Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-05T11:40:16.838Z Has data issue: false hasContentIssue false
  • English
  • Français

Developing a neurobehavioral animal model of poverty: Drawing cross-species connections between environments of scarcity-adversity, parenting quality, and infant outcome

Published online by Cambridge University Press:  02 April 2018

Rosemarie E. Perry ,
Eric D. Finegood ,
Stephen H. Braren ,
Meriah L. Dejoseph ,
David F. Putrino ,
Donald A. Wilson ,
Regina M. Sullivan ,
C. Cybele Raver ,
Clancy Blair Open the ORCID record for Clancy Blair [Opens in a new window]  and
Family Life Project Key Investigators
Rosemarie E. Perry*
Affiliation:
New York University
Eric D. Finegood
Affiliation:
New York University
Stephen H. Braren
Affiliation:
New York University
Meriah L. Dejoseph
Affiliation:
New York University
David F. Putrino
Affiliation:
Burke Medical Research Institute Weill Cornell Medicine
Donald A. Wilson
Affiliation:
Emotional Brain Institute New York University School of Medicine
Regina M. Sullivan
Affiliation:
Emotional Brain Institute New York University School of Medicine
C. Cybele Raver
Affiliation:
New York University
Clancy Blair
Affiliation:
New York University
Family Life Project Key Investigators
Affiliation:
New York University Burke Medical Research Institute Weill Cornell Medicine Emotional Brain Institute New York University School of Medicine
*
Address correspondence and reprint requests to: Rosemarie E. Perry, Department of Applied Psychology, 627 Broadway, Room 810, New York, NY 10012; E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

Children reared in impoverished environments are at risk for enduring psychological and physical health problems. Mechanisms by which poverty affects development, however, remain unclear. To explore one potential mechanism of poverty's impact on social–emotional and cognitive development, an experimental examination of a rodent model of scarcity-adversity was conducted and compared to results from a longitudinal study of human infants and families followed from birth (N = 1,292) who faced high levels of poverty-related scarcity-adversity. Cross-species results supported the hypothesis that altered caregiving is one pathway by which poverty adversely impacts development. Rodent mothers assigned to the scarcity-adversity condition exhibited decreased sensitive parenting and increased negative parenting relative to mothers assigned to the control condition. Furthermore, scarcity-adversity reared pups exhibited decreased developmental competence as indicated by disrupted nipple attachment, distress vocalization when in physical contact with an anesthetized mother, and reduced preference for maternal odor with corresponding changes in brain activation. Human results indicated that scarcity-adversity was inversely correlated with sensitive parenting and positively correlated with negative parenting, and that parenting fully mediated the association of poverty-related risk with infant indicators of developmental competence. Findings are discussed from the perspective of the usefulness of bidirectional–translational research to inform interventions for at-risk families.

Keywords

braindevelopmentparentingpovertyregulation
Type
Regular Articles
Information
Development and Psychopathology , Volume 31 , Issue 2 , May 2019 , pp. 399 - 418
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

The rodent research presented here was supported by NIH Grants R01 MH091451 and R37 HD083217 (to R.M.S.) and T32 MH096331 (to R.E.P.). The Family Life Project Phase I Key Investigators include Lynne Vernon-Feagans, University of North Carolina; Martha Cox, University of North Carolina at Chapel Hill; Clancy Blair, New York University; Margaret Burchinal, University of North Carolina; Patricia Garrett-Peters, University of North Carolina; Mark Greenberg, Pennsylvania State University; Roger Mills-Koonce, University of North Carolina; and Michael Willoughby, RTI International. We thank the many families and research assistants for making this study possible. Human research was supported by the National Institute of Child Health and Human Development Grants P01 HD039667-01A1. The authors declare no competing financial interests.

References

Al Aïn, S., Perry, R. E., Nunez, B., Kayser, K., Hochman, C., Brehman, E., … Sullivan, R. M. (2016). Neurobehavioral assessment of maternal odor in developing rat pups: Implications for social buffering. Social Neuroscience. Advance online publication. doi:10.1080/17470919.2016.1159605Google Scholar
Andersen, S., Lyss, P., Dumont, N., & Teicher, M. (1999). Enduring neurochemical effects of early maternal separation on limbic structures. Annals of the New York Academy of Sciences, 877, 756–759.Google Scholar
Andersen, S. L., LeBlanc, C. J., & Lyss, P. J. (2001). Maturational increases in c-fos expression in the ascending dopamine systems. Synapse, 41, 345–350. doi:10.1002/syn.1091Google Scholar
Asok, A., Bernard, K., Roth, T. L., Rosen, J. B., & Dozier, M. (2013). Parental responsiveness moderates the association between early-life stress and reduced telomere length. Development and Psychopathology, 25, 577–585. doi:10.1017/S0954579413000011Google Scholar
Barnett, W. S. (1998). Long-term cognitive and academic effects of early childhood education on children in poverty. Prevention Medicine, 27, 204–207.Google Scholar
Bayley, N. (1969). Bayley Scales of Infant Development. New York: Psychological Corporation.Google Scholar
Bayley, N. (1993). Bayley II Scales of Infant Development. New York: Psychological Corporation.Google Scholar
Bernard, K., Dozier, M., Bick, J., Lewis-Morrarty, E., Lindheim, O., & Carlson, E. (2012). Enhancing attachment organization among maltreated children: Results of a randomized clinical trial. Child Development, 83, 623–636. doi:10.1111/j.1467-8624.2011.01712.xGoogle Scholar
Bernard, K., Meade, E. B., & Dozier, M. (2013). Parental synchrony and nurturance as targets in an attachment based intervention: Building upon Mary Ainsworth's insights about mother-infant interaction. Attachment and Human Development, 15, 507–523. doi:10.1080/14616734.2013.820920Google Scholar
Berry, D., Blair, C., Willoughby, M., Granger, D. A., Mills-Koonce, W. R., & Family Life Project Key Investigators. (2017). Maternal sensitivity and adrenocortical functioning across infancy and toddlerhood: Physiological adaptation to context? Development and Psychopathology, 29, 303–317. doi:10.1017/S0954579416000158Google Scholar
Bertolino, A., Saunders, R., Mattay, V., Bachevalier, J., Frank, J., & Weinberger, D. (1997). Altered development of prefrontal neurons in rhesus monkeys with neonatal mesial temporo-limbic lesions: A proton magnetic resonance spectroscopic imaging study. Cerebral Cortex, 7, 740–748.Google Scholar
Blair, C., Granger, D. A., Kivlighan, K. T., Mills-Koonce, R., Willoughby, M., Greenberg, M. T., … Family Life Project Key Investigators. (2008). Maternal and child contributions to cortisol response to emotional arousal in young children from low-income, rural communities. Developmental Psychology, 44, 1095–1109. doi:10.1037/0012-1649.44.4.1095Google Scholar
Blair, C., Granger, D. A., Willoughby, M., Mills-Koonce, R., Cox, M., Greenberg, M. T., … Family Life Project Key Investigators. (2011). Salivary cortisol mediates effects of poverty and parenting on executive functions in early childhood. Child Development, 82, 1970–1984. doi:10.1111/j.1467-8624.2011.01643.xGoogle Scholar
Blair, C., & Raver, C. C. (2012). Child development in the context of adversity: Experiential canalization of brain and behavior. American Psychologist, 67, 309–318. doi:10.1037/a0027493Google Scholar
Blair, C., & Raver, C. C. (2016). Poverty, stress, and brain development: New directions for prevention and intervention. Academic Pediatrics, 16(3, Suppl.), S30–S36. doi:10.1016/j.acap.2016.01.010Google Scholar
Blaze, J., Asok, A., & Roth, T. L. (2015). Long-term effects of early-life caregiving experiences on brain-derived neurotrophic factor histone acetylation in the adult rat mPFC. Stress, 18, 607–615. doi:10.3109/10253890.2015.1071790Google Scholar
Bokil, H., Andrews, P., Kulkarni, J. E., Mehta, S., & Mitra, P. P. (2010). Chronux: A platform for analyzing neural signals. Journal of Neuroscience Methods, 192, 146–151. doi:10.1016/j.jneumeth.2010.06.020Google Scholar
Boulanger Bertolus, J., Hegoburu, C., Ahers, J. L., Londen, E., Rousselot, J., Szyba, K., … Mouly, A. M. (2014). Infant rats can learn time intervals before the maturation of the striatum: Evidence from odor fear conditioning. Frontiers in Behavioral Neuroscience, 8, 176. doi:10.3389/fnbeh.2014.00176Google Scholar
Branchi, I., Santucci, D., & Alleva, E. (2001). Ultrasonic vocalisation emitted by infant rodents: A tool for assessment of neurobehavioural development. Behavioral Brain Research, 125, 49–56.Google Scholar
Brett, Z. H., Humphreys, K. L., Fleming, A. S., Kraemer, G. W., & Drury, S. S. (2015). Using cross-species comparisons and a neurobiological framework to understand early social deprivation effects on behavioral development. Development and Psychopathology, 27, 347–367. doi:10.1017/S0954579415000036Google Scholar
Brooks-Gunn, J., & Duncan, G. J. (1997). The effects of poverty on children. Future Child, 7, 55–71.Google Scholar
Cacioppo, J. T., Hawkley, L. C., Norman, G. J., & Berntson, G. G. (2011). Social isolation. Annals of the New York Academy of Sciences, 1231, 17–22. doi:10.1111/j.1749-6632.2011.06028.xGoogle Scholar
Callaghan, B. L., Sullivan, R. M., Howell, B., & Tottenham, N. (2014). The international society for developmental psychobiology Sackler symposium: Early adversity and the maturation of emotion circuits—A cross-species analysis. Developmental Psychobiology, 56, 1635–1650. doi:10.1002/dev.21260Google Scholar
Casquero-Veiga, M., Hadar, R., Pascau, J., Winter, C., Desco, M., & Soto-Montenegro, M. L. (2016). Response to deep brain stimulation in three brain targets with implications in mental disorders: A PET study in rats. PLOS ONE, 11, e0168689. doi:10.1371/journal.pone.0168689Google Scholar
Coopersmith, R., Henderson, S. R., & Leon, M. (1986). Odor specificity of the enhanced neural response following early odor experience in rats. Brain Research, 392, 191–197.Google Scholar
Cox, M., & Crnic, K. (2002). Qualitative ratings for parent–child interaction at 3–12 months of age. Unpublished manuscript, University of North Carolina, Chapel Hill, Department of Psychology.Google Scholar
Cunningham, M. G., Bhattacharyya, S., & Benes, F. M. (2002). Amygdalo-cortical sprouting continues into early adulthood: Implications for the development of normal and abnormal function during adolescence. Journal of Comparative Neurology, 453, 116–130. doi:10.1002/cne.10376Google Scholar
D'Aquila, P. S., Peana, A. T., Carboni, V., & Serra, G. (2000). Exploratory behavior and grooming after repeated restraint and chronic mild stress: Effect of desipramine. European Journal of Pharmacology, 399, 43–47.Google Scholar
Darmon, N., & Drewnowski, A. (2008). Does social class predict diet quality? American Journal of Clinical Nutrition, 87, 1107–1117.Google Scholar
Debiec, J., & Sullivan, R. M. (2014). Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear. Proceedings of the National Academy of Sciences, 111, 12222–12227. doi:10.1073/pnas.1316740111Google Scholar
Di Martino, A., Zuo, X. N., Kelly, C., Grzadzinski, R., Mennes, M., Schvarcz, A., … Milham, M. P. (2013). Shared and distinct intrinsic functional network centrality in autism and attention-deficit/hyperactivity disorder. Biological Psychiatry, 74, 623–632. doi:10.1016/j.biopsych.2013.02.011Google Scholar
Drury, S. S., Sanchez, M. M., & Gonzalez, A. (2016). When mothering goes awry: Challenges and opportunities for utilizing evidence across rodent, nonhuman primate and human studies to better define the biological consequences of negative early caregiving. Hormones and Behavior, 77, 182–192. doi:10.1016/j.yhbeh.2015.10.007Google Scholar
Duncan, G. J., Ziol-Guest, K. M., & Kalil, A. (2010). Early-childhood poverty and adult attainment, behavior, and health. Child Development, 81, 306–325. doi:10.1111/j.1467-8624.2009.01396.xGoogle Scholar
Dunn, A. J., Berridge, C. W., Lai, Y. I., & Yachabach, T. L. (1987). Crf-induced excessive grooming behavior in rats and mice. Peptides, 8, 841–844.Google Scholar
Ehret, G. (1976). Development of absolute auditory thresholds in the house mouse (Mus musculus). Journal of the American Academy of Audiology Society, 1, 179–184.Google Scholar
Enders, C. K. (2010). Applied missing data analysis. New York: Guilford Press.Google Scholar
Evans, G. W. (2004). The environment of childhood poverty. American Psychologist, 59, 77–92.Google Scholar
Evans, G. W., Li, D., & Whipple, S. S. (2013). Cumulative risk and child development. Psychological Bulletin, 139, 1342–1396. doi:10.1037/a0031808Google Scholar
Finegood, E. D., Blair, C., Granger, D. A., Hibel, L. C., Mills-Koonce, R., & Family Life Project Key Investigators (2016). Psychobiological influences on maternal sensitivity in the context of adversity. Developmental Psychology, 52, 1073–1087. doi:10.1037/dev0000123Google Scholar
Gee, D. G. (2016). Sensitive periods of emotion regulation: Influences of parental care on frontoamygdala circuitry and plasticity. New Directions for Child and Adolescent Development, 2016, 87–110.Google Scholar
Gee, D. G., Gabard-Durnam, L., Telzer, E. H., Humphreys, K. L., Goff, B., Shapiro, M., … Tottenham, N. (2014). Maternal buffering of human amygdala-prefrontal circuitry during childhood but not during adolescence. Psychological Science, 25, 2067–2078. doi:10.1177/0956797614550878Google Scholar
Granero, R., Louwaars, L., & Ezpeleta, L. (2015). Socioeconomic status and oppositional defiant disorder in preschoolers: Parenting practices and executive functioning as mediating variables. Frontiers in Psychology, 6, 1412. doi:10.3389/fpsyg.2015.01412Google Scholar
Hackman, D. A., & Farah, M. J. (2009). Socioeconomic status and the developing brain. Trends in Cognitive Sciences, 13, 65–73. doi:10.1016/j.tics.2008.11.003Google Scholar
Hackman, D. A., Farah, M. J., & Meaney, M. J. (2010). Socioeconomic status and the brain: Mechanistic insights from human and animal research. Nature Reviews Neuroscience, 11, 651–659. doi:10.1038/nrn2897Google Scholar
Hackman, D. A., Gallop, R., Evans, G. W., & Farah, M. J. (2015). Socioeconomic status and executive function: Developmental trajectories and mediation. Developmental Science, 18, 686–702. doi:10.1111/desc.12246Google Scholar
Hanson, J. L., Hair, N., Shen, D. G., Shi, F., Gilmore, J. H., Wolfe, B. L., & Pollak, S. D. (2013). Family poverty affects the rate of human infant brain growth. PLOS ONE, 8, e80954. doi:10.1371/journal.pone.0080954Google Scholar
Hill, D. L., & Almli, C. R. (1981). Olfactory bulbectomy in infant rats: Survival, growth and ingestive behaviors. Physiology and Behavior, 27, 811–817.Google Scholar
Hofer, M. A. (1994). Hidden regulators in attachment, separation, and loss. Monographs of the Society for Research in Child Development, 59, 192–207.Google Scholar
Hofer, M. A. (1996). Multiple regulators of ultrasonic vocalization in the infant rat. Psychoneuroendocrinology, 21, 203–217.Google Scholar
Hofer, M. A., & Shair, H. (1978). Ultrasonic vocalization during social interaction and isolation in 2-weeek-old rats. Developmental Psychobiology, 11, 495–504. doi:10.1002/dev.420110513Google Scholar
Hofer, M. A., Shair, H., & Singh, P. (1976). Evidence that maternal ventral skin substances promote suckling in infant rats. Physiology and Behavior, 17, 131–136.Google Scholar
Holochwost, S. J., Gariépy, J.-L., Propper, C. B., Gardner-Neblett, N., Volpe, V., Neblett, E., & Mills-Koonce, W. R. (2016). Sociodemographic risk, parenting, and executive functions in early childhood: The role of ethnicity. Early Childhood Research Quarterly, 36, 537–549. doi:10.1016/j.ecresq.2016.02.001Google Scholar
Hostinar, C. E., Sullivan, R. M., & Gunnar, M. R. (2014). Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: A review of animal models and human studies across development. Psychological Bulletin, 140, 256–282. doi:10.1037/a0032671Google Scholar
Howell, B. R., McMurray, M. S., Guzman, D. B., Nair, G., Shi, Y., McCormack, K. M., … Sanchez, M. M. (2017). Maternal buffering beyond glucocorticoids: Impact of early-life stress on corticolimbic circuits that control infant responses to novelty. Social Neuroscience, 12, 50–64. doi:10.1080/17470919.2016.1200481Google Scholar
Insel, T. R., Hill, J. L., & Mayor, R. B. (1986). Rat pup ultrasonic isolation calls: Possible mediation by the benzodiazepine receptor complex. Pharmacology Biochemistry and Behavior, 24, 1263–1267.Google Scholar
Jedd, K., Hunt, R. H., Cicchetti, D., Hunt, E., Cowell, R. A., Rogosch, F. A., … Thomas, K. M. (2015). Long-term consequences of childhood maltreatment: Altered amygdala functional connectivity. Development and Psychopathology, 27(4, Pt. 2), 1577–1589. doi:10.1017/S0954579415000954Google Scholar
Johnson, M. H. (2001). Functional brain development in humans. Nature Reviews Neuroscience, 2, 475–483. doi:10.1038/35081509Google Scholar
Johnson, S. B., Riis, J. L., & Noble, K. G. (2016). State of the art review: Poverty and the developing brain. Pediatrics, 137. doi:10.1542/peds.2015-3075Google Scholar
Kim, P., Evans, G. W., Angstadt, M., Shaun Ho, S., Sripada, C. S., Swain, J. E., … Luan Phan, K. (2013). Effects of childhood poverty and chronic stress on emotion regulatory brain function in adulthood. PNAS, 110, 18442–18447.Google Scholar
Landers, M. S., & Sullivan, R. M. (1999). Vibrissae-evoked behavior and conditioning before functional ontogeny of the somatosensory vibrissae cortex. Journal of Neuroscience, 19, 5131–5137.Google Scholar
Landers, M. S., & Sullivan, R. M. (2012). The development and neurobiology of infant attachment and fear. Developmental Neuroscience, 34, 101–114. doi:000336732Google Scholar
Landry, S. H., Smith, K. E., Swank, P. R., & Guttentag, C. (2008). A responsive parenting intervention: The optimal timing across early childhood for impacting maternal behaviors and child outcomes. Developmental Psychology, 44, 1335–1353. doi:10.1037/a0013030Google Scholar
Leon, M. (1975). Dietary control of maternal pheromone in the lactating rat. Physiology and Behavior, 14, 311–319.Google Scholar
Leon, M. (1980). Development of olfactory attraction by young Norway rats. In Muller-Schware, D. & Silverstein, R. M. (Eds.), Chemical signals. New York: Plenum Press.Google Scholar
Logan, D. W., Brunet, L. J., Webb, W. R., Cutforth, T., Ngai, J., & Stowers, L. (2012). Learned recognition of maternal signature odors mediates the first suckling episode in mice. Current Biology, 22, 1998–2007. doi:10.1016/j.cub.2012.08.041Google Scholar
Luby, J., Belden, A., Botteron, K., Marrus, N., Harms, M. P., Babb, C., … Barch, D. (2013). The effects of poverty on childhood brain development: The mediating effect of caregiving and stressful life events. JAMA Pediatrics, 167, 1135–1142. doi:10.1001/jamapediatrics.2013.3139Google Scholar
McLaughlin, K. A., & Sheridan, M. A. (2016). Beyond cumulative risk: A dimensional approach to childhood adversity. Current Directions in Psychological Science, 25, 239–245. doi:10.1177/0963721416655883Google Scholar
McLaughlin, K. A., Sheridan, M. A., & Lambert, H. K. (2014). Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience. Neuroscience and Biobehavioral Reviews, 47, 578–591. doi:10.1016/j.neubiorev.2014.10.012Google Scholar
McLoyd, V. C. (1998). Socioeconomic disadvantage and child development. American Psychologist, 53, 185–204.Google Scholar
Mills-Koonce, W. R., Gariepy, J. L., Propper, C., Sutton, K., Calkins, S., Moore, G., & Cox, M. (2007). Infant and parent factors associated with early maternal sensitivity: A caregiver-attachment systems approach. Infant Behavior and Development, 30, 114–126. doi:10.1016/j.infbeh.2006.11.010Google Scholar
Mills-Koonce, W. R., Garrett-Peters, P., Barnett, M., Granger, D. A., Blair, C., & Cox, M. J. (2011). Father contributions to cortisol responses in infancy and toddlerhood. Developmental Psychology, 47, 388–395. doi:10.1037/a0021066Google Scholar
Mills-Koonce, W. R., Propper, C. B., Gariepy, J. L., Blair, C., Garrett-Peters, P., & Cox, M. J. (2007). Bidirectional genetic and environmental influences on mother and child behavior: The family system as the unit of analyses. Development and Psychopathology, 19, 1073–1087. doi:10.1017/S0954579407000545Google Scholar
Mills-Koonce, W. R., Willoughby, M. T., Garrett-Peters, P., Wagner, N., Vernon-Feagans, L., & Family Life Project Key Investigators. (2016). The interplay among socioeconomic status, household chaos, and parenting in the prediction of child conduct problems and callous-unemotional behaviors. Development and Psychopathology, 28, 757–771. doi:10.1017/S0954579416000298Google Scholar
Mitra, P. P., & Bokil, H. (2008). Observed brain dynamics. New York: Oxford University Press.Google Scholar
Molet, J., Heins, K., Zhuo, X., Mei, Y. T., Regev, L., Baram, T. Z., & Stern, H. (2016). Fragmentation and high entropy of neonatal experience predict adolescent emotional outcome. Translational Psychiatry, 6, e702. doi:10.1038/tp.2015.200Google Scholar
Molet, J., Maras, P. M., Avishai-Eliner, S., & Baram, T. Z. (2014). Naturalistic rodent models of chronic early-life stress. Developmental Psychobiology, 56, 1675–1688. doi:10.1002/dev.21230Google Scholar
Moriceau, S., Roth, T. L., & Sullivan, R. M. (2010). Rodent model of infant attachment learning and stress. Developmental Psychobiology, 52, 651–660. doi:10.1002/dev.20482Google Scholar
Moriceau, S., Shionoya, K., Jakubs, K., & Sullivan, R. M. (2009). Early-life stress disrupts attachment learning: The role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine. Journal of Neuroscience, 29, 15745–15755. doi:10.1523/JNEUROSCI.4106-09.2009Google Scholar
Moriceau, S., & Sullivan, R. M. (2004). Unique neural circuitry for neonatal olfactory learning. Journal of Neuroscience, 24, 1182–1189. doi:10.1523/JNEUROSCI.4578-03.2004 24/5/1182Google Scholar
Moriceau, S., & Sullivan, R. M. (2006). Maternal presence serves as a switch between learning fear and attraction in infancy. Nature Neuroscience, 9, 1004–1006. doi:10.1038/nn1733Google Scholar
Morrison, G. L., Fontaine, C. J., Harley, C. W., & Yuan, Q. (2013). A role for the anterior piriform cortex in early odor preference learning: Evidence for multiple olfactory learning structures in the rat pup. Journal of Neurophysiology, 110, 141–152. doi:10.1152/jn.00072.2013Google Scholar
Muthén, L. K., & Muthén, B. O. (1998–2012). Mplus user's guide (7th ed.). Los Angeles: Author.Google Scholar
National Institute of Child Health and Human Development Early Child Care Research Network (1999). Child care and mother–child interaction in the first 3 years of life. Developmental Psychology, 35, 1399–1413.Google Scholar
Nelson, C. A., Zeanah, C. H., Fox, N. A., Marshall, P. J., Smyke, A. T., & Guthrie, D. (2007). Cognitive recovery in social deprived young children: The Bucharest early intervention project. Science, 318, 1937–1940. doi:10.1126/science.1143921Google Scholar
Noble, K. G., Houston, S. M., Kan, E., & Sowell, E. R. (2012). Neural correlates of socioeconomic status in the developing human brain. Developmental Science, 15, 516–527. doi:10.1111/j.1467-7687.2012.01147.xGoogle Scholar
Oswalt, G. L., & Wilson, D. A. (1979). Adult-male odor suppresses ultrasonic vocalization in infant rats. Paper presented at the Eastern Conference on Reproductive Behavior, New Orleans.Google Scholar
Paxinos, G., & Watson, C. (1986). The rat brain in stereotaxic coordinates (Compact 6th ed.). New York: Academic Press.Google Scholar
Perry, R. E., Al Aïn, S., Raineki, C., Sullivan, R. M., & Wilson, D. A. (2016). Development of odor hedonics: Experience-dependent ontogeny of circuits supporting maternal and predator odor responses in rats. Journal of Neuroscience, 36, 6634–6650. doi:10.1523/JNEUROSCI.0632-16.2016Google Scholar
Perry, R. E., Blair, C., & Sullivan, R. M. (2017). Neurobiology of infant attachment: Attachment despite adversity and parental programming of emotionality. Current Opinion in Psychology, 17, 1–6.Google Scholar
Perry, R. E., & Sullivan, R. M. (2014). Neurobiology of attachment to an abusive caregiver: Short-term benefits and long-term costs. Developmental Psychobiology, 56, 1626–1634. doi:10.1002/dev.21219Google Scholar
Poldrack, R. A., & Farah, M. J. (2015). Progress and challenges in probing the human brain. Nature, 526, 371–379. doi:10.1038/nature15692Google Scholar
Posner, J., Cha, J., Roy, A. K., Peterson, B. S., Bansal, R., Gustafsson, H. C., … Monk, C. (2016). Alterations in amygdala-prefrontal circuits in infants exposed to prenatal maternal depression. Translational Psychiatry, 6, e935. doi:10.1038/tp.2 016.146Google Scholar
Preacher, K. J., & Hayes, A. F. (2008). Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behavior Research Methods, 40, 879–891.Google Scholar
Preacher, K. J., & Kelley, K. (2011). Effect size measures for mediation models: Quantitative strategies for communicating indirect effects. Psychological Methods, 16, 93–115. doi:10.1037/a0022658Google Scholar
Raineki, C., Holman, P. J., Debiec, J., Bugg, M., Beasley, A., & Sullivan, R. M. (2010). Functional emergence of the hippocampus in context fear learning in infant rats. Hippocampus, 20, 1037–1046. doi:10.1002/hipo.20702Google Scholar
Raineki, C., Moriceau, S., & Sullivan, R. M. (2010). Developing a neurobehavioral animal model of infant attachment to an abusive caregiver. Biological Psychiatry, 67, 1137–1145. doi:10.1016/j.biopsych.2009.12.019Google Scholar
Raineki, C., Pickenhagen, A., Roth, T. L., Babstock, D. M., McLean, J. H., Harley, C. W., … Sullivan, R. M. (2010). The neurobiology of infant maternal odor learning. Brazilian Journal of Medical and Biological Research, 43, 914–919. doi:S0100-879X2010007500090Google Scholar
Raineki, C., Sarro, E., Rincón-Cortés, M., Perry, R., Boggs, J., Holman, C. J., … Sullivan, R. M. (2015). Paradoxical neurobehavioral rescue by memories of early-life abuse: The safety signal value of odors learned during abusive attachment. Neuropsychopharmacology, 40, 906–914. doi:10.1038/npp.2014.266Google Scholar
Raver, C. C., Roy, A. L., Pressler, E., Ursache, A. M., & McCoy, D. C. (2016). Poverty-related adversity and emotion regulation predict internalizing behavior problems among low-income children ages 8-11. Behavioral Sciences, 7, E2. doi:10.3390/bs7010002Google Scholar
Rilling, J. K., & Young, L. J. (2014). The biology of mammalian parenting and its effect on offspring social development. Science, 345, 771–776. doi:10.1126/science.1252723Google Scholar
Rincón-Cortés, M., Barr, G. A., Mouly, A. M., Shionoya, K., Nunez, B. S., & Sullivan, R. M. (2015). Enduring good memories of infant trauma: Rescue of adult neurobehavioral deficits via amygdala serotonin and corticosterone interaction. Proceedings of the National Academy of Sciences, 112, 881–886. doi:10.1073/pnas.1416065112Google Scholar
Rincón-Cortés, M., & Sullivan, R. M. (2014). Early-life trauma and attachment: Immediate and enduring effects on neurobehavioral and stress axis development. Frontiers in Endocrinology, 5, 33. doi:10.3389/fendo.2014.00033Google Scholar
Rincón-Cortés, M., & Sullivan, R. M. (2016). Emergence of social behavior deficit, blunted corticolimbic activity and adult depression-like behavior in a rodent model of maternal maltreatment. Translational Psychiatry, 6, e930. doi:10.1038/tp.2016.205Google Scholar
Sarro, E. C., Wilson, D. A., & Sullivan, R. M. (2014). Maternal regulation of infant brain state. Current Biology, 24, 1664–1669. doi:10.1016/j.cub.2014.06.017Google Scholar
Scheinost, D., Sinha, R., Cross, S. N., Kwon, S. H., Sze, G., Constable, R. T., & Ment, L. R. (2017). Does prenatal stress alter the developing connectome? Pediatric Research, 81, 214–226. doi:10.1038/pr.2016.197Google Scholar
Seminowicz, D. A., Mayberg, H. S., McIntosh, A. R., Goldapple, K., Kennedy, S., Segal, Z., & Rafi-Tari, S. (2004). Limbic-frontal circuitry in major depression: A path modeling metanalysis. Neuroimage, 22, 409–418. doi:10.1016/j.neuroimage.2004.01.015Google Scholar
Shair, H. N. (2007). Acquisition and expression of a socially mediated separation response. Behavioural Brain Research, 182, 180–192. doi:10.1016/j.bbr.2007.02.016Google Scholar
Sheffield, J. M., & Barch, D. M. (2016). Cognition and resting-state functional connectivity in schizophrenia. Neuroscience and Biobehavioral Reviews, 61, 108–120. doi:10.1016/j.neubiorev.2015.12.007Google Scholar
Sheridan, M. A., & McLaughlin, K. A. (2014). Dimensions of early experience and neural development: Deprivation and threat. Trends in Cognitive Sciences, 18, 580–585. doi:10.1016/j.tics.2014.09.001Google Scholar
Silvers, J. A., Lumian, D. S., Gabard-Durnam, L. G., Gee, D. G., Goff, B., Fareri, D. S., … Tottenham, N. (2016). Previous institutionalization is followed by broader amygdala-hippocampal-PFC network connectivity during aversive learning in human development. Journal of Neuroscience, 36, 6420–6430. doi:10.1523/JNEUROSCI.0038-16.2016Google Scholar
Singh, P. J., & Tobach, E. (1975). Olfactory bulbectomy and nursing behavior in rat pups (Wistar DAB). Developmental Psychobiology, 8, 151–164. doi:10.1002/dev.420080207Google Scholar
Sprujit, B. M., van Hooff, J. A., & Gispen, W. H. (1992). Ethology and neurobiology of grooming behavior. Physiological Reviews, 72, 825–852.Google Scholar
Sripanidkulchai, K., Sripanidkulchai, B., & Wyss, J. (2004). The cortical projection of the basolateral amygdaloid nucleus in the rat: A retrograde fluorescent dye study. Journal of Comparative Neurology, 229, 419–431.Google Scholar
Staff, R. T., Murray, A. D., Ahearn, T. S., Mustafa, N., Fox, H. C., & Whalley, L. J. (2012). Childhood socioeconomic status and adult brain size: Childhood socioeconomic status influences adult hippocampal size. Annals of Neurology, 71, 653–660. doi:10.1002/ana.22631Google Scholar
Stifter, C. A., & Corey, J. (2001). Vagal regulation and observed social behavior in infancy. Social Development, 10, 189–201. doi:10.1111/1467-9507.00158Google Scholar
Sturrock, R. (1978). Development of the indusium griseum: I. A quantitative light microscopic study of neurons and glia. Journal of Anatomy, 125(Pt 2), 293.Google Scholar
Sullivan, R. M., Landers, M., Yeaman, B., & Wilson, D. A. (2000). Good memories of bad events in infancy. Nature, 407, 38–39. doi:10.1038/35024156Google Scholar
Sullivan, R. M., & Perry, R. E. (2015). Mechanisms and functional implications of social buffering in infants: Lessons from animal models. Social Neuroscience, 10, 500–511. doi:10.1080/17470919.2015.1087425Google Scholar
Sullivan, R. M., & Wilson, D. A. (1991). Neural correlates of conditioned odor avoidance in infant rats. Behavioral Neuroscience, 105, 307–312.Google Scholar
Sullivan, R. M., & Wilson, D. A. (1995). Dissociation of behavioral and neural correlates of early associative learning. Developmental Psychobiology, 28, 213–219. doi:10.1002/dev.420280403Google Scholar
Sullivan, R. M., Wilson, D. A., Wong, R., Correa, A., & Leon, M. (1990). Modified behavioral and olfactory bulb responses to maternal odors in preweanling rats. Developmental Brain Research, 53, 243–247.Google Scholar
Szyf, M., Weaver, I., & Meaney, M. (2007). Maternal care, the epigenome and phenotypic differences in behavior. Reproductive Toxicology, 24, 9–19. doi:10.1016/j.reprotox.2007.05.001Google Scholar
Takahashi, L. K. (1992). Ontogeny of behavioral inhibition induced by unfamiliar adult male conspecifics in preweanling rats. Physiology Behavior, 52, 493–498.Google Scholar
Tang, A. C., Reeb-Sutherland, B. C., Romeo, R. D., & McEwen, B. S. (2014). On the causes of early-life experience effects: Evaluating the role of mom. Frontiers in Neuroendocrinology, 35, 245–251. doi:10.1016/j.yfrne.2013.11.002Google Scholar
Teicher, M. H., & Blass, E. M. (1977). First suckling response of the newborn albino rat: The roles of olfaction and amniotic fluid. Science, 198, 635–636.Google Scholar
Thapar, A., & Rutter, R. (2015). Using natural experiments and animal models to study causal hypotheses in relation to child mental health problems. In Thapar, A., Pine, D. S., Leckman, J. F., Scott, S., Snowling, M. J., & Taylor, E. (Eds.), Rutter's child and adolescent psychiatry (pp. 145–162). Chichester: Wiley.Google Scholar
Tottenham, N. (2015). Social scaffolding of human amygdala-mPFC circuit development. Social Neuroscience, 10, 489–499. doi:10.1080/17470919.2015.1087424Google Scholar
US Census Bureau. (2015). Age and sex of all people, family members and unrelated individuals iterated by income-to-poverty ratio and race. Retrieved from https://www.census.gov/data/tables/time-series/demo/income-poverty/cps-pov/pov01.htmlGoogle Scholar
Vernon-Feagans, L., & Cox, M. (2013). The Family Life Project: An epidemiological and developmental study of young children living in poor rural communities. Monographs of the Society for Research in Child Development, 78, 1–150.Google Scholar
Vidyasagar, D. (2006). Global notes: Counting the world's poor—How do we define poverty? Journal of Perinatology, 26, 325–327. doi:10.1038/sj.jp.7211531Google Scholar
Walker, C. D., Bath, K. G., Joels, M., Korosi, A., Larauche, M., Lucassen, P. J., … Baram, T. Z. (2017). Chronic early-life stress induced by limited bedding and nesting (LBN) material in rodents: Critical considerations of methodology, outcomes and translational potential. Stress. Advance online publication. doi:10.1080/10253890.2017.1343296Google Scholar
Weber, E. M., & Olsson, I. A. S. (2008). Maternal behaviour in Mus musculus sp.: An ethological review. Applied Animal Behaviour Science, 114, 1–22. doi:10.1016/j.applanim.2008.06.006Google Scholar
Wilson, D. A., Peterson, J., Basavaraj, B. S., & Saito, M. (2011). Local and regional network function in behaviorally relevant cortical circuits of adult mice following postnatal alcohol exposure. Alcoholism: Clinical and Experimental Research, 35, 1974–1984. doi:10.1111/j.1530-0277.2011.01549.xGoogle Scholar
Yan, C. G., Rincón-Cortés, M., Raineki, C., Sarro, E., Colcombe, S., Guilfoyle, D. N., … Castellanos, F. X. (2017). Aberrant development of intrinsic brain activity in a rat model of caregiver maltreatment of offspring. Translational Psychiatry, 7, e1005. doi:10.1038/tp.2016.276Google Scholar
Yoshikawa, H., Aber, J. L., & Beardslee, W. R. (2012). The effects of poverty on the mental, emotional, and behavioral health of children and youth: Implications for prevention. American Psychologist, 67, 272–284. doi:10.1037/a0028015Google Scholar
Zhang, Z. W. (2004). Maturation of layer V pyramidal neurons in the rat prefrontal cortex: Intrinsic properties and synaptic function. Journal of Neurophysiology, 91, 1171–1182. doi:10.1152/jn.00855.2003Google Scholar