchecki, D.; Nelson, D.Y.; van Oers, H.; Levine, S. Activation and inhibition of the hypothalamic-pituitary-adrenal axis of the neonatal rat: Effects of maternal deprivation. Psychoneuroendocrinology 1995, 20, 169–182, doi:10.1016/0306-4530(94)00051-B.
[169]  Shionoya, K.; Moriceau, S.; Bradstock, P.; Sullivan, R.M. Maternal attenuation of hypothalamic paraventricular nucleus norepinephrine switches avoidance learning to preference learning in preweanling rat pups. Horm. Behav. 2007, 52, 391–400, doi:10.1016/j.yhbeh.2007.06.004.
[170]  DeVries, A.C.; Glasper, E.R.; Detillion, C.E. Social modulation of stress responses. Physiol. Behav. 2003, 79, 399–407, doi:10.1016/S0031-9384(03)00152-5.
[171]  Kikusui, T.; Winslow, J.T.; Mori, Y. Social buffering: Relief from stress and anxiety. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006, 361, 2215–2228.
[172]  Kirschbaum, C.; Prussner, J.C.; Stone, A.A.; Federenko, I.; Gaab, J.; Lintz, D.; Schommer, N.; Hellhammer, D.H. Persistent high cortisol responses to repeated psychological stress in a subpopulation of healthy men. Psychosom. Med. 1995, 57, 468–474.
[173]  Gregg, M.E.; James, J.E.; Matyas, T.A.; Thorsteinsson, E.B. Hemodynamic profile of stress-induced anticipation and recovery. Int. J. Psychophysiol. 1999, 34, 147–162, doi:10.1016/S0167-8760(99)00074-4.
[174]  Hennessy, M.B.; Nigh, C.K.; Sims, M.L.; Long, S.J. Plasma cortisol and vocalization responses of postweaning age guinea pigs to maternal and sibling separation: Evidence for filial attachment after weaning. Dev. Psychobiol. 1995, 28, 103–115, doi:10.1002/dev.420280204.
[175]  Hennessy, M.B.; Maken, D.S.; Graves, F.C. Presence of mother and unfamiliar female alters levels of testosterone, progesterone, cortisol, adrenocorticotropin, and behavior in maturing Guinea pigs. Horm. Behav. 2002, 42, 42–52, doi:10.1006/hbeh.2002.1794.
[176]  Yeh, K.Y. Corticosterone concentrations in the serum and milk of lactating rats: Parallel changes after induced stress. Endocrinology 1984, 115, 1364–1370, doi:10.1210/endo-115-4-1364.
[177]  Levine, S. Plasma-free corticosteroid response to electric shock in rats stimulated in infancy. Science 1962, 135, 795–796.
[178]  Van Oers, H.J.; de Kloet, E.R.; Li, C.; Levine, S. The ontogeny of glucocorticoid negative feedback: Influence of maternal deprivation. Endocrinology 1998, 139, 2838–2846.
[179]  Ivy, A.S.; Brunson, K.L.; Sandman, C.; Baram, T.Z. Dysfunctional nurturing behavior in rat dams with limited access to nesting material: A clinically relevant model for early-life stress. Neuroscience 2008, 154, 1132–1142, doi:10.1016/j.neuroscience.2008.04.019.
[180]  Gilles, E.E.; Schultz, L.; Baram, T.Z. Abnormal corticosterone regulation in an immature rat model of continuous chronic stress. Pediatr. Neurol. 1996, 15, 114–119, doi:10.1016/0887-8994(96)00153-1.
[181]  Rice, C.J.; Sandman, C.A.; Lenjavi, M.R.; Baram, T.Z. A novel mouse model for acute and long-lasting consequences of early life stress. Endocrinology 2008, 149, 4892–4900, doi:10.1210/en.2008-0633.
[182]  Avishai-Eliner, S.; Gilles, E.E.; Eghbal-Ahmadi, M.; Bar-El, Y.; Baram, T.Z. Altered regulation of gene and protein expression of hypothalamic-pituitary-adrenal axis components in an immature rat model of chronic stress. J. Neuroendocrinol. 2001, 13, 799–807.
[183]  Moriceau, S.; Raineki, C.; Holman, J.D.; Holman, J.G.; Sullivan, R.M. Enduring neurobehavioral effects of early life trauma mediated through learning and corticosterone suppression. Front. Behav. Neurosci. 2009, 3, doi:10.3389/neuro.08.022.2009.
[184]  Roth, T.L.; Lubin, F.D.; Funk, A.J.; Sweatt, J.D. Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol. Psychiatry 2009, 65, 760–769, doi:10.1016/j.biopsych.2008.11.028.
[185]  Avishai-Eliner, S.; Yi, S.J.; Newth, C.J.; Baram, T.Z. Effects of maternal and sibling deprivation on basal and stress induced hypothalamic-pituitary-adrenal components in the infant rat. Neurosci. Lett. 1995, 192, 49–52, doi:10.1016/0304-3940(95)11606-W.
[186]  Bale, T.L.; Baram, T.Z.; Brown, A.S.; Goldstein, J.M.; Insel, T.R.; McCarthy, M.M.; Nemeroff, C.B.; Reyes, T.M.; Simerly, R.B.; Susser, E.S.; et al. Early life programming and neurodevelopmental disorders. Biol. Psychiatry 2010, 68, 314–319.
[187]  Brunson, K.L.; Chen, Y.; Avishai-Eliner, S.; Baram, T.Z. Stress and the developing hippocampus: A double-edged sword? Mol. Neurobiol. 2003, 27, 121–136, doi:10.1385/MN:27:2:121.
[188]  Franklin, T.B.; Mansuy, I.M. The prevalence of epigenetic mechanisms in the regulation of cognitive functions and behaviour. Curr. Opin. Neurobiol. 2010, 20, 441–449, doi:10.1016/j.conb.2010.04.007.
[189]  Denenberg, V.H. Early experience and emotional development. Sci. Am. 1963, 208, 138–146, doi:10.1038/scientificamerican0663-138.
[190]  Denenberg, V.H.; Carlson, P.V.; Stephens, M.W. Effects of infantile shock upon emotionality at weaning. J. Comp. Physiol. Psychol. 1962, 55, 819–820, doi:10.1037/h0045414.
[191]  Harlow, H.F.; Harlow, M.K. The affectional systems. In Behavior of Nonhuman Primates; Schrier, A., Harlow, H.F., Stollnitz, F., Eds.; Academic Press: New York, NY, USA, 1965; Volume 2, pp. 287–344.
[192]  Levine, S. The pituitary-adrenal system and the developing brain. Prog. Brain Res. 1970, 32, 79–85, doi:10.1016/S0079-6123(08)61521-6.
[193]  Levine, S. Maternal and environmental influences on the adrenocortical response to stress in weanling rats. Science 1967, 156, 258–260.
[194]  Rosenzweig, M.R.; Bennett, E.L.; Diamond, M.C.; Wu, S.Y.; Slagle, R.W.; Saffran, E. Influences of environmental complexity and visual stimulation on development of occipital cortex in rat. Brain Res. 1969, 14, 427–445, doi:10.1016/0006-8993(69)90120-6.
[195]  Jacobson-Pick, S.; Richter-Levin, G. Differential impact of juvenile stress and corticosterone in juvenility and in adulthood, in male and female rats. Behav. Brain Res. 2010, 214, 268–276, doi:10.1016/j.bbr.2010.05.036.
[196]  Vermetten, E.; Bremner, J.D. Olfaction as a traumatic reminder in posttraumatic stress disorder: Case reports and review. J. Clin. Psychiatry 2003, 64, 202–207, doi:10.4088/JCP.v64n0214.
[197]  Kaufman, J.; Plotsky, P.M.; Nemeroff, C.B.; Charney, D.S. Effects of early adverse experiences on brain structure and function: Clinical implications. Biol. Psychiatry 2000, 48, 778–790, doi:10.1016/S0006-3223(00)00998-7.
[198]  Nemeroff, C.B. Neurobiological consequences of childhood trauma. J. Clin. Psychiatry 2004, 65, 18–28.
[199]  Teicher, M.H.; Andersen, S.L.; Polcari, A.; Anderson, C.M.; Navalta, C.P.; Kim, D.M. The neurobiological consequences of early stress and childhood maltreatment. Neurosci. Biobehav. Rev. 2003, 27, 33–44, doi:10.1016/S0149-7634(03)00007-1.
[200]  Meaney, M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 2001, 24, 1161–1192, doi:10.1146/annurev.neuro.24.1.1161.
[201]  Branchi, I.; D’Andrea, I.; Gracci, F.; Santucci, D.; Alleva, E. Birth spacing in the mouse communal nest shapes adult emotional and social behavior. Physiol. Behav. 2009, 96, 532–539, doi:10.1016/j.physbeh.2008.12.003.
[202]  Coe, C.L.; Glass, J.C.; Wiener, S.G.; Levine, S. Behavioral, but not physiological, adaptation to repeated separation in mother and infant primates. Psychoneuroendocrinology 1983, 8, 401–409, doi:10.1016/0306-4530(83)90019-7.
[203]  O’Connor, T.G.; Cameron, J.L. Translating research findings on early experience to prevention: Animal and human evidence on early attachment relationships. Am. J. Prev. Med. 2006, 31, S175–S181, doi:10.1016/j.amepre.2006.07.005.
[204]  Suomi, S.J. Early determinants of behaviour: Evidence from primate studies. Br. Med. Bull. 1997, 53, 170–184, doi:10.1093/oxfordjournals.bmb.a011598.
[205]  Gunnar, M.; Quevedo, K. The neurobiology of stress and development. Annu. Rev. Psychol. 2007, 58, 145–173, doi:10.1146/annurev.psych.58.110405.085605.
[206]  Kaffman, A.; Meaney, M.J. Neurodevelopmental sequelae of postnatal maternal care in rodents: Clinical and research implications of molecular insights. J. Child Psychol. Psychiatry 2007, 48, 224–244, doi:10.1111/j.1469-7610.2007.01730.x.
[207]  Korosi, A.; Baram, T.Z. The pathways from mother’s love to baby’s future. Front. Behav. Neurosci. 2009, 3, doi:10.3389/neuro.08.027.2009.
[208]  Pryce, C.R.; Feldon, J. Long-term neurobehavioural impact of the postnatal environment in rats: Manipulations, effects and mediating mechanisms. Neurosci. Biobehav. Rev. 2003, 27, 57–71, doi:10.1016/S0149-7634(03)00009-5.
[209]  Sanchez, M.M. The impact of early adverse care on HPA axis development: Nonhuman primate models. Horm. Behav. 2006, 50, 623–631, doi:10.1016/j.yhbeh.2006.06.012.
[210]  Tang, A.C.; Akers, K.G.; Reeb, B.C.; Romeo, R.D.; McEwen, B.S. Programming social, cognitive, and neuroendocrine development by early exposure to novelty. Proc. Natl. Acad. Sci. USA 2006, 103, 15716–15721.
[211]  Tang, A.C.; Reeb-Sutherland, B.C.; Yang, Z.; Romeo, R.D.; McEwen, B.S. Neonatal novelty-induced persistent enhancement in offspring spatial memory and the modulatory role of maternal self-stress regulation. J. Neurosci. 2011, 31, 5348–5352.
[212]  Rosenfeld, P.; Wetmore, J.B.; Levine, S. Effects of repeated maternal separations on the adrenocortical response to stress of preweanling rats. Physiol. Behav. 1992, 52, 787–791, doi:10.1016/0031-9384(92)90415-X.
[213]  Plotsky, P.M.; Meaney, M.J. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res. Mol Brain Res. 1993, 18, 195–200, doi:10.1016/0169-328X(93)90189-V.
[214]  Sapolsky, R.M. Mothering style and methylation. Nat. Neurosci. 2004, 7, 791–792, doi:10.1038/nn0804-791.
[215]  Meerlo, P.; Horvath, K.M.; Nagy, G.M.; Bohus, B.; Koolhaas, J.M. The influence of postnatal handling on adult neuroendocrine and behavioural stress reactivity. J. Neuroendocrinol. 1999, 11, 925–933.
[216]  Levine, S. The influence of social factors on the response to stress. Psychother. Psychosom. 1993, 60, 33–38, doi:10.1159/000288677.
[217]  Levine, S. The ontogeny of the hypothalamic-pituitary-adrenal axis. The influence of maternal factors. Ann. N. Y. Acad. Sci. 1994, 746, 275–288. discussion 289–293, doi:10.1111/j.1749-6632.1994.tb39245.x.
[218]  Meaney, M.J.; Bhatnagar, S.; Diorio, J.; Larocque, S.; Francis, D.; O’Donnell, D.; Shanks, N.; Sharma, S.; Smythe, J.; Viau, V. Molecular basis for the development of individual differences in the hypothalamic-pituitary-adrenal stress response. Cell. Mol. Neurobiol. 1993, 13, 321–347, doi:10.1007/BF00711576.
[219]  Sapolsky, R.M. The physiological relevance of glucocorticoid endangerment of the hippocampus. Ann. N. Y. Acad. Sci. 1994, 746, 294–304. discussion 304–297, doi:10.1111/j.1749-6632.1994.tb39247.x.
[220]  Fenoglio, K.A.; Chen, Y.; Baram, T.Z. Neuroplasticity of the hypothalamic-pituitary-adrenal axis early in life requires recurrent recruitment of stress-regulating brain regions. J. Neurosci. 2006, 26, 2434–2442, doi:10.1523/JNEUROSCI.4080-05.2006.
[221]  Andersen, S.L.; Lyss, P.J.; Dumont, N.L.; Teicher, M.H. Enduring neurochemical effects of early maternal separation on limbic structures. Ann. N. Y. Acad. Sci. 1999, 877, 756–759, doi:10.1111/j.1749-6632.1999.tb09317.x.
[222]  Caldji, C.; Diorio, J.; Meaney, M.J. Variations in maternal care alter GABA(A) receptor subunit expression in brain regions associated with fear. Neuropsychopharmacology 2003, 28, 1950–1959, doi:10.1038/sj.npp.1300237.
[223]  Cirulli, F.; Berry, A.; Alleva, E. Early disruption of the mother-infant relationship: Effects on brain plasticity and implications for psychopathology. Neurosci. Biobehav. Rev. 2003, 27, 73–82, doi:10.1016/S0149-7634(03)00010-1.
[224]  Hall, F.S.; Wilkinson, L.S.; Humby, T.; Robbins, T.W. Maternal deprivation of neonatal rats produces enduring changes in dopamine function. Synapse 1999, 32, 37–43, doi:10.1002/(SICI)1098-2396(199904)32:1<37::AID-SYN5>3.0.CO;2-4.
[225]  Higley, J.D.; Hasert, M.F.; Suomi, S.J.; Linnoila, M. Nonhuman primate model of alcohol abuse: Effects of early experience, personality, and stress on alcohol consumption. Proc. Natl. Acad. Sci. USA 1991, 88, 7261–7265.
[226]  Ladd, C.O.; Huot, R.L.; Thrivikraman, K.V.; Nemeroff, C.B.; Meaney, M.J.; Plotsky, P.M. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog. Brain Res. 2000, 122, 81–103.
[227]  Liu, D.; Diorio, J.; Day, J.C.; Francis, D.D.; Meaney, M.J. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat. Neurosci. 2000, 3, 799–806, doi:10.1038/77702.
[228]  Tyler, K.; Moriceau, S.; Sullivan, R.M.; Greenwood-van Meerveld, B. Long-term colonic hypersensitivity in adult rats induced by neonatal unpredictable vs predictable shock. Neurogastroenterol. Motil. 2007, 19, 761–768, doi:10.1111/j.1365-2982.2007.00955.x.
[229]  Tanaka, M. Emotional stress and characteristics of brain noradrenaline release in the rat. Ind. Health 1999, 37, 143–156, doi:10.2486/indhealth.37.143.
[230]  Tsuda, A.; Ida, Y.; Satoh, H.; Tsujimaru, S.; Tanaka, M. Stressor predictability and rat brain noradrenaline metabolism. Pharmacol. Biochem. Behav. 1989, 32, 569–572, doi:10.1016/0091-3057(89)90198-6.
[231]  Raineki, C.; Rincon Cortes, M.; Belnoue, L.; Sullivan, R.M. Effects of early life abuse differ across development: Infant social behavior deficits are followed by adolescent depressive-like behaviors mediated by the amygdala. J. Neurosci. 2012. in press.

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