Adult depression-like behavior, amygdala and olfactory cortex functions are restored by odor previously paired with shock during infant’s sensitive period attachment learning
Open accessAbstract
Maltreatment from the caregiver induces vulnerability to later life psychopathologies, yet attraction and comfort is sometimes provided by cues associated with early life maltreatment. We used a rat model of early life maltreatment with odor-0.5 mA shock conditioning to produce depressive-like behaviors and questioned whether stimuli associated with maltreatment would restore emotional neurobehavioral function to control levels. Pups received daily novel odor-0.5 mA shock conditioning from postnatal day 8 to 12. This procedure produces a new maternal odor that controls pups' attachment behaviors. In adulthood, either with or without the infant odor, animals received a Forced Swim Test, Sucrose Preference Test or assessment of amygdala and olfactory system functioning using field potential signal evoked by olfactory bulb paired-pulse electrical stimulation. Following neonatal odor-shock pairings, but not unpaired controls, adults without the odor present showed increased depression-like behavior in the Forced Swim Test and Sucrose Preference Test and a deficit in paired-pulse inhibition in amygdala and piriform (olfactory) cortex. All effects were brought to control levels when the infant conditioned odor was presented during behavioral and neural tests. The ability of cues associated with early life maltreatment to normalize behavior and amygdala activity suggests these cues provide adaptive value in adulthood.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Amygdala-dependent deficits are task-specific: amygdala hyperactivity underlies decreased social exploration in adolescence and depressive/anxiety-like behavior in adulthood, in parallel with impaired threat aversion learning and blunted amygdala activation during fear conditioning.
“Amygdala-dependent deficits are expressed in a task-specific manner: amygdala hyperactivity underlies decreased social exploration in adolescence and depressive and anxiety-like behavior in adulthood (Fig. 2), in parallel with impaired ability to learn aversions to threat and blunted amygdala activation during fear conditioning (Raineki et al., 2012, Sevelinges et al., 2007, Sevelinges et al., 201”
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 Sevelinges et al., 2011
Only early life trauma associated with attachment leads to lifelong amygdala-dependent behavioral deficits, such as poor social behavior (onset prior to weaning) and depressive-like behaviors (onset post-weaning).
“Testing later in life shows that only the early life trauma associated with attachment will lead to lifelong amygdala-dependent behavioral deficits, such as poor social behavior (onset prior to weaning) and depressive-like behaviors (onset post- weaning (Raineki et al., 2012, Raineki et al., 2010b, Sevelinges et al., 2011, Sullivan et al., 2000a, Sullivan et al., 2000b).”
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 Sevelinges et al., 2011
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Searle, J. R. (1980) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00005756 · Cited by 6,954 · see citing works
Depression: a new animal model sensitive to antidepressant treatments
PORSOLT, R. D., LE PICHON, M., & JALFRE, M. (1977) · Nature · doi:10.1038/266730a0 · Cited by 4,451 · see citing works
Nestler, E. J., Barrot, M., DiLeone, R. J., Eisch, A. J., Gold, S. J., & Monteggia, L. M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00653-0 · Cited by 3,217 · see citing works
Heim, C., & Nemeroff, C. B. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01157-x · Cited by 2,791 · see citing works
Drevets, W. C., Price, J. L., & Furey, M. L. (2008) · Brain Structure and Function · doi:10.1007/s00429-008-0189-x · Cited by 2,209 · cited 1× · see citing works
“Clinical studies have indicated that the amygdala is associated with depression (Dreverts et al., 2008; Monk et al., 2008; Nestler et al., 2002a,b; Ressler and Mayberg, 2007; Sheline et al., 1998; Whalen et al., 2002).”
Failure to escape traumatic shock.
Seligman, M. E., & Maier, S. F. (1967) · Journal of Experimental Psychology · doi:10.1037/h0024514 · Cited by 1,981 · cited 1× · see citing works
“These influences of early life shock and its predictabilitymay be limited to infancy, since the adult literature suggests that unpredictable adverse events are associated with depression-like behavior and related to the “learned helplessness” (Seligman and Maier, 1967; Sherman et al., 1979).”
The Amygdaloid Complex: Anatomy and Physiology
SAH, P., FABER, E. S. L., LOPEZ DE ARMENTIA, M., & POWER, J. (2003) · Physiological Reviews · doi:10.1152/physrev.00002.2003 · Cited by 1,745 · see citing works
Species-specific defense reactions and avoidance learning
Bolles, R. C. (1970) · Psychological Review · doi:10.1037/h0028589 · Cited by 1,610 · see citing works
The neurobiological consequences of early stress and childhood maltreatment
Teicher, M. H., Andersen, S. L., Polcari, A., Anderson, C. M., Navalta, C. P., & Kim, D. M. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00007-1 · Cited by 1,465 · see citing works
Swanson, L. W., & Petrovich, G. D. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01265-x · Cited by 1,351 · see citing works
Cortical pathways to the mammalian amygdala
McDonald, A. J. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00003-3 · Cited by 1,303 · see citing works
Handbook of Developmental Cognitive Neuroscience
(2008) · The MIT Press eBooks · doi:10.7551/mitpress/7437.001.0001 · Cited by 1,188 · see citing works
Gene-environment interplay and psychopathology: multiple varieties but real effects
Rutter, M., Moffitt, T. E., & Caspi, A. (2006) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2005.01557.x · Cited by 1,058 · see citing works
Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic
Ressler, K. J., & Mayberg, H. S. (2007) · Nature Neuroscience · doi:10.1038/nn1944 · Cited by 1,007 · see citing works
SÁNCHEZ, M. M., LADD, C. O., & PLOTSKY, P. M. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003029 · Cited by 1,003 · see citing works
Cicchetti, D., & Toth, S. L. (2005) · Annual Review of Clinical Psychology · doi:10.1146/annurev.clinpsy.1.102803.144029 · Cited by 861 · see citing works
The development of nociceptive circuits
Fitzgerald, M. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1701 · Cited by 778 · 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
Haberly, L. B., & Price, J. L. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901780408 · Cited by 680 · see citing works
Do early‐life events permanently alter behavioral and hormonal responses to stressors?
Anisman, H., Zaharia, M. D., Meaney, M. J., & Merali, Z. (1998) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(98)00025-2 · Cited by 654 · see citing works
Developmental determinants of sensitivity and resistance to stress
Levine, S. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.03.013 · Cited by 574 · see citing works
(2004) · PubMed · Cited by 567 · see citing works
Behavior of Nonhuman Primates.
Southwick, C. H. (1966) · PubMed Central · Cited by 567 · see citing works
GABAergic dysfunction in mood disorders
Brambilla, P., Pérez, J., Barale, F., Schettini, G., & Soares, J. C. (2003) · Molecular Psychiatry · doi:10.1038/sj.mp.4001362 · Cited by 567 · see citing works
Harlow, H. F., & Harlow, M. K. (1965) · Elsevier eBooks · doi:10.1016/b978-1-4832-2821-1.50008-2 · Cited by 564 · see citing works
Preclinical models: status of basic research in depression
Nestler, E. J., Gould, E., & Manji, H. K. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01405-1 · Cited by 559 · see citing works
Luskin, M. B., & Price, J. L. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902160305 · Cited by 552 · see citing works
Papp, M., Willner, P., & Muscat, R. (1991) · Psychopharmacology · doi:10.1007/bf02244188 · Cited by 542 · see citing works
Price, J. L. (1973) · The Journal of Comparative Neurology · doi:10.1002/cne.901500105 · Cited by 530 · see citing works
Helfer, R. E., & Kempe, C. H. (1974) · Medical Entomology and Zoology · Cited by 496 · see citing works
Amygdala core nuclei volumes are decreased in recurrent major depression
Sheline, Y. I., Gado, M. H., & Price, J. L. (1998) · NeuroReport · doi:10.1097/00001756-199806220-00021 · Cited by 472 · see citing works
From Fear to Safety and Back: Reversal of Fear in the Human Brain
Schiller, D., Levy, I., Niv, Y., LeDoux, J. E., & Phelps, E. A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2265-08.2008 · Cited by 429 · see citing works
Early life influences on life-long patterns of behavior and health
McEwen, B. S. (2003) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.10074 · Cited by 418 · see citing works
Pryce, C. R., Rüedi‐Bettschen, D., Dettling, A. C., Weston, A. A., Russig, H. D., Ferger, B., & Feldon, J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.011 · Cited by 414 · see citing works
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
Self-citationBrain development under stress: Hypotheses of glucocorticoid actions revisited
Oitzl, M. S., Champagne, D. L., van der Veen, R., & de Kloet, E. R. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.07.006 · Cited by 358 · see citing works
Haberly, L. B., & Price, J. L. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901810407 · Cited by 356 · see citing works
Monk, C. S., Klein, R. G., Telzer, E. H., Schroth, E. A., Mannuzza, S., Moulton, J. L., Guardino, M., Masten, C. L., McClure-Tone, E. B., Fromm, S., et al. (2008) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.06111917 · Cited by 335 · see citing works
Cameron, N. M., Champagne, F. A., Parent, C., Fish, E. W., Ozaki-Kuroda, K., & Meaney, M. J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.022 · Cited by 320 · see citing works
Good memories of bad events in infancy
Sullivan, R. M., Landers, M., Yeaman, B., & Wilson, D. A. (2000) · Nature · doi:10.1038/35024156 · Cited by 315 · see citing works
Self-citationThe amygdala, fear, and memory
FANSELOW, M. S., & GALE, G. D. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07077.x · Cited by 299 · see citing works
First Suckling Response of the Newborn Albino Rat: The Roles of Olfaction and Amniotic Fluid
Teicher, M. H., & Blass, E. M. (1977) · Science · doi:10.1126/science.918660 · Cited by 282 · see citing works
Toward a general theory of infantile attachment: a comparative review of aspects of the social bond
Rajecki, D. W., Lamb, M. E., & Obmascher, P. (1978) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00075816 · Cited by 266 · see citing works
Understanding the potency of stressful early life experiences on brain and body function
McEwen, B. S. (2008) · Metabolism · doi:10.1016/j.metabol.2008.07.006 · Cited by 260 · see citing works
Heim, C. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.041.2009 · Cited by 245 · see citing works
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
Self-citationDistinct neural signatures for safety and danger in the amygdala and striatum of the mouse.
Rogan, M. T., Leon, K. S., Pérez, D. L., & Kandel, E. (2005) · Neuron · doi:10.1016/j.neuron.2005.02.017 · Cited by 227 · see citing works
Cirulli, F., Francia, N., Berry, A., Aloe, L., Alleva, E., & Suomi, S. J. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.09.001 · Cited by 225 · see citing works
Unresolved attachment, PTSD, and dissociation in women with childhood abuse histories.
Stovall-McClough, K. C., & Cloître, M. (2006) · Journal of Consulting and Clinical Psychology · doi:10.1037/0022-006x.74.2.219 · Cited by 223 · see citing works
Roth, T. L., & Sullivan, R. M. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.01.032 · Cited by 204 · see citing works
Self-citationMuller, J. F., Mascagni, F., & McDonald, A. J. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20832 · Cited by 203 · see citing works
Freud, S. (1922) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-192210000-00046 · Cited by 193 · see citing works
Developing a neurobehavioral animal model of infant attachment to an abusive caregiver
Raineki, C., Moriceau, S., & Sullivan, R. M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.12.019 · Cited by 190 · see citing works
Self-citationInfantile Experience with Suckling Odors Determines Adult Sexual Behavior in Male Rats
Fillion, T. J., & Blass, E. M. (1986) · Science · doi:10.1126/science.3945807 · Cited by 188 · see citing works
Early life stress impairs fear conditioning in adult male and female rats
Kosten, T. A., Lee, H. J., & Kim, J. J. (2006) · Brain Research · doi:10.1016/j.brainres.2006.03.009 · Cited by 170 · see citing works
An Animal Model of a Behavioral Intervention for Depression
Pollak, D. D., Monje, F. J., Zuckerman, L., Denny, C. A., Drew, M. R., & Kandel, E. R. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.041 · Cited by 167 · see citing works
Evidence that maternal ventral skin substances promote suckling in infant rats☆☆☆
HOFER, M., Shair, H. N., & Singh, P. J. (1976) · Physiology & Behavior · doi:10.1016/0031-9384(76)90279-1 · Cited by 163 · see citing works
Functional neuroimaging studies of the amygdala in depression
Whalen, P. J., Shin, L. M., Somerville, L. H., McLean, A. A., & Kim, H. (2002) · Seminars in Clinical Neuropsychiatry · doi:10.1053/scnp.2002.35219 · Cited by 163 · see citing works
A neuropharmacologically-relevant animal model of depression
Sherman, A. D., Allers, G. L., Petty, F., et al. (1979) · Neuropharmacology · doi:10.1016/0028-3908(79)90087-x · Cited by 162 · see citing works
Ostroff, L. E., Cain, C. K., Bedont, J. L., Monfils, M., & LeDoux, J. E. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913384107 · Cited by 154 · see citing works
Early olfactory learning induces an enhanced olfactory bulb response in young rats
Sullivan, R. M., & Leon, M. (1986) · Developmental Brain Research · doi:10.1016/0165-3806(86)90256-7 · Cited by 151 · see citing works
Self-citationSluckin, W. (1979) · Cited by 148 · see citing works
Camp, L. L., & Rudy, J. W. (1988) · Developmental Psychobiology · doi:10.1002/dev.420210103 · Cited by 147 · see citing works
Matsuzawa-Yanagida, K., Narita, M., Nakajima, M., Kuzumaki, N., Niikura, K., Nozaki, H., Takagi, T., Tamai, E., Hareyama, N., Terada, M., et al. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301590 · Cited by 144 · see citing works
Feeding and Behavioral Activation in Infant Rats
HALL, W. G. (1979) · Science · doi:10.1126/science.451591 · Cited by 141 · see citing works
Sullivan, R. M., Hofer, M. A., & Brake, S. (1986) · Developmental Psychobiology · doi:10.1002/dev.420190612 · Cited by 134 · see citing works
Self-citationInhibition of infant glucocorticoid stress response: Specific role of maternal cues
Stanton, M. E., & Levine, S. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230504 · Cited by 132 · see citing works
Luskin, M. B., & Price, J. L. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902090304 · Cited by 116 · see citing works
Shishkina, G. T., Kalinina, T. S., & Дыгало, Н. Н. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.09.017 · Cited by 111 · see citing works
Tseng, G., & Haberly, L. B. (1988) · Journal of Neurophysiology · doi:10.1152/jn.1988.59.5.1352 · Cited by 106 · see citing works
Emergence of Interoceptive and Exteroceptive Control of Behavior in Rats
Haroutunian, V. H., & Campbell, B. A. (1979) · Science · doi:10.1126/science.472715 · Cited by 105 · see citing works
Experience‐Dependent Affective Learning and Risk for Psychopathology in Children
Pollak, S. D. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1301.011 · Cited by 103 · see citing works
Marr, J. N., & Gardner, L. E. (1965) · The Journal of Genetic Psychology · doi:10.1080/00221325.1965.10532774 · Cited by 99 · see citing works
Reconsideration of the role of the hippocampus in learned inhibition
Chan, K.-H., Morell, J. R., Jarrard, L. E., & Davidson, T. L. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00363-6 · Cited by 99 · see citing works
Integrating Neuroscience and Psychological Approaches in the Study of Early Experiences
Gunnar, M. R. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1301.024 · Cited by 97 · see citing works
Early Experience Modifies the Postnatal Assembly of Autonomic Emotional Motor Circuits in Rats
Card, J. P., Levitt, P. R., Gluhovsky, M. Y., & Rinaman, L. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2345-05.2005 · Cited by 97 · see citing works
Early Life Stress: Long-Term Physiological Impact in Rodents and Primates
Pryce, C. R., Rüedi‐Bettschen, D., Dettling, A. C., & Feldon, J. (2002) · Physiology · doi:10.1152/nips.01367.2001 · Cited by 96 · see citing works
Muigg, P., Hoelzl, U., Palfrader, K., Neumann, I. D., Wigger, A., Landgraf, R., & Singewald, N. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.08.035 · Cited by 87 · see citing works
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
Self-citationModified behavioral and olfactory bulb responses to maternal odors in preweanling rats
Sullivan, R. M., Wilson, D. A., Wong, R., Correa, A., & Leon, M. (1990) · Developmental Brain Research · doi:10.1016/0165-3806(90)90013-o · Cited by 81 · see citing works
Self-citationMainardi, D., Marsan, M., & Pasquali, A. (1965) · The Mouseion at the JAXlibrary (Jackson Laboratory) · Cited by 79 · see citing works
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
Self-citationRoche, M., Harkin, A., & Kelly, J. P. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301253 · Cited by 73 · see citing works
Conditioning of aversion to an odor paired with peripheral shock in the developing rat
Kucharski, D., & Spear, N. E. (1984) · Developmental Psychobiology · doi:10.1002/dev.420170505 · Cited by 71 · see citing works
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
Self-citationJosselyn, S., Falls, W., Gewirtz, J. C., Pistell, P., & Davis, M. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300530 · Cited by 66 · see citing works
The ontogenesis of defensive reactions to shock in preweanling rats
Collier, A. C., & Bolles, R. C. (1980) · Developmental Psychobiology · doi:10.1002/dev.420130206 · Cited by 63 · see citing works
Tyler, K., Moriceau, S., Sullivan, R. M., & Greenwood‐van Meerveld, B. (2007) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2007.00955.x · Cited by 63 · see citing works
Self-citationAttachment Relationship Experiences and Childhood Psychopathology
Zeanah, C. H., Keyes, A. W., & Settles, L. D. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1301.003 · Cited by 63 · see citing works
Varea, E., Castillo-Gómez, E., Gómez‐Climent, M. Á., Blasco‐Ibáñez, J. M., Crespo, C., Martinez-Guijarro, F. J., & Nácher, J. (2007) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2007.01.001 · Cited by 62 · see citing works
Castro, J. E., Varea, E., Márquez, C., Cordero, M. I., Poirier, G. L., & Sandi, C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008618 · Cited by 60 · see citing works
Neural correlates of conditioned odor avoidance in infant rats.
Sullivan, R. M., & Wilson, D. A. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.2.307 · Cited by 59 · see citing works
Self-citationBalu, D. T., Hodes, G. E., Anderson, B. T., & Lucki, I. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.234 · Cited by 58 · see citing works
Habituation of the forelimb-withdrawal response in neonatal rats.
Stehouwer, D. J., & Campbell, B. A. (1978) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.4.2.104 · Cited by 58 · see citing works
Moriceau, S. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.022.2009 · Cited by 57 · see citing works
Self-citationSevelinges, Y., Sullivan, R. M., Messaoudi, B., & Mouly, A. (2008) · Learning & Memory · doi:10.1101/lm.998508 · Cited by 55 · see citing works
Self-citationNeural correlates of conditioned odor avoidance in infant rats.
Sullivan, R. M., & Wilson, D. A. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.2.307 · Cited by 54 · see citing works
Self-citationMouly, A., & Scala, G. D. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.024 · Cited by 52 · see citing works
Self-citationHabituation of the forelimb-withdrawal response in neonatal rats.
Stehouwer, D. J., & Campbell, B. A. (1978) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.4.2.104 · Cited by 49 · see citing works
Ontogeny of Nociception and Antinociception
Barr, G. A. (1995) · PsycEXTRA Dataset · doi:10.1037/e495712006-011 · Cited by 47 · see citing works
Emerich, D. F., Scalzo, F. M., Enters, E. K., Spear, N. E., & SPEAR, L. P. (1985) · Developmental Psychobiology · doi:10.1002/dev.420180303 · Cited by 44 · see citing works
Aggressive Behavior in Abused Children
Connor, D. F., Doerfler, L. A., Volungis, A. M., Steingard, R. J., & Melloni, R. H. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1301.009 · Cited by 44 · see citing works
Savander, V., LeDoux, J. E., & Pitkänen, A. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(96)12750-6 · Cited by 43 · see citing works
Shah, A. A., Oxley, G., Lovic, V., & Fleming, A. S. (2002) · Developmental Psychobiology · doi:10.1002/dev.10064 · Cited by 40 · see citing works
Mother Lowers Glucocorticoid Levels of Preweaning Rats After Acute Threat
Wiedenmayer, C. P., Magariños, A. M., McEwen, B. S., & Barr, G. A. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1301.038 · Cited by 36 · see citing works
Early Olfactory Experience, Novelty, and Choice of Sexual Partner by Male Rats
Moore, C., JORDAN, L., & Wong, L. (1996) · Physiology & Behavior · doi:10.1016/s0031-9384(96)00249-1 · Cited by 32 · see citing works
Cándido, A., González, F., & de Brugada, I. (2004) · Behavioural Processes · doi:10.1016/j.beproc.2004.01.011 · Cited by 28 · see citing works
Bell, R. W., & Denenberg, V. H. (1963) · Animal Behaviour · doi:10.1016/0003-3472(63)90003-4 · Cited by 26 · see citing works
Princivalle, A. P., Spreafico, R., Bowery, N. G., et al. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.01060.x · Cited by 20 · see citing works
Sevelinges, Y., Lévy, F., Mouly, A., & Ferreira, G. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.003 · Cited by 19 · see citing works
Self-citationLong‐term impact of early olfactory experience on later olfactory conditioning
Blais, I., Terkel, J., & Goldblatt, A. (2006) · Developmental Psychobiology · doi:10.1002/dev.20176 · Cited by 14 · see citing works
Developmental origins of moral masochism: A failure-to-thrive toddler's interactions with mother
Haynes-Seman, C. (1987) · Child Abuse & Neglect · doi:10.1016/0145-2134(87)90005-6 · Cited by 9 · see citing works
Sevelinges, Y., Mouly, A., Lévy, F., & Ferreira, G. (2009) · Developmental Psychobiology · doi:10.1002/dev.20378 · Cited by 9 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- Haberly LB Price JL Association and commissural fiber systems of the olfactory cortex of the rat.II - Systems originating in the olfactory peduncle J. Com. Neurol 1978b 181 781 807 690285
Cited by
Sorted by citations
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
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
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
Self-citationGunnar, M. R., Hostinar, C. E., Sanchez, M. M., Tottenham, N., & Sullivan, R. M. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1070198 · Cited by 158 · see citing works
Self-citationOpendak, M., Gould, E., & Sullivan, R. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2017.02.002 · Cited by 94 · see citing works
Self-citationNorepinephrine, neurodevelopment and behavior
Saboory, E., Ghasemi, M., & Mehranfard, N. (2020) · Neurochemistry International · doi:10.1016/j.neuint.2020.104706 · Cited by 75 · see citing works
Raineki, C., Sarro, E., Rincón-Cortés, M., Perry, R., Boggs, J., Holman, C. J., Wilson, D. A., & Sullivan, R. M. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.266 · Cited by 71 · see citing works
Self-citationRaber, J., Arzy, S., Bertolus, J. B., Depue, B., Haas, H. E., Hofmann, S. G., Kangas, M., Kensinger, E., Lowry, C. A., Marusak, H. A., et al. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.03.015 · Cited by 62 · see citing works
Self-citation
- Authors
- Sevelinges, Y., Mouly, A.-M., Raineki, C., Moriceau, S., Forest, C., & Sullivan, R. M.
- Affiliations
- Lyon 1 Université (FR)
- Nathan Kline Institute for Psychiatric Research (US)
- University of Oklahoma (US)
- Corresponding author
- Sullivan, Regina M.
- Venue
- Developmental Cognitive Neuroscience
- Publisher
- Elsevier BV
- Published
- 2011-01
- Volume
- 1
- Issue
- 1
- Pages
- 77-87
- ISSN
- 1878-9293 (ISSN-L)
- PMC
- PMC2964861
- OpenAlex
- W1966526686
- Cited by
- 56
- References
- 114
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 2 · 2023: 1 · 2022: 1 · 2020: 5 · 2019: 5 · 2018: 2 · 2017: 5 · 2016: 9 · 2015: 3 · 2014: 8 · 2013: 5 · 2012: 4
- FWCI
- 3.50
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Developmental Cognitive Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Agence Nationale de la Recherche
- National Institutes of Health
- U.S. Public Health Service (NIHMH091451)
- National Institute of Mental Health (R01MH091451)
- National Institute on Deafness and Other Communication Disorders (DC-009910, R01DC009910)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- depression-like behavior, maternal odor, sensitive period, amygdala, piriform cortex, olfactory bulb, paired-pulse inhibition, forced swim test, sucrose preference, rat model
- MeSH terms
- Age Factors, Amygdala, Animals, Animals, Newborn, Association Learning, Conditioning, Psychological, Depression, Electric Stimulation, Female, Male, Object Attachment, Odorants, Olfactory Pathways, Pregnancy, Rats, Long-Evans, Rats
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