Brain opioids and mother—infant social motivation
Abstract
Brain opioids were the first neurochemical system to be implicated in the elaboration of socialbonding processes. Although a variety of neurochemical systems help elaborate social rewards and specific social behaviors, the role of opioids in the control of maternal behavior remains controversial. Although a great deal of data indicate that intermediate doses of morphine can reduce maternal behavior, the evidence, taken together, suggests that endogeneous opioids promote the regulatory control of maternal behavior, probably by providing feedback concerning the satisfaction that can be had from indulging in various maternal behaviors. Thus opioid blockade with naltrexone can reduce maternal competence in animals, while at the same time increasing maternal motivation. Opiate blockade likewise appears to increase the social motivation of rat pups, but reduces the reinforcing quality of interaction with the mother, suggesting that opioids provide feedback concerning the pleasurable qualities of social interaction in both mothers and infants. The clinical implications of this knowledge are not straightforward, but they generally suggest that clinically deficient social bonding might be capable of being strengthened via manipulation of brain opioid systems.
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These hedonic maternal response and behaviour-mediating brain circuits may be modulated by EO in a narrow physiological range by providing satisfaction feedback to augment reinforcement.
“These hedonic maternal response and behaviour-mediating brain circuits behaviours may be modulated by EO in a narrow physiological range by providing satisfaction feedback to augment reinforcement (59).”
From Neuroendocrinology of Parental Response to Baby‐Cry (2011) · cites this paper as [59]
Cites
The Physiology of Reproduction
Blandau, R. J. (1988) · JAMA · doi:10.1001/jama.1988.03410200127050 · Cited by 3,000 · see citing works
Endogenous opioids and social behavior
Panksepp, J., Herman, B. H., Vilberg, T., Bishop, P., & DeEskinazi, F. G. (1980) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(80)90036-6 · Cited by 531 · see citing works
Self-citationInsel, T. R. (1992) · Psychoneuroendocrinology · doi:10.1016/0306-4530(92)90073-g · Cited by 487 · see citing works
The psychobiology of play: Theoretical and methodological perspectives
Panksepp, J., Siviy, S., & Normansell, L. (1984) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(84)90005-8 · Cited by 468 · see citing works
Self-citationEndorphin-Mediated Increases in Pain Threshold During Pregnancy
Gintzler, A. R. (1980) · Science · doi:10.1126/science.7414330 · Cited by 341 · see citing works
Mammalian parenting; biochemical, neurobiological and behavioral determinants
(1991) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(91)90623-k · Cited by 196 · see citing works
The Physiological Control of Mammalian Vocalization
(1988) · Springer eBooks · doi:10.1007/978-1-4613-1051-8 · Cited by 180 · see citing works
Bridges, R. S., & Grimm, C. T. (1982) · Science · doi:10.1126/science.7123227 · Cited by 172 · see citing works
Opiates and play dominance in juvenile rats.
Panksepp, J., Jalowiec, J., DeEskinazi, F. G., & Bishop, P. (1985) · Behavioral Neuroscience · doi:10.1037/0735-7044.99.3.441 · Cited by 167 · see citing works
Self-citationOpiates and play dominance in juvenile rats.
Panksepp, J., Jalowiec, J. E., DeEskinazi, F. G., & Bishop, P. (1985) · Behavioral Neuroscience · doi:10.1037//0735-7044.99.3.441 · Cited by 167 · see citing works
Self-citationBrain Opioids and Social Emotions
Panksepp, J., Siviy, S. M., & NORMANSELL, L. A. (1985) · Elsevier eBooks · doi:10.1016/b978-0-12-586780-1.50006-9 · Cited by 165 · see citing works
Self-citationMorphine reduces social cohesion in rats
Panksepp, J., Najam, N., & Soares, F. (1979) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(79)90002-9 · Cited by 105 · see citing works
Self-citationKinsley, C. H., & Bridges, R. S. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230405 · Cited by 102 · see citing works
Opiate regulation of maternal behavior in the rat
Grimm, C. T., & Bridges, R. S. (1983) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(83)90336-2 · Cited by 97 · see citing works
Neural and Neurochemical Control of the Separation Distress Call
Panksepp, J., Normansell, L., Herman, B. H., Bishop, P., & Crepeau, L. J. (1988) · Springer eBooks · doi:10.1007/978-1-4613-1051-8_15 · Cited by 93 · see citing works
Self-citationBridges, R. S., & Ronsheim, P. M. (2008) · Neuroendocrinology · doi:10.1159/000124763 · Cited by 87 · see citing works
Opioid Receptor Subtype Involvement in Maternal Behavior in Lactating Rats
Mann, P. E., Kinsley, C. H., & Bridges, R. S. (2008) · Neuroendocrinology · doi:10.1159/000125762 · Cited by 86 · see citing works
Opioid peptides of the pituitary and hypothalamus: changes in pregnant and lactating rats
Petraglia, F., Baraldi, M., Giarrè, G., Facchinetti, F., Santi, M., Volpe, A., & Genazzani, A. R. (1985) · Journal of Endocrinology · doi:10.1677/joe.0.1050239 · Cited by 83 · see citing works
Naltrexone and other potential new pharmacological treatments of autism
Panksepp, J., Lensing, P., Leboyer, M., & Bouvard, M. P. (1991) · Brain dysfunction · Cited by 79 · see citing works
Self-citationKeverne, E. B., & Kendrick, K. M. (1991) · Brain Research · doi:10.1016/0006-8993(91)90492-e · Cited by 75 · see citing works
The psychobiology of prosocial behaviors: separation distress, play, and altruism
Panksepp, J. (1986) · Cambridge University Press eBooks · doi:10.1017/cbo9780511752834.003 · Cited by 50 · see citing works
Self-citationKendrick, K. M., & Keverne, E. B. (1989) · Brain Research · doi:10.1016/0006-8993(89)91462-5 · Cited by 49 · see citing works
Dorsomedial diencephalic involvement in the juvenile play of rats.
Siviy, S. M., & Panksepp, J. (1985) · Behavioral Neuroscience · doi:10.1037//0735-7044.99.6.1103 · Cited by 45 · see citing works
Self-citationOpiate antagonism reduces placentophagia and pup cleaning by parturient rats
Mayer, A. D., Faris, P. L., Komisaruk, B. R., & Rosenblatt, J. S. (1985) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(85)90314-4 · Cited by 43 · see citing works
Long-term effects of parity on opioid and nonopioid behavioral and endocrine responses
Mann, P. E., Kinsley, C. H., Ronsheim, P. M., & Bridges, R. S. (1989) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(89)90357-2 · Cited by 40 · see citing works
Kovács, G. L., Sarnyai, Z., Izbéki, F., Szabó, G., Telegdy, G., Barth, T., Jošt, K., & Brtník, F. (1987) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-5347(25)00277-0 · Cited by 30 · see citing works
Maternal Responsiveness in Humans: Emotional, Cognitive, and Biological Factors
Corter, C. M., & Fleming, A. S. (1990) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60201-6 · Cited by 26 · see citing works
Flagged first, then by citations
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Sorted by citations
Infant Intersubjectivity: Research, Theory, and Clinical Applications
Trevarthen, C., & Aitken, K. J. (2001) · Journal of Child Psychology and Psychiatry · doi:10.1111/1469-7610.00701 · Cited by 1,606 · see citing works
Neuroendocrine perspectives on social attachment and love
Sue Carter, C. (1998) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00055-9 · Cited by 1,425 · see citing works
“…endogenous opioids and prolactin affect parental behavior, possibly by modulating the rewarding aspects of this behavior (Panksepp, 1981; Panksepp et al., 1994, 1997), or by pacing of mother – infant interactions (Bridges, 1990), or through their documented abilities to influence the…”
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
“Such findings suggest that opiates provide a critical part of the neural basis on which primate sociality has evolved (Keverne et al. 1989; Nelson & Panksepp 1998; Panksepp et al. 1994).”
BackgroundInfluentialNelson, E. E., & Panksepp, J. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(97)00052-3 · Cited by 688 · see citing works
The Simulation of Smiles (SIMS) model: Embodied simulation and the meaning of facial expression
Niedenthal, P. M., Mermillod, M., Maringer, M., & Hess, U. (2010) · Behavioral and Brain Sciences · doi:10.1017/s0140525x10000865 · Cited by 618 · see citing works
Kamil, A. C. (2001) · Evolution and Human Behavior · doi:10.1016/s1090-5138(01)00068-x · Cited by 548 · see citing works
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
Neuroendocrine regulation of maternal behavior
Bridges, R. S. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.11.007 · Cited by 346 · see citing works
“Opioids: Opposing roles for opioids in maternal care have been proposed, including a stimulatory role (Panksepp et al., 1994) as well as inhibitory or disruptive role (Bridges and Grimm, 1982).”
BackgroundBurkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307 · see citing works
Responses to maternal separation : mechanisms and mediators
Kuhn, C. M., & Schanberg, S. M. (1998) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(98)00034-3 · Cited by 287 · see citing works
González, A., Lovic, V., Ward, G. R., Wainwright, P. E., & Fleming, A. S. (2000) · Developmental Psychobiology · doi:10.1002/1098-2302(2001)38:1 · Cited by 273 · see citing works
Separation distress call in the human neonate in the absence of maternal body contact
Christensson, K., Cabrera, T., Christensson, E., Uvnäs‐Moberg, K., & Winberg, J. (1995) · Acta Paediatrica · doi:10.1111/j.1651-2227.1995.tb13676.x · Cited by 234 · see citing works
Hormonal changes when falling in love
Marazziti, D., & Canale, D. (2003) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2003.08.006 · Cited by 219 · see citing works
“Consistent with this hypothesis is the observation that stress and threatening situations may facilitate the onset of new social bonds and intimate ties (Bowlby, 1973; Reite, 1985; Kraemer, 1992; Panksepp et al., 1994).”
BackgroundPANKSEPP, J., NELSON, E., & BEKKEDAL, M. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51914.x · Cited by 210 · see citing works
Self-citationStress physiology and developmental psychopathology: Past, present, and future
Doom, J. R., & Gunnar, M. R. (2013) · Development and Psychopathology · doi:10.1017/s0954579413000667 · Cited by 204 · see citing works
Fleming, A. S., Kraemer, G. W., Gonzalez, A., Lovic, V., Rees, S., & Melo, A. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00793-1 · Cited by 203 · see citing works
“, 1994), important for affiliation and postpartum maternal behavior (Insel, 1997; Noonan et al., 1994; Panksepp et al., 1994; Uvans-Moberg, 1998).”
BackgroundToward a neuroscience of attachment.
Coan, J. A. (2008) · Cited by 192 · see citing works
Van Ree, J. M., Niesink, R. J. M., Van Wolfswinkel, L., Ramsey, N. F., Kornet, M. (. ). M. W., Van Furth, W. R., Vanderschuren, L. J. M. J., Gerrits, M. A. F. M., & Van den Berg, C. L. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00544-6 · Cited by 166 · see citing works
The neuroendocrinology of primate maternal behavior
Wendy Saltzman, A., & Dario Maestripieri, A. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.09.017 · Cited by 150 · see citing works
“This " brain opioid theory of social attachment " has been supported by numerous findings in a variety of mammalian and avian species, including studies of mother–infant interactions (reviewed by Panksepp et al., 1980, 1994; Maestripieri, 2010).”
ResultTranslating mouse vocalizations: prosody and frequency modulation1
Lahvis, G. P., Alleva, E., & Scattoni, M. L. (2010) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2010.00603.x · Cited by 140 · see citing works
“…numbers of USVs during maternal separation (Moles et al. 2004), consistent with the evidence that enkephalin interactions with mu-opioid receptor can mediate social reward and isolation distress (Bertrand et al. 1997, Kalin et al. 1988, Panksepp et al. 1980, 1994, Vanderschuren et al. 1995).”
ResultThe social brain: Neurobiological basis of affiliative behaviours and psychological well-being
Walker, S. C., & McGlone, F. P. (2013) · Neuropeptides · doi:10.1016/j.npep.2013.10.008 · Cited by 138 · see citing works
“…animals studies provide evidence that endogenous opioids mediate the rewarding effects of a number of social behaviours, including infant attachment, maternal behaviour, social play and allogrooming (Panksepp et al., 1981, 1994; Vanderschuren et al., 1997; Dunbar, 2010; D’Amato and Pavone, 2012).”
BackgroundInfluentialWirth, M. M., & Schultheiss, O. C. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.08.003 · Cited by 139 · see citing works
Waller, R. E., & Wagner, N. J. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.10.005 · Cited by 138 · see citing works
Burkett, J. P., Spiegel, L. L., Inoue, K., Murphy, A. Z., & Young, L. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.117 · Cited by 133 · see citing works
The Neurobiology of Social Affiliation and Pair Bonding
Carter, C. S., & Keverne, E. B. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00004-8 · Cited by 128 · see citing works
Breastfeeding and the mother–infant relationship—A review
JANSEN, J., de Weerth, C., & Riksen‐Walraven, J. M. (2008) · Developmental Review · doi:10.1016/j.dr.2008.07.001 · Cited by 126 · see citing works
“The maternal bond, therefore, may be the result of the motivation and rewards associated with carrying out maternal caregiving behavior, as was previously suggested by Panksepp, Nelson, and Siviy (1994).”
BackgroundResultOpiate systems in mother and infant primates coordinate intimate contact during reunion
Kalin, N. H., Shelton, S. E., & Lynn, D. E. (1995) · Psychoneuroendocrinology · doi:10.1016/0306-4530(95)00023-2 · Cited by 122 · see citing works
“During the postnatal period, high-dose morphine, in contrast to lower doses, disrupts maternal behavior in rodents (Mann et al., 1990; Rubin & Bridges, 1984; Panksepp et al., 1994).”
BackgroundSync to link: Endorphin-mediated synchrony effects on cooperation
Lang, M., Bahna, V., Shaver, J. H., Reddish, P., & Xygalatas, D. (2017) · Biological Psychology · doi:10.1016/j.biopsycho.2017.06.001 · Cited by 120 · see citing works
Oxytocin mediates acquisition of maternally associated odor preferences in preweanling rat pups.
Nelson, E. E., & Panksepp, J. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.3.583 · Cited by 113 · see citing works
Self-citationHormonal Physiology of Childbearing: Evidence and Implications for Women, Babies, and Maternity Care
Buckley, S. J. (2015) · Issue Lab (Candid) · Cited by 113 · see citing works
The Neurobiology of Social Affiliation and Pair Bonding
Carter, C. S., & Keverne, E. B. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50006-8 · Cited by 109 · see citing works
Neuroendocrinology of Parental Response to Baby‐Cry
Swain, J. E., Kim, P., & Ho, S. S. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02212.x · Cited by 106 · see citing works
Byrnes, E. M., Rigero, B. A., & Bridges, R. S. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00941-3 · Cited by 90 · see citing works
Alcoholics Anonymous: Cult or Cure?
Vaillant, G. E. (2005) · Australian & New Zealand Journal of Psychiatry · doi:10.1080/j.1440-1614.2005.01600.x · Cited by 87 · see citing works
Schaal, B., & Marlier, L. (1998) · Neonatology · doi:10.1159/000014033 · Cited by 85 · see citing works
Byrnes, E. M. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0122-4 · Cited by 77 · see citing works
“Opioids are known to influence various components of maternal behavior, including placentophagia (Mayer et al. 1985), maternal motivation (Nelson and Panksepp 1998; Panksepp et al.1994), as well as the amount of time the dam spends nursing her pups (Byrnes et al. 2000).”
BackgroundMeditative analgesia: the current state of the field
Grant, J. A. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12282 · Cited by 78 · see citing works
McClintock, C. H., Lau, E., & Miller, L. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.01600 · Cited by 73 · see citing works
The neuroanatomical delineation of agentic and affiliative extraversion
Grodin, E. N., & White, T. L. (2015) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-014-0331-6 · Cited by 72 · see citing works
Ulmer-Yaniv, A., Avitsur, R., Kanat-Maymon, Y., Schneiderman, I., Zagoory-Sharon, O., & Feldman, R. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2016.02.017 · Cited by 68 · see citing works
Pereira, M., & Ferreira, A. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.08.005 · Cited by 68 · see citing works
“…system is associated with social rewards, affiliation and attenuation of the reaction to social separation (Berridge and Robinson 2003) and has been proposed to be critical during the initial stages of mother-young attachment (Nelson and Panksepp 1998; Panksepp et al. 1994; Swain et al. 2011).”
BackgroundJohnson, N. L., Carini, L. M., Schenk, M. E., Stewart, M., & Byrnes, E. M. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00029 · Cited by 67 · see citing works
“In a number of species, including humans and non-human primates, endogenous opioids modulate affiliative behaviors, including mother–infant attachment (Panksepp et al., 1994; Kalin et al., 1995; Nelson and Panksepp, 1998; Saltzman and Maestripieri, 2010).”
BackgroundThe neuroscience of emotion in music
Panksepp, J., & Trevarthen, C. (2008) · Oxford University Press eBooks · doi:10.1093/oso/9780198566281.003.0007 · Cited by 66 · see citing works
Self-citationMAYES, L. C. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1376.018 · Cited by 79 · see citing works
Paternal vs Maternal Kangaroo Care for Procedural Pain in Preterm Neonates
Johnston, C. C. (2011) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpediatrics.2011.130 · Cited by 63 · see citing works
Emery, M. A., & Akil, H. (2020) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-110719-095912 · Cited by 56 · see citing works
“…endogenous opioid system on social bonding inmammals, as well as influencing human feelings of social connection, is well established (Inagaki 2018, Panksepp et al. 1994, Resendez et al. 2016) and is perturbed by the use of opiate drugs (Ragen et al. 2015, Rubin & Bridges 1984,Wang et al. 2018).”
BackgroundNeural mechanisms of the link between giving social support and health
Inagaki, T. K. (2018) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13703 · Cited by 62 · see citing works
Opioids and attachment in rhesus macaque (Macaca mulatta) abusive mothers.
Graves, F. C., Wallen, K., & Dario Maestripieri, A. (2002) · Behavioral Neuroscience · doi:10.1037//0735-7044.116.3.489 · Cited by 61 · see citing works
“This hypothesis has been supported by many studies of nonprimate animals such as rats, voles, guinea pigs, and chicks (Nelson & Panksepp 1998; Panksepp, Herman, Vilberg, Bishop, & DeEskinazi, 1980; Panksepp, Nelson, & Siviy, 1994 ).”
ResultCoping in groups of domestic horses – Review from a social and neurobiological perspective
Dierendonck, M. C. V., & Spruijt, B. M. (2012) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2012.02.007 · Cited by 61 · see citing works
Cinque, C., Pondiki, S., Oddi, D., Certo, M. G. D., Marinelli, S., Troisi, A., Moles, A., & D'Amato, F. R. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.83 · Cited by 58 · see citing works
The Biopsychology of Maternal Behavior in Nonhuman Mammals
Kristal, M. B. (2009) · ILAR Journal · doi:10.1093/ilar.50.1.51 · Cited by 57 · see citing works
“Opioids also contribute to the onset and maintenance of maternal behavior, not only because of the interaction with oxytocin but also almost certainly because of the importance of opioids to motivation and reward (Nelson and Panksepp 1998; Panksepp et al. 1994) and to pain and hypoalgesia.”
Measuring dog-owner relationships: Crossing boundaries between animal behaviour and human psychology
Rehn, T., & Keeling, L. J. (2016) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2016.07.003 · Cited by 54 · see citing works
Kalinichev, M., Easterling, K. W., & Holtzman, S. G. (2000) · Psychopharmacology · doi:10.1007/s002130000556 · Cited by 54 · see citing works
“Inhibition of active maternal behavior during the suckling bout may quiet the female and thereby contribute to the homeostasis in regulating maternal care ( Panksepp et al. 1994; Bridges 1996).”
BackgroundInfluentialRoth, T. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00961-7 · Cited by 50 · see citing works
“Learning and memory are critical to the normal development of mother–infant relationships, and opioids have a direct impact on this learning in both infants and adults in several species [7,8,19,55,57,67,87].”
BackgroundThe impact of postnatal environment on opioid peptides in young and adult male Wistar rats
Gustafsson, L., Oreland, S., Hoffmann, P., & Nylander, I. (2007) · Neuropeptides · doi:10.1016/j.npep.2007.10.006 · Cited by 48 · see citing works
Establishment of a preference by the newborn lamb for its mother: The role of opioids.
Shayit, M., Nowak, R., Keller, M., & Weller, A. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.3.446 · Cited by 43 · see citing works
Nocjar, C., & Panksepp, J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.04.004 · Cited by 44 · see citing works
Self-citationThe neurobiological link between compassion and love
Esch, T., & Stefano, G. B. (2011) · Medical Science Monitor · doi:10.12659/msm.881441 · Cited by 41 · see citing works
Addiction and reward-related genes show altered expression in the postpartum nucleus accumbens
Zhao, C., Eisinger, B. E., Driessen, T. M., & Gammie, S. C. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00388 · Cited by 39 · see citing works
“A role for endogenous opioids in maternal care has previously been suggested (Panksepp et al., 1994) and here a new insight may be that rewards from other signals are reduced in mothers, while rewards from offspring are enhanced.”
BackgroundNylander, I., & Roman, E. (2012) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2012.00077 · Cited by 40 · see citing works
“Opioids modulate social behavior, especially social interactions early in life, and several lines of evidence support a functional role of opioids in parental behavior and social bonding processes (Panksepp et al., 1980, 1994; Nelson and Panksepp, 1998).”
BackgroundPanksepp, J. (2001) · Neuropsychoanalysis · doi:10.1080/15294145.2001.10773353 · Cited by 39 · see citing works
“One can also imagine that pharmacological modulation of these chemistries might alleviate early bonding problems between mothers and children (Panksepp et al., 1994a), but at present there is insufficient evidence to make any data-based prescriptions in this realm.”
Self-citationExamining the role of endogenous opioids in learned odor–stroke associations in infant rats
Roth, T. L., & Sullivan, R. M. (2005) · Developmental Psychobiology · doi:10.1002/dev.20107 · Cited by 38 · see citing works
Sinha, S. S., Goetz, R. R., & Klein, D. F. (2006) · Psychiatry Research · doi:10.1016/j.psychres.2004.11.011 · Cited by 38 · see citing works
Schwandt, M. L., Lindell, S. G., Higley, J. D., Suomi, S. J., Heilig, M. A., & Barr, C. S. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.03.002 · Cited by 37 · see citing works
“…and behavioral outcomes, including anti-nociception, reward, immune function, gastrointestinal function, social attachment, and stress response (Panksepp et al., 1994; Van Ree et al., 2000; Drolet et al., 2001; Bodnar, 2004; Ribeiro et al., 2005; Frew and Drummond, 2007; Sher and Stanley,…”
Changes in adaptability following perinatal morphine exposure in juvenile and adult rats
Klausz, B., Pintér, O., Sobor, M., Gyarmati, Z., Fürst, Z., Tímár, J., & Zelena, D. (2010) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2010.11.025 · Cited by 38 · see citing works
Genetic and neuroendocrine regulation of the postpartum brain
Gammie, S. C., Driessen, T. M., Zhao, C., Saul, M. C., & Eisinger, B. E. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.05.002 · Cited by 35 · see citing works
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript and dynorphin (Pdyn) (Panksepp et al., 1994; Parada et al., 2008; Higham et al., 2011; Mileva-Seitz et al., 2012; de Moura et al., 2015); shown in red circles in Fig.”
BackgroundThe neurochemistry of social reward during development: What have we learned from rodent models?
Manduca, A., Carbone, E., Schiavi, S., Cacchione, C., Buzzelli, V., Campolongo, P., & Trezza, V. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15321 · Cited by 34 · see citing works
“…coworkers, opioids alter the competence in maternal behavior rather than the motivation of the mother in eliciting this early form of interaction (Panksepp et al. 1994): Thus, low doses of morphine did not reduce the mother's tendency to maintain proximity to the pups (i.e., when pups were…”
BackgroundA full belly and colostrum: Two major determinants of filial love
Val‐Laillet, D., Simon, M., & Nowak, R. (2004) · Developmental Psychobiology · doi:10.1002/dev.20024 · Cited by 35 · see citing works
The neuroevolutionary and neuroaffective psychobiology of the prosocial brain
Panksepp, J. (2012) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780198568308.013.0012 · Cited by 34 · see citing works
Self-citationOpioid receptor antagonism during early lactation results in the increased duration of nursing bouts
Byrnes, E. M., Rigero, B. A., & Bridges, R. S. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00231-6 · Cited by 33 · see citing works
Romantic love evolved by co-opting mother-infant bonding
Bode, A. (2023) · Frontiers in Psychology · doi:10.3389/fpsyg.2023.1176067 · Cited by 31 · see citing works
Kalinichev, M., Easterling, K. W., & Holtzman, S. G. (2002) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300068 · Cited by 31 · see citing works
“…endogenous opioids modulate maternal motivation (Panksepp et al, 1994) as well as inhibit active maternal behaviors during nursing bouts in rats and mice (Haney and Miczek, 1989; Mann et al, 1991), thereby contributing to homeostasis in maternal care (Panksepp et al, 1994; Bridges, 1996).”
Nowak, R. (2006) · Advances in the study of behavior · doi:10.1016/s0065-3454(06)36001-9 · Cited by 28 · see citing works
Bornstein, M. H. (2013) · Psychology Press eBooks · doi:10.4324/9781410612144 · Cited by 27 · see citing works
κ-opioid receptor as a key mediator in the regulation of appetitive 50-kHz ultrasonic vocalizations
Hamed, A., Szyndler, J., Taracha, E., Turzyńska, D., Sobolewska, A., Lehner, M., Krząścik, P., & Daszczuk, P. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3824-7 · Cited by 26 · see citing works
“…data indicate that the endogenous opioid system may play a role in the motivational and hedonic properties of food, drug rewards, and social play (Panksepp et al. 1985, 1994; Vanderschuren et al. 1997; Siviy et al. 1997; Ikemoto and Pankepp 1999; Trezza et al. 2010; Wassum et al. 2009; Barbano…”
BackgroundWallin, C. M., Bowen, S. E., & Brummelte, S. (2021) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2021.106976 · Cited by 25 · see citing works
Toward a Neuroscience of Emotion
Panksepp, J., Knutson, B. D., & Pruitt, D. L. (1998) · Springer eBooks · doi:10.1007/978-1-4899-1939-7_3 · Cited by 26 · see citing works
Self-citationWagner, N. J., Waller, R. E., Flom, M., Ronfard, S., Fenstermacher, S. K., & Saudino, K. J. (2020) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13182 · Cited by 25 · see citing works
Low social affiliation predicts increases in callous‐unemotional behaviors in early childhood
Perlstein, S., Waller, R. E., Wagner, N. J., & Saudino, K. J. (2021) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13466 · Cited by 25 · see citing works
Eisinger, B. E., Driessen, T. M., Zhao, C., & Gammie, S. C. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00110 · Cited by 24 · see citing works
“It is likely that the involvement of the opioid system in the maternal brain is complex and could be involved in multiple maternal processes, including the bonding of mothers to offspring (Panksepp et al., 1994; Nelson and Panksepp, 1998).”
BackgroundOur social baseline: The role of social proximity in economy of action.
Coan, J. A., Brown, C. L., & Beckes, L. (2013) · American Psychological Association eBooks · doi:10.1037/14250-006 · Cited by 23 · see citing works
McMillan, F. D. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.09.013 · Cited by 23 · see citing works
Fineberg, S. K., Steinfeld, M., Brewer, J. A., & Corlett, P. R. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00111 · Cited by 21 · see citing works
“He highlights the work of Jaak Panksepp in identifying a common neurobiology for mother– infant, infant–mother, and romantic attachments that involve opioids expressed in the frontostriatal dopaminergic circuitry (48).”
BackgroundWellman, J., Carr, D., Graham, A., Jones, H. E., Humm, J., Ruscio, M., Billack, B., & Kinsley, C. H. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00111-1 · Cited by 20 · see citing works
Šlamberová, R., Bar, N., & Vathy, I. (2003) · Developmental Psychobiology · doi:10.1002/dev.10141 · Cited by 20 · see citing works
Roth, T., Moriceau, S., & Sullivan, R. (2006) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.301206 · Cited by 22 · see citing works
“pups (Panksepp et al. 1994).”
BackgroundBiparental care, tactile stimulation and evolution of sociality in rodents
Gromov, V. S. (2011) · Journal of Evolutionary Biology Research · doi:10.5897/jebr.9000002 · Cited by 19 · see citing works
Sexuality in Labour and Birth: An Intimate Perspective
Buckley, S. J. (2010) · doi:10.1002/9781444317701.ch12 · Cited by 17 · see citing works
Endocrine factors of pair bonding.
Stárka, L. (2007) · PubMed · Cited by 15 · see citing works
Volkow, N. D. (2016) · BMJ · doi:10.1136/bmj.i19 · Cited by 14 · see citing works
Soares, J. A. G., Sutley-Koury, S. N., Pomrenze, M. B., & Tucciarone, J. (2025) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2024.1521016 · Cited by 13 · see citing works
Positive Emotions and the Success of Alcoholics Anonymous
Vaillant, G. E. (2014) · Alcoholism Treatment Quarterly · doi:10.1080/07347324.2014.907032 · Cited by 12 · see citing works
Campbell-Yeo, M. L., Benoit, B., Newman, A. J., Johnston, C. C., Bardouille, T., Stevens, B., & Jiang, A. (2022) · Trials · doi:10.1186/s13063-022-06424-4 · Cited by 12 · see citing works
Social Interactions in the Clinic and the Cage: Toward a More Valid Mouse Model of Autism
Lahvis, G. P., & Black, L. M. (2010) · Neuromethods · doi:10.1007/978-1-60761-883-6_7 · Cited by 11 · see citing works
Gescher, D. M., Schanze, D., Vavra, P., Wolff, P., Zimmer‐Bensch, G., Zenker, M., Frodl, T., & Schmahl, C. G. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02628-z · Cited by 10 · see citing works
Neurobehavioral Development of Infant Learning and Memory: Implications for Infant Attachment
Roth, T. L., Wilson, D. A., & Sullivan, R. M. (2004) · Advances in the study of behavior · doi:10.1016/s0065-3454(04)34003-9 · Cited by 10 · see citing works
Christou, A. I., Fanti, K. A., Mavrommatis, I., Soursou, G., Pergantis, P., & Drigas, A. S. (2025) · Children · doi:10.3390/children12040524 · Cited by 9 · see citing works
Perlstein, S., Wagner, N. J., Domínguez-Álvarez, B., Fraguela, J. A. G., Romero, E., López‐Romero, L., & Waller, R. E. (2022) · Assessment · doi:10.1177/10731911221128946 · Cited by 7 · see citing works
“Similarly, distinct genetically mediated neurotransmitter pathways are thought to differentially give rise to the processing of fear-related (Holsboer & Ising, 2009) versus affiliative cues (Baskerville & Douglas, 2010; Panksepp et al., 1994).”
BackgroundTchalova, K., Lydon, J. E., Atkinson, L. R., Fleming, A. S., Kennedy, J. L., Lecompte, V., Meaney, M. J., Moss, E., O’Donnell, K. A., O’Donnell, K. J., et al. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02888-x · Cited by 7 · see citing works
“It is thought that this emotional bond between infants and their caregivers is rooted in evolutionarily ancient neural systems involved in processing pain and reward [3, 4].”
BackgroundLe bon dieu est dans le detail: Is smiling the recognition of happiness?
Dols, J. M. F., & Carrera, P. (2010) · Behavioral and Brain Sciences · doi:10.1017/s0140525x10001512 · Cited by 7 · see citing works
- Authors
- Panksepp, J., Nelson, E., & Siviy, S.
- Affiliations
- Bowling Green State University (US)
- Corresponding author
- Panksepp, Jaak
- ORCID
- Nelson, Eric
- Venue
- Acta Paediatrica
- Publisher
- Wiley
- Published
- 1994-06
- Volume
- 83
- Issue
- s397
- Pages
- 40-46
- ISSN
- 0365-1436 (ISSN-L)
- 0803-5253
- 1651-2227
- OpenAlex
- W1997676465
- Cited by
- 133
- References
- 26
- Citations by year
- 2025: 3 · 2024: 3 · 2023: 2 · 2022: 3 · 2021: 4 · 2020: 4 · 2019: 1 · 2018: 3 · 2017: 1 · 2016: 7 · 2015: 4 · 2014: 8 · 2013: 7 · 2012: 6
- FWCI
- 0.73
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Acta Paediatrica (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (1r15hd030387-01)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (1 R15 HD 30387-01)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- endogenous opioids, maternal behavior, social motivation, morphine, naltrexone, opioid blockade, maternal competence, social reward, neonatal rats
- MeSH terms
- Animals, Biofeedback, Psychology, Female, Humans, Infant, Infant, Newborn, Maternal Behavior, Morphine, Mother-Child Relations, Motivation, Naltrexone, Object Attachment, Social Behavior
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