Memory of early maltreatment: Neonatal behavioral and neural correlates of maternal maltreatment within the context of classical conditioning

Department of Zoology, University of Oklahoma, Norman, Oklahoma 73019, USA.
Biological Psychiatry (Impact Factor: 10.26). 05/2005; 57(8):823-31. DOI: 10.1016/j.biopsych.2005.01.032
Source: PubMed


While children form an attachment to their abusive caregiver, they are susceptible to mental illness and brain abnormalities. To understand this important clinical issue, we have developed a rat animal model of abusive attachment where odor paired with shock paradoxically produces an odor preference. Here, we extend this model to a seminaturalistic paradigm using a stressed, "abusive" mother during an odor presentation and assess the underlying learning neural circuit.
We used a classical conditioning paradigm pairing a novel odor with a stressed mother that predominantly abused pups to assess olfactory learning in a seminaturalistic environment. Additionally, we used Fos protein immunohistochemistry to assess brain areas involved in learning this pain-induced odor preference within a more controlled maltreatment environment (odor-shock conditioning).
Odor-maternal maltreatment pairings within a seminatural setting and odor-shock pairings both resulted in paradoxical odor preferences. Learning-induced gene expression was altered in the olfactory bulb and anterior piriform cortex (part of olfactory cortex) but not the amygdala.
Infants appear to use a unique brain circuit that optimizes learned odor preferences necessary for attachment. A fuller understanding of infant brain function may provide insight into why early maltreatment affects psychiatric well-being.

Download full-text


Available from: Regina Marie Sullivan, Mar 30, 2014
    • "For example, when rat pups are young and reliant upon maternal care for survival, they learn maternal odour preference to support attachment and feeding [46]. Prior to the age of P12, rat pups will paradoxically form an odour preference if an odour is paired with an aversive stimulus, a behaviour that is thought to promote maternal attachment in the face of adversity [47] [48] [49]. At around P10 when rat pups begin to explore the extra-nest environment for the first time [50], odour aversion learning begins to emerge, which coincides with engagement of the amygdala [51] [52]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Given the profound influence that early life experiences can have upon psychosocial functioning later in life, it is intriguing that most adults fail to recall autobiographical events from their early childhood years. Infantile amnesia is the term used to describe this phenomenon of accelerated forgetting during infancy, and it is not unique to humans. Over the years, information garnered from animal studies has provided clues as to the neurobiological basis of infantile amnesia. The purpose of this review is to provide a neurobiological update on what we now know about infantile amnesia since the publication of Campbell and Spear's seminal review on the topic more than 40 years ago. We present evidence that infantile amnesia is unlikely to be explained by a unitary theory, with the protracted development of multiple brain regions and neurotransmitter systems important for learning and memory likely to be involved. The recent discovery that exposure to early life stress can alleviate infantile amnesia offers a potential explanation as to how early adversity can so profoundly affect mental health in adulthood, and understanding the neurobiological basis for this early transition may lead to the development of effective therapeutic interventions. Copyright © 2015. Published by Elsevier B.V.
    Behavioural brain research 07/2015; DOI:10.1016/j.bbr.2015.07.030 · 3.03 Impact Factor
  • Source
    • ", milk , warmth , tactile stimulation – called stroking ) but also painful stimuli ( 0 . 5 mA shock , tail pinch ) ( Haroutunian & Campbell , 1979 ; Camp & Rudy , 2004 ; Roth & Sullivan , 2005 ; Sullivan et al . , 2000 ; Takahashi et al . "
    [Show abstract] [Hide abstract]
    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
  • Source
    • "With a method previously used (Blaze et al., 2013; Roth et al., 2009) and adapted from earlier studies (Gilles et al., 1996; Ivy et al., 2008; Raineki et al., 2010; Roth & Sullivan, 2005), infant rats were divided into three equal groups on postnatal day (PN) 1 using a within litter design. For 30 min daily beginning on PN1 and ending on PN7, up to two males and two females from the same litter were exposed to either a stressed dam in a novel environment with limited nesting material (maltreatment condition) or a dam in a familiar environment with adequate nesting material (foster care condition). "
    [Show abstract] [Hide abstract]
    ABSTRACT: We have previously shown in infant rats that brief and repeated experiences with a stressed dam outside the homecage (maltreatment) alters methylation of DNA associated with the brain-derived neurotrophic factor (bdnf) gene within the developing and adult prefrontal cortex. BDNF is a key mediator of activity-dependent processes that have a profound influence on neural development and plasticity. Here we examined whether maltreatment also alters bdnf DNA methylation in two additional regions known to be prominently affected by diverse forms of early life adversity in humans- the hippocampus and amygdala. We found significant bdnf DNA methylation modifications present within the adult hippocampus (dorsal and ventral) and amygdala (central/basolateral complex). We observed that the nature of change differed between sexes, gene locus (bdnf I vs. IV), and brain region. Furthermore, a manipulation that did not produce any obvious behavior difference in infants (brief and repeated experiences with a nurturing foster dam) also had long-term effects on methylation. These data provide further empirical support of DNA methylation modifications as biological consequences of caregiving environments. © 2014 Wiley Periodicals, Inc. Dev Psychobiol
    Developmental Psychobiology 12/2014; 56(8). DOI:10.1002/dev.21218 · 3.31 Impact Factor
Show more