Rodent Model of Infant Attachment Learning and Stress

Nathan Kline Institute for Psychiatric Research and Child & Adolescent Psychiatry, New York University School of Medicine, Orangeburg, NY 10962, USA.
Developmental Psychobiology (Impact Factor: 3.31). 11/2010; 52(7):651-60. DOI: 10.1002/dev.20482
Source: PubMed


Here we review the neurobiology of infant odor learning in rats, and discuss the unique role of the stress hormone corticosterone (CORT) in the learning necessary for the developing rat. During the first 9 postnatal (PN) days, infants readily learn odor preferences, while aversion and fear learning are attenuated. Such restricted learning may ensure that pups only approach their mother. This sensitive period of preference learning overlaps with the stress hyporesponsive period (SHRP, PN4-14) when pups have a reduced CORT response to most stressors. Neural underpinnings responsible for sensitive-period learning include increased activity within the olfactory bulb and piriform "olfactory" cortex due to heightened release of norepinephrine from the locus coeruleus. After PN10 and with the decline of the SHRP, stress-induced CORT release permits amygdala activation and facilitates learned odor aversions and fear. Remarkably, odor preference and attenuated fear learning can be reestablished in PN10-15 pups if the mother is present, an effect due to her ability to suppress pups' CORT and amygdala activity. Together, these data indicate that functional changes in infant learning are modified by a unique interaction between the developing CORT system, the amygdala, and maternal presence, providing a learning system that becomes more flexible as pups mature.


Available from: Tania L Roth, Mar 21, 2014
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    • "The critical value of this relationship for survival qualifies the caregiver as a species - expected stimulus for the infant . Therefore , the infant , regardless of rodent , non - human primate , or human , has the same goal , which is to ensure proximity to the caregiver ( Ainsworth , 1969 ; Bowlby , 1982 ; Moriceau & Roth , 2010 ) . If the caregiver is a species - expected stimulus , then premature separation or near complete deprivation in the infant period should have devastating consequences on the developmental trajectory of systems that require maternal presence . "
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    ABSTRACT: Early-life caregiving shapes the architecture and function of the developing brain. The fact that the infant-caregiver relationship is critically important for infant functioning across all altricial species, and that the anatomical circuits supporting emotional functioning are highly preserved across different species, suggests that the results of studies examining the role of early adversity and emotional functioning should be translatable across species. Here we present findings from four different research laboratories, using three different species, which have converged on a similar finding: adversity accelerates the developmental trajectory of amygdala-prefrontal cortex (PFC) development and modifies emotional behaviors. First, a rodent model of attachment learning associated with adversity is presented showing precocial disruption of attachment learning and emergence of heightened fear learning and emotionality. Second, a model of infant-mother separation is presented in which early adversity is shown to accelerate the developmental emergence of adult-like fear retention and extinction. Third, a model of early life adversity in Rhesus monkeys is presented in which a naturally occurring variation in maternal-care (abuse) is shown to alter the functioning of emotion circuits. Finally, a human model of maternal deprivation is presented in which children born into orphanages and then adopted abroad exhibit aberrant development of emotion circuits. The convergence of these cross-species studies on early life adversity suggests that adversity targets the amygdala and PFC and has immediate impact on infant behavior with the caregiver, and emotional reactions to the world. These results provide insight into mechanisms responsible for caregiver induced mental health trajectory alterations. © 2014 Wiley Periodicals, Inc. Dev Psychobiol
    Developmental Psychobiology 12/2014; 56(8). DOI:10.1002/dev.21260 · 3.31 Impact Factor
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    • "During the first 10 days of the neonatal rat's life ( " sensitive period " ), pups learn to approach and prefer a novel, artificial odor, even when it is paired with painful sensory stimuli, such as tail pinches or moderate (.5 mA) electric shocks (Camp & Rudy, 1988; Sullivan, Brake et al., 1986; Sullivan, Hofer et al., 1986; Sullivan et al., 2000). Pain-induced odor preference learning of rat pups is neither due to the pups' inability to detect pain nor to differences in their pain threshold (Barr, 1995; Moriceau et al., 2010). "
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    ABSTRACT: Childhood maltreatment is associated with adverse brain development and later life psychiatric disorders, with maltreatment from the caregiver inducing a particular vulnerability to later life psychopathologies. Here we review two complementary rodent models of early life abuse, which are used to examine the infant response to trauma within attachment and the developmental trajectories that lead to later life neurobehavioral deficits. These rodent models include being reared with an abusive mother, and a more controlled attachment-learning paradigm using odor-shock conditioning to produce a new maternal odor. In both of these rodent models, pups learn a strong attachment and preference to the maternal odor. However, both models produce similar enduring neurobehavioral deficits, which emerge with maturation. Importantly, cues associated with our models of abuse serve as paradoxical safety signals, by normalizing enduring neurobehavioral deficits following abuse. Here we review these models and explore implications for human interventions for early life maltreatment. © 2014 Wiley Periodicals, Inc. Dev Psychobiol 9999: XX–XX, 2014.
    Developmental Psychobiology 12/2014; 56(8). DOI:10.1002/dev.21219 · 3.31 Impact Factor
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    • "However, the roles of stress, glucocorticoids, and NE have been well characterized in neonatal olfactory learning. Critical periods both overlap with and are dependent upon levels of corticosterone, stress, and specifically NE release into the OB (Moriceau and Sullivan, 2004; Moriceau et al., 2009, 2010). In adults, the application of an acute stressor that activates the LC (Valentino and Van Bockstaele, 2008), such as a bright light or sound, or a context that modifies the arousal of the animal can affect memory consolidation and recall, although the precise effects depend on the timing, context, intensity and duration of the stressor involved (reviewed in Joels et al., 2006; Sandi and Pinelo-Nava, 2007). "
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    ABSTRACT: Non-associative habituation and odor recognition tasks have been widely used to probe questions of social recognition, odor memory duration, and odor memory specificity. Among others, these paradigms have provided valuable insight into how neuromodulation, and specifically norepinephrine/noradrenaline (NE) influences odor memory. In general, NE levels are modulated by arousal, stress, and behavioral state, but there is sparse evidence of a direct relationship between NE and odor memory in adult rodents. The present study uses simple mild psychological stressors (bright light and sound) to modulate NE levels physiologically in order to probe stressors NE-dependent effect on odor recognition memory. In rats with bilateral bulbar cannulations, we show that these stressors modulate olfactory memory and that this effect is at least partially mediated by the olfactory bulb. Specifically, we show that the presence of stressors during the acquisition of odor memory suppresses memory for an odor when tested 30 min after familiarization to that odor. This suppression is blocked by infusing NE antagonists into the olfactory bulb prior to odor acquisition. Additionally, we find that infusion of bulbar NE is sufficient to suppress odor memory in a manner mimicking that of our stressors. These effects are unlikely to be solely mediated by locomotor/exploratory changes produced by stressors, although these stressors influence certain behaviors not directly related to odor investigation. This study provides important information about how behaviorally relevant changes in NE can influence top-down sensory processing and odor memory.
    Frontiers in Integrative Neuroscience 12/2013; 7:97. DOI:10.3389/fnint.2013.00097
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