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

Roth, Tania L.; Sullivan, Regina M.

doi:10.1016/j.biopsych.2005.01.032

Cited by 204Child Abuse and TraumaMemory and Neural MechanismsNeuroendocrine regulation and behavior

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

Roth, Tania L., Sullivan, Regina M.·2005·Biological Psychiatry

DOI 10.1016/j.biopsych.2005.01.032

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Abstract

Background 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.Methods 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).Results 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.Conclusions 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.

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The anterior piriform is activated by odors learned during the sensitive period, while the posterior piriform is engaged in response to learned odor in older pups and adults.
“In particular, the anterior piriform is activated by odors learned during this sensitive period, while the posterior piriform is engaged in response to learned odor in older pups and adults (Moriceau and Sullivan, 2006, Moriceau et al., 2006, Roth and Sullivan, 2005).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Roth and Sullivan, 2005
Once pups are born, a novel odor placed either on the mother or in the air surrounding her will readily take on the properties of maternal odor.
“Once pups are born, a new maternal odor can be rapidly learned; a novel odor (e.g. peppermint) placed either on the mother or in the air surrounding her will readily take on the properties of maternal odor (Cheslock et al., 2000, Roth and Sullivan, 2005, Sullivan et al., 1990).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Roth and Sullivan, 2005
Both natural maternal odor and a learned artificial maternal odor generate the same responses from the olfactory bulb.
“It is important to note that both natural maternal odor and a learned artificial maternal odor generate the same responses from the olfactory bulb (Raineki et al., 2010c, Roth and Sullivan, 2005).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Roth and Sullivan, 2005
Pairing painful maternal care with a novel peppermint odor does not activate the survival circuit for aversion learning; instead pups learn to approach the odor, which takes on qualities of maternal odor.
“Pairing this painful maternal care with a novel peppermint odor does not activate the important survival circuit within the brain to support aversion learning. Rather, pups not only learn to approach this odor, but this odor takes on the qualities of maternal odor to support nipple attachment and prosocial behaviors (Roth and Sullivan, 2005, Sullivan et al., 1986, Sullivan et al., 2000a).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Roth and Sullivan, 2005

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Molecular Biology Of Early Olfactory Memory: Figure 1.Preprint
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Abnormal, abusive, and stress-related behaviors in baboon mothers
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Ecology and Experience
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Habituation of the forelimb-withdrawal response in neonatal rats.
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Olfactory-mediated fear-potentiated startle.
Paschall, G. Y., & Davis, M. E. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.1.4 · Cited by 47 · see citing works
Ontogeny of Nociception and Antinociception
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Effects of 6‐hydroxydopamine‐induced catecholamine depletion on shock‐precipitated wall climbing of infant rat pups
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Aggressive Behavior in Abused Children
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Dissociation of behavioral and neural correlates of early associative learning
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The ontogeny of conditioned odor potentiation of startle.
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Developing a Sense of Safety
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Child physical abuse: Risk for psychopathology and efficacy of interventions
Brown, E. (2003) · Current Psychiatry Reports · doi:10.1007/s11920-003-0024-2 · Cited by 33 · see citing works
Blockade of mitral/tufted cell habituation to odors by association with reward: a preliminary note
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Regulation of rat maternal behavior by broadband pup vocalizations
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Child Maltreatment Risk Assessments: An Evaluation Guide
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Chapter VIII c-Fos in learning: beyond the mapping of neuronal activity
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Calcium Signaling in Mitral Cell Dendrites of Olfactory Bulbs of Neonatal Rats and Mice During Olfactory Nerve Stimulation and β-Adrenoceptor ActivationPreprint
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Child Maltreatment Risk Assessments
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Chapter II Neuroanatomical and functional mapping using activation of transcription factors
Dragunow, M., & Bilkey, D. K. (2002) · Handbook of chemical neuroanatomy · doi:10.1016/s0924-8196(02)80013-6 · Cited by 2 · see citing works

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Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience
McLaughlin, K. A., Sheridan, M. A., & Lambert, H. K. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.012 · Cited by 1,389 · see citing works
Lasting epigenetic influence of early-life adversity on the BDNF gene
Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.11.028 · Cited by 1,273 · see citing works
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Dimensions of early experience and neural development: deprivation and threat
Sheridan, M. A., & McLaughlin, K. A. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2014.09.001 · Cited by 697 · see citing works
The Peptide That Binds: A Systematic Review of Oxytocin and its Prosocial Effects in Humans
MacDonald, K., & MacDonald, T. M. (2010) · Harvard Review of Psychiatry · doi:10.3109/10673220903523615 · Cited by 585 · see citing works
Cortical processing of odor objects.
Wilson, D. A., & Sullivan, R. M. (2011) · Neuron · doi:10.1016/j.neuron.2011.10.027 · Cited by 468 · see citing works
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Linking prenatal maternal adversity to developmental outcomes in infants: The role of epigenetic pathways
Monk, C. E., Spicer, J., & Champagne, F. A. (2012) · Development and Psychopathology · doi:10.1017/s0954579412000764 · Cited by 458 · see citing works
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Walker, C., Bath, K. G., Joëls, M., Kőrösi, A., Larauche, M. H., Lucassen, P. J., Morris, M. J., Raineki, C., Roth, T. L., Sullivan, R. M., et al. (2017) · Stress · doi:10.1080/10253890.2017.1343296 · Cited by 402 · see citing works
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Maternal presence serves as a switch between learning fear and attraction in infancy
Moriceau, S., & Sullivan, R. M. (2006) · Nature Neuroscience · doi:10.1038/nn1733 · Cited by 386 · see citing works
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A developmental neurobiological model of motivated behavior: Anatomy, connectivity and ontogeny of the triadic nodes
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Epigenetic influence of social experiences across the lifespan
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Fragmentation and Unpredictability of Early-Life Experience in Mental Disorders
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Naturalistic rodent models of chronic early‐life stress
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Influence of maternal care on the developing brain: Mechanisms, temporal dynamics and sensitive periods
Curley, J. P., & Champagne, F. A. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.11.001 · Cited by 257 · see citing works
Dual Circuitry for Odor-Shock Conditioning during Infancy: Corticosterone Switches between Fear and Attraction via Amygdala
Moriceau, S., Wilson, D. A., Levine, S. D., & Sullivan, R. M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0499-06.2006 · Cited by 240 · see citing works
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DNA methylation and childhood maltreatment: From animal models to human studies
Lutz, P.-E., & Turecki, G. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.07.069 · Cited by 236 · see citing works
Effects of early-life abuse differ across development: infant social behavior deficits are followed by adolescent depressive-like behaviors mediated by the amygdala
Raineki, C., Cortés, M. R., Belnoue, L., & Sullivan, R. M. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5843-11.2012 · Cited by 217 · see citing works
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Early-life stress disrupts attachment learning: the role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine
Moriceau, S., Shionoya, K., Jakubs, K., & Sullivan, R. M. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4106-09.2009 · Cited by 214 · see citing works
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Epigenetic marking of the BDNF gene by early-life adverse experiences
Roth, T. L., & Sweatt, J. D. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.05.005 · Cited by 196 · see citing works
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Social influences on neurobiology and behavior: Epigenetic effects during development
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Developing a neurobehavioral animal model of infant attachment to an abusive caregiver
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The Development and Neurobiology of Infant Attachment and Fear
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Infant bonding and attachment to the caregiver: insights from basic and clinical science
Sullivan, R., Perry, R., Sloan, A., Kleinhaus, K., & Burtchen, N. (2011) · Clinics in Perinatology · doi:10.1016/j.clp.2011.08.011 · Cited by 181 · see citing works
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Neurobiology of infant attachment
Moriceau, S., & Sullivan, R. M. (2005) · Developmental Psychobiology · doi:10.1002/dev.20093 · Cited by 180 · see citing works
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How Early Experience Shapes Human Development: The Case of Psychosocial Deprivation
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Committee on the Prevention of Mental Disorders and Substance Abuse Among Children, Youth, and Young Adults: Research Advances and Promising Interventions
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Chapter 33. Neuroscience of Psychotherapy
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Previous institutionalization is followed by broader amygdala-hippocampal-PFC network connectivity during aversive learning in human development
Silvers, J. A., Lumian, D. S., Gabard-Durnam, L., Gee, D. G., Goff, B., Fareri, D. S., Caldera, C., Flannery, J., Telzer, E. H., Humphreys, K. L., et al. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.0038-16.2016 · Cited by 140 · see citing works
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Early Life Trauma and Attachment: Immediate and Enduring Effects on Neurobehavioral and Stress Axis Development
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Neonatal Behavioral Changes in Rats With Gestational Exposure to Lipopolysaccharide: A Prenatal Infection Model for Developmental Neuropsychiatric Disorders
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The Importance of Early Experiences for Neuro-Affective Development
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Differential Methylation of Genes in the Medial Prefrontal Cortex of Developing and Adult Rats Following Exposure to Maltreatment or Nurturing Care During Infancy
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Rodent model of infant attachment learning and stress
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How Early Life Stress Impact Maternal Care: A Systematic Review of Rodent Studies
Orso, R., Creutzberg, K. C., Wearick‐Silva, L. E., Viola, T. W., Tractenberg, S. G., Benetti, F., & Grassi‐Oliveira, R. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00197 · Cited by 121 · see citing works
Transitions in sensitive period attachment learning in infancy: The role of corticosterone
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The international society for developmental psychobiology Sackler symposium: early adversity and the maturation of emotion circuits-a cross-species analysis
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New insights into early-life stress and behavioral outcomes
Bolton, J. L., Molet, J., Ivy, A. S., & Baram, T. Z. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.12.012 · Cited by 110 · see citing works
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Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity
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Functional emergence of the hippocampus in context fear learning in infant rats
Raineki, C., Holman, P. J., Dębiec, J., Bugg, M., Beasley, A., & Sullivan, R. M. (2009) · Hippocampus · doi:10.1002/hipo.20702 · Cited by 103 · see citing works
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Emergence of social behavior deficit, blunted corticolimbic activity and adult depression-like behavior in a rodent model of maternal maltreatment
Rincón‐Cortés, M., & Sullivan, R. M. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.205 · Cited by 101 · see citing works
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Emerging roles of epigenetic mechanisms in the enduring effects of early-life stress and experience on learning and memory
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Aberrant development of intrinsic brain activity in a rat model of caregiver maltreatment of offspring
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Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior
Opendak, M., Gould, E., & Sullivan, R. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2017.02.002 · Cited by 94 · see citing works
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Epigenetic mechanisms in the development of behavior: Advances, challenges, and future promises of a new field
Roth, T. L. (2013) · Development and Psychopathology · doi:10.1017/s0954579413000618 · Cited by 95 · see citing works
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Oxytocin receptor gene polymorphism, perceived social support, and psychological symptoms in maltreated adolescents
Hostinar, C. E., Cicchetti, D., & Rogosch, F. A. (2014) · Development and Psychopathology · doi:10.1017/s0954579414000066 · Cited by 92 · see citing works
Ontogeny of memory: an update on 40 years of work on infantile amnesia
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Network structure reveals clusters of associations between childhood adversities and development outcomes
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Maternal Obesity as a Risk Factor for Brain Development and Mental Health in the Offspring
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Bdnf DNA methylation modifications in the hippocampus and amygdala of male and female rats exposed to different caregiving environments outside the homecage
Roth, T. L., Matt, S. M., Chen, K., & Blaze, J. (2014) · Developmental Psychobiology · doi:10.1002/dev.21218 · Cited by 89 · see citing works
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Early life trauma increases threat response of peri-weaning rats, reduction of axo-somatic synapses formed by parvalbumin cells and perineuronal net in the basolateral nucleus of amygdala
Santiago, A. N., Lim, K. Y., Opendak, M., Sullivan, R. M., & Aoki, C. (2018) · Journal of Comparative Neurology · doi:10.1002/cne.24522 · Cited by 87 · see citing works
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Maternal attenuation of hypothalamic paraventricular nucleus norepinephrine switches avoidance learning to preference learning in preweanling rat pups
Shionoya, K., Moriceau, S., Bradstock, P., & Sullivan, R. M. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.06.004 · Cited by 85 · see citing works
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Exposure to caregiver maltreatment alters expression levels of epigenetic regulators in the medial prefrontal cortex
Blaze, J., & Roth, T. L. (2013) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2013.10.001 · Cited by 80 · see citing works
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Using a Developmental Ecology Framework to Align Fear Neurobiology Across Species
Callaghan, B. L., Meyer, H. C., Opendak, M. M., Tieghem, M. V., Harmon, C., Li, A., Lee, F. S., Sullivan, R. M., & Tottenham, N. (2019) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050718-095727 · Cited by 81 · see citing works
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Repeated restraint stress increases basolateral amygdala neuronal activity in an age-dependent manner
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During infant maltreatment, stress targets hippocampus, but stress with mother present targets amygdala and social behavior
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Neurobiology of attachment to an abusive caregiver: Short‐term benefits and long‐term costs
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Enduring effects of infant memories: infant odor-shock conditioning attenuates amygdala activity and adult fear conditioning
Sevelinges, Y., Moriceau, S., Holman, P., Miner, C., Muzny, K., Gervais, R., Mouly, A.-M., & Sullivan, R. M. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.04.025 · Cited by 74 · see citing works
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Defining age limits of the sensitive period for attachment learning in rat pups
Upton, K. J., & Sullivan, R. M. (2010) · Developmental Psychobiology · doi:10.1002/dev.20448 · Cited by 71 · see citing works
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Ontogeny of odor-LiCl vs. odor-shock learning: Similar behaviors but divergent ages of functional amygdala emergencePreprint
Raineki, C., Shionoya, K., Sander, K., & Sullivan, R. M. (2009) · Learning & Memory · doi:10.1101/lm.977909 · Cited by 71 · see citing works
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Understanding pup affective state through ethologically significant ultrasonic vocalization frequency
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Developmental regulation of fear learning and anxiety behavior by endocannabinoids
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Neurobehavioral assessment of maternal odor in developing rat pups: implications for social buffering
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Resilience priming: Translational models for understanding resiliency and adaptation to early life adversity
Kentner, A. C., Cryan, J. F., & Brummelte, S. (2019) · Developmental Psychobiology · doi:10.1002/dev.21775 · Cited by 64 · see citing works
Neurodevelopmental mechanisms linking ACEs with psychopathology
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Cannabinoids reverse the effects of early stress on neurocognitive performance in adulthoodPreprint
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Authors: Roth, T. L., & Sullivan, R. M.
Affiliations: University of Oklahoma (US)
Corresponding author: Roth, Tania L.
ORCID: Roth, Tania L.
Sullivan, Regina M.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2005-04
Volume: 57
Issue: 8
Pages: 823-831
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2005.01.032
OpenAlex: W1991479884
Cited by: 204
References: 129
Citations by year: 2026: 10 · 2025: 3 · 2024: 8 · 2023: 8 · 2022: 3 · 2021: 9 · 2020: 8 · 2019: 16 · 2018: 10 · 2017: 13 · 2016: 17 · 2015: 8 · 2014: 12 · 2013: 15 · 2012: 8
FWCI: 8.49
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Drug Abuse (F31 DA06082, F31DA006082)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD33402, R01HD033402)
Topics: Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords: maternal abuse, odor preference, classical conditioning, olfactory learning, Fos expression, olfactory bulb, anterior piriform cortex, amygdala, infant brain development, rat model
MeSH terms: Animals, Animals, Newborn, Child Abuse, Conditioning, Classical, Disease Models, Animal, Electroshock, Female, Humans, Immunohistochemistry, Infant, Infant, Newborn, Male, Maternal Behavior, Memory, Nerve Net, Odorants, Oncogene Proteins v-fos, Maze Learning, Rats, Long-Evans, Rats

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

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