Maternal behavior and developmental psychopathology

Leckman, James F.; Herman, Amy E.

doi:10.1016/s0006-3223(01)01277-x

Cited by 139Neuroendocrine regulation and behaviorNeurotransmitter Receptor Influence on BehaviorGenetics and Neurodevelopmental Disorders

Maternal behavior and developmental psychopathology

Leckman, James F., Herman, Amy E.·2002·Biological Psychiatry

DOI 10.1016/s0006-3223(01)01277-x

Open this paper in CoChat — free account

Abstract

This paper reviews recent developments in the phenomenology, neurobiology, and genetics of maternal behavior in animal model systems from an evolutionary perspective on psychopathology. Following a review of the phenomenology and neurobiology of maternal behavior, recent studies addressing the role of genetic factors in the maternal behavior of rodents were identified in a search of literature in peer-reviewed journals. Gene knockout studies were evaluated with regard to mouse strain background, method of behavioral phenotyping, and quantification of the behavioral deficits. Gene knockout data were then analyzed using a cluster analysis technique. At least nine genes have been identified that are necessary for the expression of one or more aspects of maternal behavior. These genes encode for three transcription factors: three enzymes, including dopamine beta hydroxylase and neuronal nitric oxide synthase; two receptors, including the prolactin and the estrogen alpha receptor; and one neuropeptide, oxytocin. Cluster analysis suggested possible relationships between specific genes. Gene knockout technology has provided new insights into the molecular basis of maternal behavior that are congruent with the existing neurobiological literature. Future studies of genetic and environmental influences on maternal behavior have the potential to inform models of disease pathogenesis.

Integrity signals

Registry

Crossref · 10.1016/s0006-3223(01)01277-x

Cites

102 of 102 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Maternal licking and grooming of rat pups during the postpartum period has been associated with greater OT receptor binding or increased activity in brain areas critical for the development of parenting in mammals, including the medial preoptic area, lateral septum, the paraventricular nucleus of the hypothalamus, and the nucleus accumbens.
“For instance, maternal licking and grooming of rat pups during the postpartum period has been associated with greater OT receptor binding or increased activity in brain areas critical for the development of parenting in mammals, including the medial preoptic area, lateral septum, the paraventricular nucleus of the hypothalamus, and the nucleus accumbens (13–16).”
From Oxytocin and the development of parenting in humans (2010) · cites this paper as [15]

Cluster analysis and display of genome-wide expression patterns
Eisen, M. B., Spellman, P. T., Brown, P. O., & Botstein, D. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.25.14863 · Cited by 12,617 · see citing works
The Physiology of Reproduction
Legendre, M., & Jalabert, B. (1988) · Annals of Internal Medicine · doi:10.7326/0003-4819-109-2-176_1 · Cited by 7,879 · see citing works
Maternal Care, Hippocampal Glucocorticoid Receptors, and Hypothalamic-Pituitary-Adrenal Responses to Stress
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170 · see citing works
Drug abuse: hedonic homeostatic dysregulation
Koob, G. F., & Moal, M. L. (1997) · Science · doi:10.1126/science.278.5335.52 · Cited by 2,535 · see citing works
Prolactin: structure, function, and regulation of secretion
Freeman, M. E., Kanyicska, B., Lerant, A., & Nagy, G. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.4.1523 · Cited by 2,457 · see citing works
Nongenomic Transmission Across Generations of Maternal Behavior and Stress Responses in the Rat
Francis, D., Diorio, J., Liu, D., & Meaney, M. J. (1999) · Science · doi:10.1126/science.286.5442.1155 · Cited by 1,965 · see citing works
Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene.
Lubahn, D. B., Moyer, J. S., GOLDING, T. S., Couse, J. F., Korach, K. S., & Smithies, O. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.23.11162 · Cited by 1,901 · see citing works
Molecular Mechanisms of Human Hypertension
Lifton, R. P., Gharavi, A. G., & Geller, D. S. (2001) · Cell · doi:10.1016/s0092-8674(01)00241-0 · Cited by 1,686 · see citing works
Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638 · see citing works
Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat
Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., & Meaney, M. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5335 · Cited by 1,437 · see citing works
Maternal care, hippocampal synaptogenesis and cognitive development in rats
Liu, D., Diorio, J., Day, J. C., Francis, D. D., & Meaney, M. J. (2000) · Nature Neuroscience · doi:10.1038/77702 · Cited by 1,195 · see citing works
The neurobiology of attachment
Insel, T. R., & Young, L. J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35053579 · Cited by 1,173 · see citing works
Social amnesia in mice lacking the oxytocin gene
Ferguson, J. N., Young, L. J., Hearn, E. F., Matzuk, M. M., Insel, T. R., & Winslow, J. T. (2000) · Nature Genetics · doi:10.1038/77040 · Cited by 1,130 · see citing works
Collected Papers: Through Paediatrics to Psycho-Analysis
(1959) · Archives of Disease in Childhood · doi:10.1136/adc.34.176.359 · Cited by 1,107 · see citing works
A family study of obsessive–compulsive disorder
(1995) · American Journal of Psychiatry · doi:10.1176/ajp.152.1.76 · Cited by 1,022 · see citing works
The Anatomical Connections of the Macaque Monkey Orbitofrontal Cortex. A Review
Cavada, C. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.220 · Cited by 917 · see citing works
Maternal behavior in mammals.
Rheingold, H. L. (1963) · Medical Entomology and Zoology · Cited by 886 · see citing works
Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype?
Gerlai, R. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)20020-7 · Cited by 881 · see citing works
Cerebral hemisphere regulation of motivated behavior
Swanson, L. W. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02905-x · Cited by 846 · see citing works
Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin
Pedersen, C. A., & Prange, A. J. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.12.6661 · Cited by 841 · see citing works
Functional neuroimaging and the neuroanatomy of obsessive-compulsive disorder
Saxena, S., & Rauch, S. L. (2000) · Psychiatric Clinics of North America · doi:10.1016/s0193-953x(05)70181-7 · Cited by 840 · see citing works
Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse.Preprint
Ormandy, C. J., Camus, A., Barra, J., Damotte, D., Lucas, B., Buteau, H., Edery, M., Brousse, N., Babinet, C., Binart, N., et al. (1997) · Genes & Development · doi:10.1101/gad.11.2.167 · Cited by 806 · see citing works
Symptoms of obsessive-compulsive disorder
(1997) · American Journal of Psychiatry · doi:10.1176/ajp.154.7.911 · Cited by 766 · see citing works
Oxytocin is required for nursing but is not essential for parturition or reproductive behavior.
Nishimori, K., Young, L. J., Guo, Q., Wang, Z., Insel, T. R., & Matzuk, M. M. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.21.11699 · Cited by 734 · see citing works
Plasma oxytocin levels in autistic children
Modahl, C., Green, L. A., Fein, D., Morris, M., Waterhouse, L., Feinstein, C., & Levin, H. (1998) · Biological Psychiatry · doi:10.1016/s0006-3223(97)00439-3 · Cited by 728 · see citing works
Nonhormonal basis of maternal behavior in the rat
Rosenblatt, J. S. (1967) · Science · doi:10.1126/science.156.3781.1512 · Cited by 721 · see citing works
Long-term behavioral and neuroendocrine adaptations to adverse early experience
Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., Meaney, M. J., & Plotsky, P. M. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62132-9 · Cited by 717 · see citing works
A Family Study of Obsessive-compulsive Disorder
Nestadt, G., Samuels, J., Riddle, M., Bienvenu, O. J., Liang, K.-Y., LaBuda, M., Walkup, J., Grados, M., & Hoehn-Saric, R. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.4.358 · Cited by 657 · see citing works
Defective mammopoiesis, but normal hematopoiesis, in mice with a targeted disruption of the prolactin gene
Horseman, N. D., Zhao, W., Montecino‐Rodriguez, E., Tanaka, M., Nakashima, K., Engle, S. J., Smith, F., Markoff, E., & Dorshkind, K. (1997) · The EMBO Journal · doi:10.1093/emboj/16.23.6926 · Cited by 649 · see citing works
The Effects of Early Rearing Environment on the Development of GABAA and Central Benzodiazepine Receptor Levels and Novelty-Induced Fearfulness in the Rat
Caldji, C. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00110-4 · Cited by 606 · see citing works
Behavioural abnormalities in male mice lacking neuronal nitric oxide synthase
Nelson, R. J., Demas, G. E., Huang, P. L., Fishman, M. C., Dawson, V. L., Dawson, T. M., & Snyder, S. H. (1995) · Nature · doi:10.1038/378383a0 · Cited by 595 · see citing works
Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest
Lefebvre, L., Viville, S., Barton, S. C., Ishino, F., Keverne, E. B., & Surani, M. A. (1998) · Nature Genetics · doi:10.1038/2464 · Cited by 561 · see citing works
A neurobiological basis of social attachment.
(1997) · American Journal of Psychiatry · doi:10.1176/ajp.154.6.726 · Cited by 553 · see citing works
Noradrenaline is essential for mouse fetal development
THOMAS, S. A., Matsumoto, A. M., & Palmiter, R. D. (1995) · Nature · doi:10.1038/374643a0 · Cited by 534 · see citing works
Regulation of Maternal Behavior and Offspring Growth by Paternally Expressed Peg3
Li, L.-L., Keverne, E. B., Aparicio, S. A. J. R., Ishino, F., Barton, S. C., & Surani, M. A. (1999) · Science · doi:10.1126/science.284.5412.330 · Cited by 512 · see citing works
Effects of early adverse experiences on brain structure and function: clinical implications
Kaufman, J., Plotsky, P. M., Nemeroff, C. B., & Charney, D. S. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00998-7 · Cited by 508 · see citing works
Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat
Francis, D. D., Champagne, F. C., & Meaney, M. J. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00599.x · Cited by 496 · see citing works
Roles of Estrogen Receptor-α Gene Expression in Reproduction-Related Behaviors in Female Mice**This work was supported by the Harry Frank Guggenheim Foundation (to S.O.), the University of Missouri-Columbia molecular biology program (to D.B.L.), and NIH Grant HD-05751 (to D.W.P.).
Ogawa, S., Eng, V., Taylor, J. A., Lubahn, D. B., Korach, K. S., & Pfaff, D. W. (1998) · Endocrinology · doi:10.1210/endo.139.12.6357 · Cited by 487 · see citing works
Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas.
Pedersen, C. A., Caldwell, J. D., Walker, C., Ayers, G., & Mason, G. A. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.6.1163 · Cited by 475 · see citing works
Endogenous Peptides and Learning and Memory Processes
(1981) · Elsevier eBooks · doi:10.1016/b978-0-12-474980-1.x5001-6 · Cited by 456 · see citing works
Medial preoptic area and onset of maternal behavior in the rat.
Numan, M., Rosenblatt, J. S., & Komisaruk, B. R. (1977) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077304 · Cited by 422 · see citing works
Oxytocin and autistic disorder: alterations in peptide forms
Green, L., Fein, D., Modahl, C., Feinstein, C., Waterhouse, L., & Morris, M. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01139-8 · Cited by 404 · see citing works
Neural circuits mediating stress
López, J. F., Akil, H., & Watson, S. J. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00266-8 · Cited by 373 · see citing works
Nonhuman primate model of alcohol abuse: effects of early experience, personality, and stress on alcohol consumption.
Higley, J. D., Hasert, M. F., Suomi, S. J., & Linnoila, M. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.16.7261 · Cited by 368 · see citing works
Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats.
Bridges, R. S., Numan, M. J., Ronsheim, P. M., MANN, P., & Lupini, C. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.20.8003 · Cited by 349 · see citing works
A Defect in Nurturing in Mice Lacking the Immediate Early Gene fosB
Brown, J. R., Ye, H., Bronson, R. T., Dikkes, P., & Greenberg, M. E. (1996) · Cell · doi:10.1016/s0092-8674(00)80101-4 · Cited by 339 · see citing works
Inhibition of post-partum maternal behaviour in the rat by injecting an oxytocin antagonist into the cerebral ventricles
van Leengoed, E., Kerker, E., & Swanson, H. H. (1987) · Journal of Endocrinology · doi:10.1677/joe.0.1120275 · Cited by 300 · see citing works
Null Mutation of the Prolactin Receptor Gene Produces a Defect in Maternal Behavior
Lucas, B. K., Ormandy, C. J., Binart, N., Bridges, R. S., & Kelly, P. A. (1998) · Endocrinology · doi:10.1210/endo.139.10.6243 · Cited by 296 · see citing works
Peg1/Mest imprinted gene on chromosome 6 identified by cDNA subtraction hybridization
Kaneko‐Ishino, T., Kuroiwa, Y., Miyoshi, N., Kohda, T., Suzuki, R., Yokoyama, M., Viville, S., Barton, S. C., Ishino, F., & Surani, M. A. (1995) · Nature Genetics · doi:10.1038/ng0995-52 · Cited by 283 · see citing works
Amygdaloid inhibition of maternal behavior in the nulliparous female rat☆
FLEMING, A., Vaccarino, F. J., & Luebke, C. (1980) · Physiology & Behavior · doi:10.1016/0031-9384(80)90377-7 · Cited by 271 · see citing works
Comparison of the effects of early handling and early deprivation on maternal care in the rat
Pryce, C. R., Rüedi‐Bettschen, D., & Feldon, J. (2001) · Developmental Psychobiology · doi:10.1002/dev.1018 · Cited by 270 · see citing works
Estrogen receptors in the human forebrain and the relation to neuropsychiatric disorders
Österlund, M. K., & Hurd, Y. L. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00059-9 · Cited by 263 · see citing works
Peg3 imprinted gene on proximal chromosome 7 encodes for a zinc finger protein
Kuroiwa, Y., Kaneko‐Ishino, T., Kagitani, F., Kohda, T., Li, L. L., Tada, M., Suzuki, R., Yokoyama, M., Shiroishi, T., Wakana, S., et al. (1996) · Nature Genetics · doi:10.1038/ng0296-186 · Cited by 257 · see citing works
Lesions of the hypothalamic paraventricular nucleus disrupt the initiation of maternal behavior
Insel, T. R., & Harbaugh, C. R. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90234-5 · Cited by 250 · see citing works
Society, Stress and Disease
LENNART, L. (1977) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-197709000-00016 · Cited by 243 · see citing works
Obsessive-Compulsive Disorder in Pregnancy, the Puerperium, and the Premenstruum
Williams, K. E., & Koran, L. M. (1997) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.v58n0709 · Cited by 229 · see citing works
Oxytocin, vasopressin, and autism: Is there a connection?
Insel, T. R., O’Brien, D. J., & Leckman, J. F. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(98)00142-5 · Cited by 226 · see citing works
Self-citation
A longitudinal study of the effect of different social rearing conditions on cerebrospinal fluid norepinephrine and biogenic amine metabolites in rhesus monkeys
Kraemer, G. W. (1989) · Neuropsychopharmacology · doi:10.1016/0893-133x(89)90021-3 · Cited by 212 · see citing works
Mesotelencephalic dopamine system and reproductive behavior in the female rat: Effects of ventral tegmental 6-hydroxydopamine lesions on maternal and sexual responsiveness.
Hansen, S., Harthon, C., Waslin, E., Löfberg, L., & al, E. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.4.588 · Cited by 211 · see citing works
Oxytocin, Vasopressin, and Autism: Is There a Connection?
Insel, T. R., O’Brien, D. J., & Leckman, J. F. (2002) · The MIT Press eBooks · doi:10.7551/mitpress/3077.003.0049 · Cited by 211 · see citing works
Self-citation
Elevated Cerebrospinal Fluid Levels of Oxytocin in Obsessive-compulsive Disorder: Comparison With Tourette's Syndrome and Healthy Controls
Leckman, J. F. (1994) · Archives of General Psychiatry · doi:10.1001/archpsyc.1994.03950100030003 · Cited by 209 · see citing works
Self-citation
Early parental preoccupations and behaviors and their possible relationship to the symptoms of obsessive–compulsive disorder
Leckman, J. F., Mayes, L. C., Feldman, R., Evans, D. W., King, R. A., & Cohen, D. J. (1999) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.1999.tb10951.x · Cited by 207 · see citing works
Atlas of the neurons that express mRNA for the long form of the prolactin receptor in the forebrain of the female rat
Bakowska, J. C., & Morrell, J. I. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970922)386:2 · Cited by 198 · see citing works
Progressive impairment of developing neuroendocrine cell lineages in the hypothalamus of mice lacking the Orthopedia genePreprint
Acampora, D., Postiglione, M. P., Avantaggiato, V., Bonito, M. D., Vaccarino, F. M., Michaud, J. L., & Simeone, A. (1999) · Genes & Development · doi:10.1101/gad.13.21.2787 · Cited by 198 · see citing works
Neuroanatomical Circuitry for Mammalian Maternal Behaviora
Numan, M., & Sheehan, T. P. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51915.x · Cited by 194 · see citing works
Mesotelencephalic dopamine system and reproductive behavior in the female rat: Effects of ventral tegmental 6-hydroxydopamine lesions on maternal and sexual responsiveness.
Hansen, S., Harthon, C., Wallin, E., et al. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.4.588 · Cited by 186 · see citing works
Using Knockout and Transgenic Mice to Study Neurophysiology and Behavior
Picciotto, M. R., & Wickman, K. (1998) · Physiological Reviews · doi:10.1152/physrev.1998.78.4.1131 · Cited by 185 · see citing works
Recent life events and obsessive–compulsive disorder (OCD): the role of pregnancy/delivery
Maina, G., Albert, U., Bogetto, F., Vaschetto, P., & Ravizza, L. (1999) · Psychiatry Research · doi:10.1016/s0165-1781(99)00090-6 · Cited by 178 · see citing works
Development of the hippocampal formation from2 to 42 years: MRI evidence of smaller area dentata in autism
Saitoh, O. (2001) · Brain · doi:10.1093/brain/124.7.1317 · Cited by 175 · see citing works
Oxytocin Control of Maternal Behavior Regulation by Sex Steroids and Offspring Stimuli<sup>a</sup>
PEDERSEN, C. A. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51916.x · Cited by 172 · see citing works
Impaired Maternal Behavior in Mice Lacking Norepinephrine and Epinephrine
THOMAS, S. A., & Palmiter, R. D. (1997) · Cell · doi:10.1016/s0092-8674(00)80446-8 · Cited by 167 · see citing works
Autism: recent molecular genetic advances
Lamb, J. A. (2000) · Human Molecular Genetics · doi:10.1093/hmg/9.6.861 · Cited by 163 · see citing works
Plasma β‐Endorphin, Adrenocorticotropin Hormone, and Cortisol in Autism
Tordjman, S., McBride, P., Hertzig, M. E., Snow, M. E., Anderson, G. M., Hall, L. M., Thompson, S., Ferrari, P., & Cohen, D. J. (1997) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.1997.tb01697.x · Cited by 152 · see citing works
Peg3/Pw1 is an imprinted gene involved in the TNF-NFκB signal transduction pathway
Relaix, F., Wei, X.-J., Wu, X., & Sassoon, D. A. (1998) · Nature Genetics · doi:10.1038/ng0398-287 · Cited by 152 · see citing works
Sex with knockout models: behavioral studies of estrogen receptor α1Published on the World Wide Web on 26 April 1999.1
Rissman, E. F., Wersinger, S. R., Fugger, H. N., & Foster, T. C. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01452-3 · Cited by 150 · see citing works
Projection Sites of Medial Preoptic Area and Ventral Bed Nucleus of the Stria Terminalis Neurons that Express Fos during Maternal Behavior in Female Rats
Numan, M., & Numan, M. J. (1997) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1997.t01-1-00597.x · Cited by 149 · cited 1× · see citing works
“Classic lesion studies done in rodent model systems (rats, mice, and voles) have implicated the medial preoptic area (MPOA) of the hypothalamus, the ventral part of the bed nucleus of the stria terminalis (BNSTv), and the lateral septum (LS) as regions pivotal for regulation of pupdirected maternal behavior (Kaliniche…”
Background
Reversal of Sex Roles in Genetic Female Mice by Disruption of Estrogen Receptor Gene
Ogawa, S., Taylor, J. A., Lubahn, D. B., Korach, K. S., & Pfaff, D. W. (2008) · Neuroendocrinology · doi:10.1159/000127154 · Cited by 145 · see citing works
Using c-Fos immunocytochemistry to identify forebrain regions that may inhibit maternal behavior in rats.
Sheehan, T. P., Cirrito, J. R., Numan, M. J., & Numan, M. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.2.337 · Cited by 139 · see citing works
Commentary: The broken mouse: the role of development, plasticity and environment in the interpretation of phenotypic changes in knockout mice
Gingrich, J. A., & Hen, R. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00061-6 · Cited by 123 · see citing works
Maternal Aggression Is Reduced in Neuronal Nitric Oxide Synthase-Deficient Mice
Gammie, S. C., & Nelson, R. J. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-18-08027.1999 · Cited by 118 · see citing works
Maternal Behavior in the Laboratory Rat
Rosenblatt, J. S., & Siegel, H. I. (1980) · Springer eBooks · doi:10.1007/978-94-011-6287-6_7 · Cited by 118 · see citing works
The Human Homolog of a Mouse-Imprinted Gene, Peg3, Maps to a Zinc Finger Gene-Rich Region of Human Chromosome 19q13.4Preprint
Kim, J., Ashworth, L. K., Branscomb, E., & Stubbs, L. J. (1997) · Genome Research · doi:10.1101/gr.7.5.532 · Cited by 111 · see citing works
Central Nervous System Distribution of Vasopressin, Oxytocin, and Neurophysin
Sofroniew, M. V., & Weindl, A. (1981) · Elsevier eBooks · doi:10.1016/b978-0-12-474980-1.50022-2 · Cited by 110 · see citing works
Factors influencing maternal responsiveness in humans: Usefulness of an animal model
Fleming, A. J. (1988) · Psychoneuroendocrinology · doi:10.1016/0306-4530(88)90014-5 · Cited by 106 · see citing works
Gene targeting approaches to neuroendocrinology: oxytocin, maternal behavior, and affiliation
Young, L. J., Winslow, J. T., Wang, Z., Gingrich, B., Guo, Q., Matzuk, M. M., & Insel, T. R. (1997) · Hormones and Behavior · doi:10.1006/hbeh.1997.1377 · Cited by 105 · see citing works
Inhibition of Neuronal Nitric Oxide Synthase Increases Aggressive Behavior in Mice
Demas, G. E., Eliasson, M. J. L., Dawson, T. M., Dawson, V. L., Kriegsfeld, L. J., Nelson, R. J., & Snyder, S. H. (1997) · Molecular Medicine · doi:10.1007/bf03401818 · Cited by 101 · see citing works
The medial preoptic area, necessary for adult maternal behavior in rats, is only partially established as a component of the neural circuit that supports maternal behavior in juvenile rats.
Kalinichev, M., Rosenblatt, J. S., & Morrell, J. I. (2000) · Behavioral Neuroscience · doi:10.1037//0735-7044.114.1.196 · Cited by 85 · see citing works
Intergenerational Transmission of Parental Bonding Among Women
Miller, L., KRAMER, R. A., Warner, V., WICKRAMARATNE, P. J., & Weissman, M. M. (1997) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-199708000-00022 · Cited by 81 · see citing works
Preoccupations and Behaviors Associated with Romantic and Parental Love: Perspectives on the Origin of Obsessive-Compulsive Disorder
Leckman, J. F., & Mayes, L. C. (1999) · Child and Adolescent Psychiatric Clinics of North America · doi:10.1016/s1056-4993(18)30172-x · Cited by 79 · see citing works
Self-citation
Corticotronpin-releasing hormone inhibits maternal behavior and induces pup-killing
Pedersen, C. A., Caldwell, J. D., McGuire, M., & Evans, D. L. (1991) · Life Sciences · doi:10.1016/0024-3205(91)90278-j · Cited by 73 · see citing works
Induction of c‐Fos‐like and FosB‐like immunoreactivity reveals forebrain neuronal populations involved differentially in pup‐mediated maternal behavior in juvenile and adult rats
Kalinichev, M., Rosenblatt, J. S., Nakabeppu, Y., & Morrell, J. I. (2000) · The Journal of comparative neurology · doi:10.1002/(sici)1096-9861(20000103)416:1 · Cited by 72 · see citing works
Understanding Developmental Psychopathology: How Useful Are Evolutionary Accounts?
Leckman, J. F., & Mayes, L. C. (1998) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-199810000-00010 · Cited by 72 · see citing works
Self-citation
Fkh5 -deficient mice show dysgenesis in the caudal midbrain and hypothalamic mammillary body
Wehr, R., Mansouri, A., de Maeyer, T., & Gruß, P. (1997) · Development · doi:10.1242/dev.124.22.4447 · Cited by 70 · see citing works
The medial preoptic area, necessary for adult maternal behavior in rats, is only partially established as a component of the neural circuit that supports maternal behavior in juvenile rats.
Kalinichev, M., Rosenblatt, J. S., & Morrell, J. I. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.1.196 · Cited by 59 · see citing works
Society, Stress and Disease.
(1979) · Annals of Internal Medicine · doi:10.7326/0003-4819-90-3-479_1 · Cited by 56 · see citing works
Mice reared with Rat Aunts: Effects on Plasma Corticosterone and Open Field Activity
Denenberg, V. H., Rosenberg, K. M., Paschke, R. E., & ZARROW, M. X. (1969) · Nature · doi:10.1038/221073a0 · Cited by 36 · see citing works
Maternal Aggression in Endothelial Nitric Oxide Synthase-Deficient Mice
Gammie, S. C., Huang, P. L., & Nelson, R. J. (2000) · Hormones and Behavior · doi:10.1006/hbeh.2000.1595 · Cited by 35 · see citing works
Low versus Standard Dose mCPP Challenge in Obsessive-Compulsive Patients
Erzegovesi, S. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00178-0 · Cited by 32 · see citing works
Timing of neuroendocrine responses and effect of m-CPP and fenfluramine plasma levels in OCD
Hollander, E., Cohen, L. J., DeCaria, C. M., Saoud, J. B., Stein, D. J., Cooper, T. B., Islam, N. N., Liebowitz, M. R., & Klein, D. F. (1993) · Biological Psychiatry · doi:10.1016/0006-3223(93)90186-h · Cited by 28 · see citing works
Recent life-events and obsessive-compulsive disorder: The role of pregnancy/delivery
Bogetto, F., Albert, U., Vaschetto, P., Maina, G., & Ravizza, L. (1997) · Biological Psychiatry · doi:10.1016/s0006-3223(97)87464-1 · Cited by 8 · see citing works
From learning to love
Harlow, H. F. (1986) · Cited by 8 · see citing works
Untitled work
(1997) · doi:10.1002/(sici)1096-9861(19971201)388:4

Flagged first, then by citations

Sorted by citations

Understanding and sharing intentions: The origins of cultural cognition
Tomasello, M., Carpenter, M., Call, J., Behne, T., & Moll, H. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000129 · Cited by 4,882 · see citing works
The genetics of autism
Muhle, R., Trentacoste, S. V., & Rapin, I. (2004) · Pediatrics · doi:10.1542/peds.113.5.e472 · Cited by 1,207 · see citing works
A multidimensional model of obsessive-compulsive disorder
Mataix-Cols, D., do Rosario-Campos, M. C., & Leckman, J. F. (2005) · American Journal of Psychiatry · doi:10.1176/appi.ajp.162.2.228 · Cited by 1,074 · see citing works
Self-citation
a neurobehavioral model of affiliative bonding: implications for conceptualizing a human trait of affiliation
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
HOW THE BRAIN PROCESSES SOCIAL INFORMATION: Searching for the Social Brain
Insel, T. R., & Fernald, R. D. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144148 · Cited by 556 · see citing works
Brain basis of early parent–infant interactions: psychology, physiology, and <i>in vivo</i> functional neuroimaging studies
Swain, J. E., Lorberbaum, J. P., Kose, S., & Strathearn, L. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2007.01731.x · Cited by 499 · see citing works
Oxytocin and the development of parenting in humans
Gordon, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.02.005 · Cited by 469 · see citing works
Self-citation
Sex differences in oxytocin and vasopressin: Implications for autism spectrum disorders?
CARTER, C. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.025 · Cited by 432 · see citing works
Specifying the Neurobiological Basis of Human Attachment: Brain, Hormones, and Behavior in Synchronous and Intrusive Mothers
Atzil, S., Hendler, T., & Feldman, R. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.172 · Cited by 399 · see citing works
The signal functions of early infant crying
Soltis, J. (2004) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0400010x · Cited by 387 · see citing works
Breastfeeding, brain activation to own infant cry, and maternal sensitivity
Kim, P., Feldman, R., Mayes, L. C., Eicher, V., Thompson, N., Leckman, J. F., & Swain, J. E. (2011) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2011.02406.x · Cited by 386 · see citing works
Self-citation
Maternal postpartum behavior and the emergence of infant-mother and infant-father synchrony in preterm and full-term infants: The role of neonatal vagal tone
Feldman, R., & Eidelman, A. I. (2007) · Developmental Psychobiology · doi:10.1002/dev.20220 · Cited by 348 · see citing works
The social deficits of the oxytocin knockout mouse
Winslow, J. T., & Insel, T. R. (2002) · Neuropeptides · doi:10.1054/npep.2002.0909 · Cited by 307 · see citing works
Enteric Bacterial Metabolites Propionic and Butyric Acid Modulate Gene Expression, Including CREB-Dependent Catecholaminergic Neurotransmission, in PC12 Cells - Possible Relevance to Autism Spectrum Disorders
Nankova, B. B., Agarwal, R., MacFabe, D. F., & La Gamma, E. F. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103740 · Cited by 294 · see citing works
Neuronal nitric oxide synthase contributes to chronic stress-induced depression by suppressing hippocampal neurogenesis
Zhou, Q., Hu, Y., Hua, Y., Hu, M., Luo, C., Han, X., Zhu, X., Wang, B., Xu, J., & Zhu, D. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04914.x · Cited by 225 · see citing works
Maternal brain response to own baby‐cry is affected by cesarean section delivery
Swain, J. E., Tasgin, E., Mayes, L. C., Feldman, R., Todd Constable, R., & Leckman, J. F. (2008) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2008.01963.x · Cited by 206 · see citing works
Self-citation
Neural circuits underlying crying and cry responding in mammals
Newman, J. D. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.02.011 · Cited by 198 · see citing works
Genes Controlling Affiliative Behavior as Candidate Genes for Autism
Yrigollen, C. M., Han, S. S., Kochetkova, A., Babitz, T., Chang, J. T., Volkmar, F. R., Leckman, J. F., & Grigorenko, E. L. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.11.015 · Cited by 172 · see citing works
Self-citation
A neurocognitive model of borderline personality disorder: Effects of childhood sexual abuse and relationship to adult social attachment disturbance
Minzenberg, M. J., Poole, J. H., & Vinogradov, S. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000163 · Cited by 91 · see citing works
Cocaine addiction in mothers: Potential effects on maternal care and infant development
Strathearn, L., & Mayes, L. C. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.05142.x · Cited by 80 · see citing works
Maternal imprints and the origins of variation
Champagne, F. A. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.02.016 · Cited by 74 · see citing works
Parental attachment systems: neural circuits, genes, and experiential contributions to parental engagement
Mayes, L. C., Swain, J. E., & Leckman, J. F. (2005) · Clinical Neuroscience Research · doi:10.1016/j.cnr.2005.03.009 · Cited by 71 · see citing works
Self-citation
Report of altered urinary oxytocin and AVP excretion in neglected orphans should be reconsidered
Anderson, G. M. (2006) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-006-0153-7 · Cited by 22 · see citing works

Psychopathology among Mentally Retarded Children and Adolescents
Matson, J. L., & Frame, C. L. (1985) · Medical Entomology and Zoology · Cited by 19 · see citing works
Traditional Approaches to Child Psychopathology
Wall, K., Sumlin, E. D., & Sharp, A. C. (2021) · Wiley eBooks · doi:10.1002/9781118686089.ch1 · Cited by 1 · see citing works
Relating stability of individual dynamical networks to change in psychopathology
van der Tuin, S., Hoekstra, R. H. A., Booij, S. H., Oldehinkel, A. J., Wardenaar, K. J., van den Berg, D. P. G., Borsboom, D., & Wigman, J. T. W. (2023) · PLoS ONE · doi:10.1371/journal.pone.0293200 · Cited by 7 · see citing works
Relationship dissolution and psychopathology
Whisman, M. A., Salinger, J. M., & Sbarra, D. A. (2021) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2021.07.016 · Cited by 35 · see citing works
Dynamics of psychopathological symptomatology at patients with opiate addiction in the process of complex rehabilitation
Igumnov, S. A., & Станько, Э. П. (2016) · European Psychiatry · doi:10.1016/j.eurpsy.2016.01.1028

Authors: Leckman, J. F., & Herman, A. E.
Affiliations: Yale University (US)
Corresponding author: Leckman, James F.
ORCID: Leckman, James F.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2002-01
Volume: 51
Issue: 1
Pages: 27-43
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/s0006-3223(01)01277-x
OpenAlex: W2086366616
Cited by: 139
References: 102
Citations by year: 2026: 1 · 2025: 2 · 2024: 1 · 2023: 1 · 2022: 4 · 2021: 4 · 2020: 2 · 2019: 4 · 2018: 2 · 2017: 2 · 2016: 2 · 2015: 3 · 2014: 5 · 2013: 4 · 2012: 5
FWCI: 20.03
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 of Mental Health (MH49351, P01MH049351, MH30929)
National Center for Research Resources (RR06022)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD03008, P01HD003008)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Keywords: maternal behavior, developmental psychopathology, knockout mice, transcription factors, dopamine beta-hydroxylase, neuronal nitric oxide synthase, prolactin receptor, estrogen receptor alpha, oxytocin, rodent models
MeSH terms: Animals, Autistic Disorder, Behavior, Animal, Brain, Disease Models, Animal, Dopamine, Biological Evolution, Maternal Behavior, Muscle Proteins, Obsessive-Compulsive Disorder, Oxytocin, Phenotype, Prolactin, Cluster Analysis, Mice, Knockout, Nitric Oxide Synthase, Drosophila Proteins, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Maternal behavior and developmental psychopathology

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks