Cited by 689Neuroendocrine regulation and behaviorAttachment and Relationship DynamicsHuman-Animal Interaction Studies

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Brain substrates of infant-mother attachment: contributions of opioids, oxytocin, and norepinephrine.

Nelson, Eric E, Panksepp, Jaak·1998·Neuroscience & Biobehavioral Reviews

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Abstract

The aim of this paper is to review recent work concerning the psychobiological substrates of social bonding, focusing on the literature attributed to opioids, oxytocin and norepinephrine in rats. Existing evidence and thinking about the biological foundations of attachment in young mammalian species and the neurobiology of several other affiliative behaviors including maternal behavior, sexual behavior and social memory is reviewed. We postulate the existence of social motivation circuitry which is common to all mammals and consistent across development. Oxytocin, vasopressin, endogenous opioids and catecholamines appear to participate in a wide variety of affiliative behaviors and are likely to be important components in this circuitry. It is proposed that these same neurochemical and neuroanatomical patterns will emerge as key substrates in the neurobiology of infant attachments to their caregivers.

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“This circuitry is also influenced by opioids, which facilitates sociosexual behavior in mammals (Depue and Morrone-Strupinsky, 2005; Nelson and Panksepp, 1998).”
Background
The contribution of total and free iodothyronines to welfare maintenance and management stress coping in Ruminants and Equines: Physiological ranges and reference values
Ferlazzo, A., Cravana, C., Fazio, E., & Medica, P. (2018) · Research in Veterinary Science · doi:10.1016/j.rvsc.2018.01.025 · Cited by 19
Childhood Abuse, Attachment, and Psychopathy among Individuals Who Commit Sexual Offenses
Grady, M. D., Looman, J., & Abracen, J. (2019) · Sexual Addiction & Compulsivity The Journal of Treatment and Prevention · doi:10.1080/10720162.2019.1620660 · Cited by 19
“These patterns of dysregulation can then contribute to a range of other interactional patterns (Nelson & Panksepp, 1998) including antisocial impulsivity, depression, hypersexuality (Kafka, 2003), and sexual violence (Beech & Mitchell, 2005; Mitchell & Beech, 2011).”
Background
Prenatal stress produces sex differences in nest odor preference
de Souza, M. A., Szawka, R. E., Centenaro, L. A., Diehl, L. A., & Lucion, A. B. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.10.012 · Cited by 19
Biparental 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
Empathic Concern
Batson, C. D. (2023) · doi:10.1093/oso/9780197610923.001.0001 · Cited by 24
Effects of Rearing Conditions on Behaviour and Endogenous Opioids in Rats with Alcohol Access during Adolescence
Palm, S., Daoura, L., Roman, E., & Nylander, I. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076591 · Cited by 18
“These data together with the involvement of opioids in early life social behaviour [43-47] indicate a possible link between early life environment, opioids and adult drinking behaviour.”
Background
The origin of REM sleep: A hypothesis.
Tsoukalas, I. (2012) · Dreaming · doi:10.1037/a0030790 · Cited by 18
Interactions between the κ opioid system, corticotropin-releasing hormone and oxytocin in partner loss
Bales, K. L., & Rogers, F. D. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0061 · Cited by 17
Neurobiology and Moral Mindset
Narvaez, D. F. (2013) · SensePublishers eBooks · doi:10.1007/978-94-6209-275-4_19 · Cited by 18
Specific reduction in the cortisol awakening response after socio-affective mental training
Engert, V., Hoehne, K., & Singer, T. (2023) · Mindfulness · doi:10.1007/s12671-023-02074-y · Cited by 17
“From a mechanistic perspective, we suggest that Affect training stimulates care- and affiliation-based systems that are associated with positive affect (Klimecki et al., 2013; McCall & Singer, 2012), and modulated by oxytocin and opiates (Depue & Morrone-Strupinsky, 2005; Nelson & Panksepp, 1998).”
Background
You and your kin: Neural signatures of family-based group perception in the subgenual cortex
Rüsch, N., Bado, P., Zahn, R., Bramati, I. E., de Oliveira‐Souza, R., & Moll, J. (2014) · Social Neuroscience · doi:10.1080/17470919.2014.912676 · Cited by 17
“Research in humans and animal models has implicated a number of cortical and subcortical structures in social attachment mechanisms and prosocial behaviors (Insel & Young, 2001; Moll, Zahn, de OliveiraSouza, Krueger, & Grafman, 2005; Nelson & Panksepp, 1998).”
Background
Beta-endorphin levels in longtailed and pigtailed macaques vary by abnormal behavior rating and sex
Crockett, C. M., Sackett, G. P., Sandman, C. A., Chicz-DeMet, A., & Bentson, K. L. (2007) · Peptides · doi:10.1016/j.peptides.2007.07.014 · Cited by 17
“The role of endogenous opioids in behavior has been investigated using opioid antagonists, or blockers, such as naloxone and naltrexone, which eliminate the potentially rewarding properties of euphoria and pain attenuation [3,30,35].”
Background
Pharmacological and methodological aspects of the separation-induced vocalization test in guinea pig pups; a systematic review and meta-analysis
Groenink, L., Verdouw, P. M., Bakker, B., & Wever, K. E. (2014) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2014.10.062 · Cited by 17
Dopamine's role in social modulation of infant isolation‐induced vocalization: I. Reunion responses to the dam, but not littermates, are dopamine dependent
Shair, H. N., Muller, J. M., & Moore, H. M. (2008) · Developmental Psychobiology · doi:10.1002/dev.20353 · Cited by 17
Cross‐genus adoptions in delphinids: One example with taxonomic discussion
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Rejection: Resolving the Paradox of Emotional Numbness after Exclusion
DeWall, C. N., Baumeister, R. F., & Masicampo, E. J. (2009) · Cambridge University Press eBooks · doi:10.1017/cbo9780511770548.008 · Cited by 17
Neuro-Evolutionary Foundations of Infant Minds: From Psychoanalytic Visions of How Primal Emotions Guide Constructions of Human Minds toward Affective Neuroscientific Understanding of Emotions and Their Disorders
Panksepp, J., Clarici, A., Vandekerckhove, M. M. P., & Yovell, Y. (2019) · Psychoanalytic Inquiry · doi:10.1080/07351690.2019.1549910 · Cited by 16
“Animal research is rich in evidence concerning the mechanisms of emotion that promote social attachments (Nelson and Panksepp, 1998; Panksepp, 1998; Panksepp and Burgdorf, 2003), and it is informative about the adverse consequences for the developing organism when the appeals of offspring for…”
Background
Maternal physiological calming responses to infant suckling at the breast
Ohmura, N., Okuma, L., Truzzi, A., Esposito, G., & Kuroda, K. O. (2023) · The Journal of Physiological Sciences · doi:10.1186/s12576-023-00860-w · Cited by 16
“Gastric distention by milk ingestion has been shown to elevate plasma oxytocin in the offspring in animal models, which possibly induces satiety and positive psychological effects [23, 25, 31].”
Background
Touching to connect, explore, and explain: how the human brain makes social touch meaningful
Morrison, I. (2023) · The Senses and Society · doi:10.1080/17458927.2023.2200065 · Cited by 19
“The late neuroscientist Jaak Panksepp proposed that core functional properties of the mu-opioid system, as well as the oxytocin system, have been co-opted into the social realm and further elaborated by natural selection (Nelson and Panksepp 1998).”
Background
Toward a Theory of Holistic Needs and the Brain
Silton, N. R., Flannelly, L. T., Flannelly, K. J., & Galek, K. (2011) · Holistic Nursing Practice · doi:10.1097/hnp.0b013e31822a0301 · Cited by 16
Basic emotional foundations of social dominance in relation to Panksepp's affective taxonomy
van der Westhuizen, D., & Solms, M. (2015) · Neuropsychoanalysis · doi:10.1080/15294145.2015.1021371 · Cited by 17
“…that the onset of puberty and other developmental periods such as mating and pregnancy, which significantly increase the production and synthesis of gonadal hormones, likely exerts widespread modulations in the organization of androgen sensitive circuits in the brain (Nelson & Panksepp, 1998).”
Background
Social status, social support, and stress: a comparative review of the health consequences of social control factors
Beck, L. (2007) · Health Psychology Review · doi:10.1080/17437190802217246 · Cited by 18
“These effects have been demonstrated in a range of species, including juvenile rats, adult mice, monkeys, and chicks, and neuroanatomical similarities suggest that the role of social interaction in triggering endogenous opioid release may be generalisable to humans (Nelson & Panksepp, 1998).”
Background
Amniotic Fluid as an Extended Milieu Intérieur
Robinson, S. R., & Méndez‐Gallardo, V. (2010) · Wiley eBooks · doi:10.1002/9781444327632.ch9 · Cited by 17
Opioid Regulation of Social Homeostasis: Connecting Loneliness to Addiction
Løseth, G. E., Eikemo, M., & Leknes, S. (2024) · Biological Psychiatry · doi:10.1016/j.biopsych.2024.11.011 · Cited by 16
“Following distressing social isolation, behaviors aimed at soliciting soothing social contact and proximity to safe others are typically reduced by opioid agonist drugs and increased by antagonists (57).”
Pain and rejection sensitivity in bipolar depression
Ehnvall, A., Mitchell, P. B., Hadži-Pavlović, D., Loo, C. K. A., Breakspear, M. J., Wright, A., Roberts, G. M. P., Frankland, A., & Corry, J. (2011) · Bipolar Disorders · doi:10.1111/j.1399-5618.2011.00892.x · Cited by 15
DSP-4, a noradrenergic neurotoxin, produces sex-specific effects on pairing and courtship behavior in zebra finches
Vahaba, D. M., Lacey, W. H., & Tomaszycki, M. L. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.056 · Cited by 15
Maternal responsivity and oxytocin in opioid‐dependent mothers
Daigle, K. M., Heller, N. A., Sulinski, E., Shim, J., Lindblad, W. J., Brown, M. S., Gosse, J. A., & Hayes, M. J. (2019) · Developmental Psychobiology · doi:10.1002/dev.21897 · Cited by 17
Biopsychological Aspects of Motivation
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Oxytocin and the social facilitation of placebo effects
Itskovich, E., Bowling, D. L., Garner, J. P., & Parker, K. J. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01515-9 · Cited by 17
“Like oxytocin and dopamine, opioids—particularly those that stimulate MORs—play an important role in social reward processing [84, 85].”
Background
Addiction and Autism: A Remarkable Comorbidity?
van Wijngaarden-Cremers, P. J. M. (2014) · Journal of Alcoholism and Drug Dependence · doi:10.4172/2329-6488.1000170 · Cited by 16
“Many of the behaviours she describes are reminiscent of preoccupations, trance like repetitive behaviours and obsessions as described in young children with autism [10].”
Background
The Value of Using an Evolutionary Framework for Gauging Children’s Well-Being
Narvaez, D. F., Panksepp, J., & Schore, A. N. (2013) · Cited by 14
Navigating Motivation: A Semantic and Subjective Atlas of 7 Motives
Chierchia, G., Przyrembel, M., Lesemann, F. H. P., Bosworth, S., Snower, D. J., & Singer, T. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.568064 · Cited by 16
Effect of parental touch on relieving acute procedural pain in neonates and parental anxiety (Petal): a multicentre, randomised controlled trial in the UK
Hauck, A., van der Vaart, M., Adams, E., Baxter, L., Bhatt, A., Crankshaw, D., Dhami, A., Fry, R. E., Freire, M. B. O., Hartley, C., et al. (2024) · The Lancet Child & Adolescent Health · doi:10.1016/s2352-4642(23)00340-1 · Cited by 14
“8,9,11 Skin-to-skin care includes multiple sensory components, such as parental smell 42 and hearing soothing voices.”
Prodynorphin and kappa opioid receptor mRNA expression in the brain relates to social status and behavior in male European starlings
Riters, L. V., Cordes, M. A., & Stevenson, S. A. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.11.050 · Cited by 14
Behavioral Roles of Oxytocin and Vasopressin
Benjamin, C. (2012) · InTech eBooks · doi:10.5772/50422 · Cited by 14
“OXT is an important mediator of maternal-infant bonding in humans [106].”
Background

Authors: Nelson, E. E., & Panksepp, J.
Affiliations: Indiana University Bloomington (US)
Bowling Green State University (US)
Corresponding author: Nelson, Eric E
ORCID: Nelson, Eric E
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 1998-05
Volume: 22
Issue: 3
Pages: 437-452
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/s0149-7634(97)00052-3
OpenAlex: W1981657115
Cited by: 688
References: 207
Citations by year: 2026: 9 · 2025: 12 · 2024: 20 · 2023: 38 · 2022: 18 · 2021: 29 · 2020: 15 · 2019: 29 · 2018: 32 · 2017: 29 · 2016: 45 · 2015: 29 · 2014: 31 · 2013: 47 · 2012: 29
FWCI: 3.25
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
Social Sciences › Psychology › Social Psychology › Attachment and Relationship Dynamics
Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Human-Animal Interaction Studies
Keywords: infant-mother attachment, social bonding, oxytocin, endogenous opioids, norepinephrine, vasopressin, catecholamines, maternal behavior, affiliative behavior, social memory, sexual behavior, neurobiology of attachment, rats
MeSH terms: Animals, Brain, Brain Chemistry, Humans, Mother-Child Relations, Norepinephrine, Oxytocin, Opioid Peptides, Rats

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Brain substrates of infant-mother attachment: contributions of opioids, oxytocin, and norepinephrine.

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