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

Nelson, Eric E; Panksepp, Jaak

doi:10.1016/s0149-7634(97)00052-3

Cited by 690Neuroendocrine regulation and behaviorAttachment and Relationship DynamicsHuman-Animal Interaction Studies

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

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

DOI 10.1016/s0149-7634(97)00052-3

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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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Relationship failure (break up or divorce) often results in prolonged periods of depression, permanent damage to life satisfaction, and long-lasting collateral harm to children.
“with outright relationship failure (in the form of break up or divorce) often resulting in prolonged periods of depression [20], permanent damage to life satisfaction [21], and long-lasting collateral harm to children when they are involved as well [22, 23].”
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These parallels provide strong evidence for a link between attachment and addiction.
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From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Nelson and Panksepp 1998
EO serve as mediator of social rewards, affiliation, motivation and attenuation of separation-induced pain and anxiety.
“Overall, EO serve as mediator of social rewards, affiliation, motivation and attenuation of separation-induced pain and anxiety (66)”
From Neuroendocrinology of Parental Response to Baby‐Cry (2011) · cites this paper as [66]

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Oxytocin mediates acquisition of maternally associated odor preferences in preweanling rat pups.
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Differential expression of Fos protein in the brain of female mice dependent on pup sensory cues and maternal experience.
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Behavioral response of infant rats to maternal odor
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Differential expression of Fos protein in the brain of female mice dependent on pup sensory cues and maternal experience.
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Independence of benzodiazepine and opiate action in the suppression of isolation distress in rat pups.
Carden, S. E., & Hofer, M. A. (1990) · Behavioral Neuroscience · doi:10.1037//0735-7044.104.1.160 · Cited by 89 · see citing works
Immunoreactive Beta-Endorphin Concentrations in Brain and Plasma during Pregnancy in Rats: Possible Modulation by Progesterone and Estradiol
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Prenatal expression of species-typical action patterns in the rat fetus (Rattus norvegicus).
Smotherman, W. P., & Robinson, S. R. (1987) · Journal of comparative psychology · doi:10.1037/0735-7036.101.2.190 · Cited by 87 · see citing works
Endogenous opioids: Do they modulate the rat pup's response to social isolation?
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Estrogen Alters Oxytocin mRNA Levels in the Preoptic Area
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Mother as shield: Differential effects of contact and nursing on pain responsivity in infant rats: Evidence for nonopioid mediation.
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Opioid peptides of the pituitary and hypothalamus: changes in pregnant and lactating rats
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Effect of Person
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Naltrexone and other potential new pharmacological treatments of autism
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Effects of parturition and maternal experience on noradrenaline and acetylcholine release in the olfactory bulb of sheep.
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Naltrexone in autistic children: a double-blind and placebo-controlled study.
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Independence of benzodiazepine and opiate action in the suppression of isolation distress in rat pups.
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Endogenous opioids: Do they modulate the rat pup's response to social isolation?
Winslow, J., & Insel, T. R. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.2.253 · Cited by 74 · see citing works
Changes in immunostaining for oxytocin in the forebrain of the female rat during late pregnancy, parturition and early lactation
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One-trial olfactory learning enhances olfactory bulb responses to an appetitive conditioned odor in 7-day-old rats
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Naltrexone in infantile autism.
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Rough and tumble play: A fundamental brain process.
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Olfactory learning and odor memory in the rat
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Kappa opioid mediation of fetal responses to milk.
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U50, 488 increases ultrasonic vocalizations in 3‐, 10‐, and 18‐day‐old rat pups in isolation and the home cage
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Independence of ultrasonic vocalization and thermogenic responses in infant rats.
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Opioid receptors: past, present and future
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Drinking-induced alterations in reward pathways: an in vivo autoradiographic analysis
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Rat pup isolation distress and the brain benzodiaze pine receptor
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Empathy: its ultimate and proximate bases
Preston, S. D., & de Waal, F. B. M. (2002) · Behavioral and Brain Sciences · doi:10.1017/s0140525x02000018 · Cited by 4,126 · see citing works
Does Rejection Hurt? An fMRI Study of Social Exclusion
Eisenberger, N. I., Lieberman, M. D., & Williams, K. D. (2003) · Science · doi:10.1126/science.1089134 · Cited by 3,849 · see citing works
The oxytocin receptor system: structure, function, and regulation
Gimpl, G., & Fahrenholz, F. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.629 · Cited by 3,089 · see citing works
Why Does Social Exclusion Hurt? The Relationship Between Social and Physical Pain.
MacDonald, G., & Leary, M. R. (2005) · Psychological Bulletin · doi:10.1037/0033-2909.131.2.202 · Cited by 1,712 · see citing works
“…“it is conceivable that brain circuits for separation distress represent an evolutionary elaboration of an endorphin-based pain network” (p. 219), and Nelson and Panksepp (1998) stated, “The pain components made stronger contributions to the subcomponents which aroused emotional distress during…”
Background
Motivation concepts in behavioral neuroscience
Berridge, K. C. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.02.004 · Cited by 1,302 · see citing works
“For example, thirst may be said to be caused by brain receptors for angiotensin II, and social motivations, such as attachment, have been suggested to be caused by activating brain peptide receptors for oxytocin and vasopressin [105,162].”
Background
Affective consciousness: core emotional feelings in animals and humans.
Panksepp, J. (2005) · Consciousness and Cognition · doi:10.1016/j.concog.2004.10.004 · Cited by 1,217 · see citing works
“We proceeded to demonstrate that social bonding from the infantÕs perspective was also oxytocin-facilitated in rats (Nelson & Panksepp, 1996, 1998).”
Background
Discriminative and affective touch: Sensing and feeling.
McGlone, F., Wessberg, J., & Olausson, H. (2014) · Neuron · doi:10.1016/j.neuron.2014.05.001 · Cited by 1,112 · see citing works
“neurochemical effects of prolonged social isolation (Nelson and Panksepp, 1998) and long-term changes in 5-HT function are observed in monkeys raised in a poor environment (Clarke et al.”
Background
Reward Processing by the Opioid System in the Brain
Le Merrer, J., Becker, J. A. J., Befort, K., & Kieffer, B. L. (2009) · Physiological Reviews · doi:10.1152/physrev.00005.2009 · Cited by 1,013 · see citing works
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
“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).”
BackgroundInfluential
The social role of touch in humans and primates: Behavioural function and neurobiological mechanisms
Dunbar, R. I. M. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.07.001 · Cited by 798 · see citing works
Neurobiological Mechanisms of the Placebo Effect
Benedetti, F., Mayberg, H. S., Wager, T. D., Stohler, C. S., & Zubieta, J.-K. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3458-05.2005 · Cited by 780 · see citing works
“…response to novel and emotionally salient stimuli (Watkins and Mayer, 1982; Akil et al., 1984; Kalin et al., 1988; Rubinstein et al., 1996; Sora et al., 1997; Nelson and Panksepp, 1998; Smith et al., 1998; Filliol et al., 2000; Drolet et al., 2001; Zubieta et al., 2001, 2003a; Moles et al., 2004).”
Background
Placebo Effects Mediated by Endogenous Opioid Activity on μ-Opioid Receptors
Zubieta, J.-K., Bueller, J. A., Jackson, L. R., Scott, D. J., Xu, Y., Koeppe, R. A., Nichols, T. E., & Stohler, C. S. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0439-05.2005 · Cited by 779 · see citing works
“…has also accumulated as to the involvement of this neurotransmitter system in the adaptation and response to novel and emotionally salient stimuli in both animal models and humans (Kalin et al., 1988; Nelson and Panksepp, 1998; Filliol et al., 2000; Zubieta et al., 2003b; Moles et al., 2004).”
Background
Oxytocin and social affiliation in humans
Feldman, R. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.008 · Cited by 767 · see citing works
“…postpartum behavior, including gaze, positive affect, " motherese " vocalizations, and affectionate touch, suggesting that OT across gestation functions to prime mothers for the expression of maternal behavior, consistent with the effects described in other mammals (Nelson and Panksepp, 1998).”
Result
Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: a review of animal models and human studies across development
Hostinar, C. E., Sullivan, R. M., & Gunnar, M. R. (2014) · Psychological Bulletin · doi:10.1037/a0032671 · Cited by 739 · see citing works
“…release of OT and its role in controlling behavior are diverse, although there are some similarities across species, such as lactation’s milk ejection reflex, affiliation, pain reduction, and stress reduction (Carter, 2003; Nelson & Panksepp, 1998; Neumann, 2008; Onaka, 2004; Young & Zingg, 2009).”
Background
An integrated theory of sexual offending
Ward, T., & Beech, A. (2006) · Aggression and Violent Behavior · doi:10.1016/j.avb.2005.05.002 · Cited by 682 · see citing works
Cultural group selection plays an essential role in explaining human cooperation: a sketch of the evidence.
Richerson, P., Baldini, R., Bell, A. V., Demps, K., Frost, K., Hillis, V., Mathew, S., Newton, E. K., Naar, N., Newson, L., et al. (2016) · Behavioral and Brain Sciences · doi:10.1017/s0140525x1400106x · Cited by 639 · see citing works
Sudarshan Kriya Yogic Breathing in the Treatment of Stress, Anxiety, and Depression: Part I—Neurophysiologic Model
Brown, R. P., & Gerbarg, P. L. (2005) · The Journal of Alternative and Complementary Medicine · doi:10.1089/acm.2005.11.189 · Cited by 655 · see citing works
“Many brain areas with oxytocin receptors are involved in behavior, memory, sensory processing, eating, satiety (Nelson and Panksepp, 1998), and reproduction.”
Influential
Social buffering: relief from stress and anxiety
Kikusui, T., Winslow, J. T., & Mori, Y. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1941 · Cited by 635 · see citing works
Facial expression of pain: An evolutionary account
Williams, A. C. D. C. (2002) · Behavioral and Brain Sciences · doi:10.1017/s0140525x02000080 · Cited by 585 · see citing works
“Social Support: A Review”
Taylor, S. E. (2012) · The Oxford Handbook of Health Psychology · doi:10.1093/oxfordhb/9780195342819.013.0009 · Cited by 993 · see citing works
“…may be roles for other hormones both in promoting social support initially and in regulating its biological eff ects, which include vasopressin, norepinephrine, serotonin, prolactin, and endogenous opioid peptides (Nelson & Panksepp, 1998 ; Taylor et al., 2002 ). why is social support beneficial?”
Background
The dynamic effects of nicotine on the developing brain
Dwyer, J. B., McQuown, S. C., & Leslie, F. M. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.02.003 · Cited by 559 · see citing works
“Such findings suggest that nAChRs may additionally regulate the early maturation of these neuronal pathways which play pivotal roles in regulating arousal, maternal bonding, and autonomic function during the perinatal period (Nelson and Panksepp, 1998; Itoi, 2008).”
Extending the ‘Five Domains’ model for animal welfare assessment to incorporate positive welfare states
Mellor, D., & Beausoleil, N. (2015) · Animal Welfare · doi:10.7120/09627286.24.3.241 · Cited by 627 · see citing works
The basic emotional circuits of mammalian brains: Do animals have affective lives?
Panksepp, J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.08.003 · Cited by 562 · see citing works
What does sexual orientation orient? A biobehavioral model distinguishing romantic love and sexual desire.
Diamond, L. M. (2003) · Psychological Review · doi:10.1037/0033-295x.110.1.173 · Cited by 547 · see citing works
Cellular Mechanisms of Social Attachment
Young, L. J., Lim, M. M., Gingrich, B., & Insel, T. R. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1691 · Cited by 523 · see citing works
Alone but feeling no pain: Effects of social exclusion on physical pain tolerance and pain threshold, affective forecasting, and interpersonal empathy.
DeWall, C. N., & Baumeister, R. F. (2006) · Journal of Personality and Social Psychology · doi:10.1037/0022-3514.91.1.1 · Cited by 529 · see citing works
“…cingulate cortex (ACC) functions as a neural alarm system to warn people that factors in their environment threaten their goals (Eisenberger, Lieberman, & Williams, 2003; Eisenberger & Lieberman, 2004; Nelson & Panksepp, 1998; Bush, Luu, & Posner, 2000; Kimbrell, George, Parekh, et al., 1999).”
Background
Attachment and the regulation of the right brain
Schore, A. N. (2000) · Attachment & Human Development · doi:10.1080/146167300361309 · Cited by 527 · see citing works
“Imprinting, the learning process it accesses, is described by Petrovich and Gewirtz (1985) as synchrony between sequential infant maternal stimuli and behavior (see Schore, 1994 and Nelson & Panksepp, 1998 for models of the neurochemistry of attachment).”
Background
Emotional sounds and the brain: the neuro-affective foundations of musical appreciation
Panksepp, J., & Bernatzky, G. (2002) · Behavioural Processes · doi:10.1016/s0376-6357(02)00080-3 · Cited by 498 · see citing works
“From this concordance, we would hypothesize that music may arouse that neuropeptide system, one of the best established social-emotional sys- tems of the vertebrate brain (Carter, 1998; Insel, 1997; Nelson and Panksepp, 1998).”
Background
Mothers' neural activation in response to pictures of their children and other children
Leibenluft, E., Gobbini, M. I., Harrison, T., & Haxby, J. V. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.05.017 · Cited by 493 · see citing works
The neuroendocrine basis of social recognition
Ferguson, J. N., Young, L. J., & Insel, T. R. (2002) · Frontiers in Neuroendocrinology · doi:10.1006/frne.2002.0229 · Cited by 494 · see citing works
Maternal and paternal plasma, salivary, and urinary oxytocin and parent–infant synchrony: considering stress and affiliation components of human bonding
Feldman, R., Gordon, I., & Zagoory‐Sharon, O. (2011) · Developmental Science · doi:10.1111/j.1467-7687.2010.01021.x · Cited by 486 · see citing works
“Nelson and Panksepp (1998) suggest that hormonal changes in the mother across gestation, particularly in OT and prolactin, prime the initiation of maternal behavior following birth and provide the basis for the development of contingent parenting.”
Ultrasonic vocalizations: A tool for behavioural phenotyping of mouse models of neurodevelopmental disorders
Scattoni, M. L., Crawley, J. N., & Ricceri, L. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.08.003 · Cited by 473 · see citing works
“Opioid modulation of isolation-induced USV in neonatal rats has been reported by several authors (Carden et al., 1991; Kehoe and Blass, 1986; Nelson and Panksepp, 1998).”
Method
The emergence of social cognitive neuroscience.
Ochsner, K. N., & Lieberman, M. D. (2001) · American Psychologist · doi:10.1037/0003-066x.56.9.717 · Cited by 536 · see citing works
Social re-orientation and brain development: An expanded and updated view
Nelson, E. E., Jarcho, J. M., & Guyer, A. E. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.12.008 · Cited by 447 · see citing works
“…brain nd behavioral organization are considered particularly amenable o specific types of information during specific developmental indows (Nelson and Panksepp, 1998; Bell et al., 2010; Meaney, 010; Nelson and Guyer, 2011; Crone and Dahl, 2012; Takesian nd Hensch, 2013; Nelson et al.,…”
Deficit in Attachment Behavior in Mice Lacking the µ-Opioid Receptor Gene
Moles, A., Kieffer, B. L., & D'Amato, F. R. (2004) · Science · doi:10.1126/science.1095943 · Cited by 449 · see citing works
Understanding weaning distress
Weary, D. M., Jasper, J., & Hötzel, M. J. (2007) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2007.03.025 · Cited by 446 · see citing works
“Several neurochemicals are associated with attachment, but the best evidence is available for four substances: oxytocin, norepinephrine, vasopressin and endogenous opioids (Nelson and Panksepp, 1998).”
BackgroundInfluential
Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: A review of single administration studies
Bos, P. A., Panksepp, J., Bluthé, R.-M., & Honk, J. V. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2011.01.002 · Cited by 429 · see citing works
Coregulation, Dysregulation, Self-Regulation: An Integrative Analysis and Empirical Agenda for Understanding Adult Attachment, Separation, Loss, and Recovery
Sbarra, D. A., & Hazan, C. (2008) · Personality and Social Psychology Review · doi:10.1177/1088868308315702 · Cited by 427 · see citing works
“Furthermore, the opioid theory of social affiliation (Depue & Morrone-Strupinsky, 2005; Nelson & Panksepp, 1998; Panksepp et al. 1997) posits that the rewarding effects of social contact facilitate learning and funnel attention toward social stimuli and may produce social “addiction” or attachment.”
Influential
Mentalizing homeostasis: the social origins of interoceptive inference
Fotopoulou, A., & Tsakiris, M. (2017) · Neuropsychoanalysis · doi:10.1080/15294145.2017.1294031 · Cited by 428 · see citing works
Autism, oxytocin and interoception
Quattrocki, E., & Friston, K. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.09.012 · Cited by 393 · see citing works
Operational Details of the Five Domains Model and Its Key Applications to the Assessment and Management of Animal Welfare
Mellor, D. J. (2017) · Animals · doi:10.3390/ani7080060 · Cited by 419 · see citing works
Topography of social touching depends on emotional bonds between humans
Suvilehto, J. T., Glerean, E., Dunbar, R. I. M., Hari, R., & Nummenmaa, L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1519231112 · Cited by 385 · see citing works
How we know our own minds: The relationship between mindreading and metacognition
Carruthers, P. (2009) · Behavioral and Brain Sciences · doi:10.1017/s0140525x09000545 · Cited by 610 · see citing works
“Nichols and Stich (2003) and Goldman (2006) each maintain, in contrast, that introspection is intact in autism, with difficulties in otherunderstanding arising from difficulties in supposing or empathizing.”
BackgroundInfluential
Plasma oxytocin concentration during pregnancy is associated with development of postpartum depression
Skrundz, M., Bolten, M., Nast, I., Hellhammer, D. H., & Meinlschmidt, G. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.74 · Cited by 349 · see citing works
“Furthermore, maternal OXT functioning influences reciprocal affective behaviors between mother and offspring in mammalian species (Nelson and Panksepp, 1998).”
Background
What is Basic about Basic Emotions? Lasting Lessons from Affective Neuroscience
Panksepp, J., & Watt, D. F. (2011) · Emotion Review · doi:10.1177/1754073911410741 · Cited by 340 · see citing works
Annotation: The `effects' of parenting reconsidered: findings, challenges, and applications
O’Connor, T. G. (2002) · Journal of Child Psychology and Psychiatry · doi:10.1111/1469-7610.00046 · Cited by 328 · see citing works
Music, empathy and cultural understanding
Clarke, E., DeNora, T., & Vuoskoski, J. K. (2015) · Physics of Life Reviews · doi:10.1016/j.plrev.2015.09.001 · Cited by 323 · see citing works
Neurologizing the Psychology of Affects: How Appraisal-Based Constructivism and Basic Emotion Theory Can Coexist
Panksepp, J. (2007) · Perspectives on Psychological Science · doi:10.1111/j.1745-6916.2007.00045.x · Cited by 314 · see citing works
“…neurochemistries that could powerfully and specifically alleviate the pain of separation distress (namely opioids, oxytocin, and prolactin) could serve as affective substrates for the construction of social bonds andmore subtle prosocial feelings (Nelson & Panksepp, 1998; Panksepp, 1981a, 1998a).”
Background
The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction
Burkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307 · see citing works
“These parallels provide strong evidence for a link between attachment and addiction (MacLean 1990; Nelson and Panksepp 1998; Insel 2003; Fisher 2004; Reynaud et al. 2010).”
Affectionate Touch to Promote Relational, Psychological, and Physical Well-Being in Adulthood: A Theoretical Model and Review of the Research
Jakubiak, B. K., & Feeney, B. C. (2016) · Personality and Social Psychology Review · doi:10.1177/1088868316650307 · Cited by 302 · see citing works
“…including social stress (e.g., Onaka, 2004), it has been christened the “cuddle hormone” because hugs, kisses, and other affectionate types of touch increase the release of oxytocin (e.g., Insel, 1992, 1997; Nelson & Panksepp, 1998; Uvnäs-Moberg, 1997; UvnäsMoberg, Arn, & Magnusson, 2005).”
Background
Toward a cross-species understanding of empathy
Panksepp, J., & Panksepp, J. B. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.04.009 · Cited by 296 · see citing works
Oxytocin, vasopressin and pair bonding: implications for autism
Hammock, E. A. D., & Young, L. J. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1939 · Cited by 289 · see citing works
“Additionally, the data do not explainwhy some species display bonding behaviour and others do not, since it is believed that all mammals have genes encoding oxytocin and the OTR, as both are necessary for lactation (Nishimori et al. 1996).”
Background
Friends with benefits: Social support and its relevance for farm animal welfare
Rault, J. (2011) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2011.10.002 · Cited by 278 · see citing works
The animal and human neuroendocrinology of social cognition, motivation and behavior
McCall, C., & Singer, T. (2012) · Nature Neuroscience · doi:10.1038/nn.3084 · Cited by 273 · see citing works
Analysis of taste mixtures by adults and children
Oram, N., Laing, D. G., Freeman, M., & Hutchinson, I. (2000) · Developmental Psychobiology · doi:10.1002/1098-2302(2001)38:1 · Cited by 30 · see citing works
Rowers' high: behavioural synchrony is correlated with elevated pain thresholds
Cohen, E. E. A., Ejsmond-Frey, R., Knight, N., & Dunbar, R. I. M. (2010) · Biology Letters · doi:10.1098/rsbl.2009.0670 · Cited by 261 · see citing works
Skin‐to‐skin contact the first hour after birth, underlying implications and clinical practice
Widström, A., Brimdyr, K., Svensson, K., Cadwell, K., & Nissen, E. (2019) · Acta Paediatrica · doi:10.1111/apa.14754 · Cited by 264 · see citing works
“This is an example of the early symbiotic biological relationship between the dyad (24,25).”
Background
Towards a neuroscience of empathy: Ontogeny, phylogeny, brain mechanisms, context and psychopathology
Gonzalez-Liencres, C., Shamay‐Tsoory, S., & Brüne, M. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.05.001 · Cited by 264 · see citing works
TARGET ARTICLE: Selective Investment Theory: Recasting the Functional Significance of Close Relationships
Brown, S. L., & Brown, R. M. (2006) · Psychological Inquiry · doi:10.1207/s15327965pli1701_01 · Cited by 250 · see citing works
“Nevertheless, conservation of neural structure and function across mammals suggests that bond-related neural phenomena may characterize more than the few mammalian species that have been studied (Nelson & Panksepp, 1998).”
Emotional endophenotypes in evolutionary psychiatry
Panksepp, J. (2006) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2006.01.004 · Cited by 248 · see citing works
“…of distress (e.g., Corticotrophin Releasing Factor) and those that can powerfully alleviate distress (e.g., brain opioids, oxytocin, and prolactin) figure heavily in the genesis of social attachments (as well as sexuality and nurturance) and may ameliorate depression (Nelson and Panksepp, 1998).”
Background
Performance of Music Elevates Pain Threshold and Positive Affect: Implications for the Evolutionary Function of Music
Dunbar, R. I. M., Kaskatis, K., MacDonald, I., & Barra, V. (2012) · Evolutionary Psychology · doi:10.1177/147470491201000403 · Cited by 243 · see citing works
“In primates, endorphin release is triggered by grooming (Keverne et al., 1989) and appears to be deeply involved in the processes involved in social bonding at the dyadic level (Nelson and Panksepp, 1998; Dunbar, 2010; Machin and Dunbar, 2011).”
Background
Evaluating the rewarding nature of social interactions in laboratory animals
Trezza, V., Campolongo, P., & Vanderschuren, L. J. M. J. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.05.007 · Cited by 258 · see citing works
“Second, this modulation occurs in brain regions involved in positive emotions and motivation (for neuroanatomical and pharmacological analyses of maternal behavior, social play and sexual behavior, see Everitt, 1990; Everitt and Stacey, 1987; Fleming et al., 1999; Grimm and Bridges, 1983; Kristal, 2009; Nelson and Pan…”
Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement
Weisman, O., Zagoory-Sharon, O., & Feldman, R. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.06.011 · Cited by 240 · see citing works
“Repeated-measure analysis of variance (ANOVA) for the four ather (log)OT assessments with condition and infant gender as the etween-subject factors revealed different pattern in the two conitions, F (1,33) 189.”
Influential
Neural circuitry underlying affective response to peer feedback in adolescence
Guyer, A. E., Choate, V. R., Pine, D. S., & Nelson, E. E. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsr043 · Cited by 236 · see citing works
Oxytocin and human social behavior.
Campbell, A. (2010) · Personality and Social Psychology Review · doi:10.1177/1088868310363594 · Cited by 232 · see citing works
It's more than sex: exploring the dyadic nature of sleep and implications for health
Troxel, W. M. (2010) · Psychosomatic Medicine · doi:10.1097/psy.0b013e3181de7ff8 · Cited by 225 · see citing works
Keep Calm and Cuddle on: Social Touch as a Stress Buffer
Morrison, I. (2016) · Adaptive Human Behavior and Physiology · doi:10.1007/s40750-016-0052-x · Cited by 256 · see citing works
What makes a cry a cry? A review of infant distress vocalizations
Lingle, S., Wyman, M. T., Kotrba, R., Teichroeb, L. J., & Romanow, C. A. (2012) · Current Zoology · doi:10.1093/czoolo/58.5.698 · Cited by 221 · see citing works
“…– which along with opioids inhibit the separation calls of infants – in maternal care suggests that social and maternal comfort are produced by the same brain chemistries that help to mediate sexual behaviour (Nelson and Panksepp, 1998; Panksepp, 1998; Panksepp, 2005; Panksepp and Biven, 2012).”
Background
Direct and indirect effects of breast milk on the neurobehavioral and cognitive development of premature infants
Feldman, R., & Eidelman, A. I. (2003) · Developmental Psychobiology · doi:10.1002/dev.10126 · Cited by 210 · see citing works
“Research in animals has pointed to the role of oxytocin and prolactin in the initiation of maternal behavior, such as affiliative touch, grooming, and proximity seeking (Grattan et al., 2001; Insel, 1997; Nelson & Panksepp, 1998).”
Background
Depression: An Evolutionarily Conserved Mechanism to Terminate Separation Distress? A Review of Aminergic, Peptidergic, and Neural Network Perspectives
Watt, D. F., & Panksepp, J. (2009) · Neuropsychoanalysis · doi:10.1080/15294145.2009.10773593 · Cited by 207 · see citing works
“Oxytocin becomes a major candidate as a potential alleviator of depression in its role of being a major modulator of separation distress (Panksepp, 1998) and, next to opiates, the best candidate for a key mediator of social attachments (Nelson & Panksepp, 1998).”
Background
Minimising the stress of weaning of beef calves: a review
Enríquez-Hidalgo, D., Hötzel, M. J., & Ungerfeld, R. (2011) · Acta veterinaria Scandinavica · doi:10.1186/1751-0147-53-28 · Cited by 206 · see citing works
“In mammals there is evidence of direct and indirect participation of hormones and neurochemicals, such as estradiol, oxytocin, prolactin, vasopressin, and several endogenous opioids in the initiation and maintenance of the motheryoung bond [45].”
It still hurts: altered endogenous opioid activity in the brain during social rejection and acceptance in major depressive disorder
Hsu, D. T., Sanford, B. J., Meyers, K. K., Love, T. M., Hazlett, K. E., Walker, S. J., Mickey, B. J., Koeppe, R. A., Langenecker, S. A., & Zubieta, J.-K. (2015) · Molecular Psychiatry · doi:10.1038/mp.2014.185 · Cited by 205 · see citing works
Rewards of beauty: the opioid system mediates social motivation in humans
Chelnokova, O., Laeng, B., Eikemo, M., Riegels, J., Løseth, G. E., Maurud, H., Willoch, F., & Leknes, S. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.1 · Cited by 204 · see citing works
The Neurobiology Shaping Affective Touch: Expectation, Motivation, and Meaning in the Multisensory Context
Ellingsen, D., Leknes, S., Løseth, G. E., Wessberg, J., & Olausson, H. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01986 · Cited by 201 · see citing works
“Thus, they are considerably less distressed by the social separation that is inherent in the majority of these studies (Nelson and Panksepp, 1998; van den Berg et al., 1999).”
Background
Synchrony as an Adaptive Mechanism for Large‐Scale Human Social Bonding
Launay, J., Tarr, B., & Dunbar, R. (2016) · Ethology · doi:10.1111/eth.12528 · Cited by 202 · see citing works
“In summary, while evidence is primarily correlational, BOTSA illustrates that for humans both social attachment and the administration of exogenous opiates have similar neurophysiological effects (Nelson & Panksepp 1998; Nummenmaa et al. 2016).”
Altered central somatosensory processing in chronic pain patients with “hysterical” anesthesia
Mailis, A., Giannoylis, I., Downar, J. H., Kwan, C. L., Mikulis, D. J., Crawley, A. P., Nicholson, K., & Davis, K. D. (2003) · Neurology · doi:10.1212/wnl.60.9.1501 · Cited by 201 · see citing works
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
“n addition, the neuropeptides vasopressin (AVP) and oxytocin OT) have attracted a lot of interest, due to the evidence that they re involved in regulating social attachment behavior in rodents nd non-human primates [39,41,42,49,70,92,120,121].”
Background
Social Exclusion and Pain Sensitivity
Bernstein, M. J., & Claypool, H. M. (2011) · Personality and Social Psychology Bulletin · doi:10.1177/0146167211422449 · Cited by 197 · see citing works
“…(e.g., Eisenberger & Lieberman, 2005) and social pain theory (MacDonald, Kingsbury, & Shaw, 2005; MacDonald & Leary, 2005) suggest that a system capable of detecting and responding to social pain “piggybacked” onto the preexisting physicalpain system during evolution (Nelson & Panksepp, 1998).”
Background
Triune ethics: The neurobiological roots of our multiple moralities
Narvaez, D. F. (2007) · New Ideas in Psychology · doi:10.1016/j.newideapsych.2007.07.008 · Cited by 195 · see citing works
“Processes of reward and memory established in early childhood enhanced the capacity to affiliate with others (Depue & Morrone-Strupinsky, 2005; Nelson & Panksepp, 1998).”
Background
Maternal Stress Induces Epigenetic Signatures of Psychiatric and Neurological Diseases in the Offspring
Zucchi, F. C. R., Yao, Y., Ward, I. D., Ilnytskyy, Y., Olson, D. M., Benzies, K., Kovalchuk, I., Kovalchuk, O., & Metz, G. A. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056967 · Cited by 193 · see citing works
“If antepartum activities are somewhat predictive of postpartum maternal care [55,26,3], even a moderate behavioural change in maternal behaviour may potentially have significant consequences for offspring development.”
Background
Connecting prosocial behavior to improved physical health: Contributions from the neurobiology of parenting
Brown, S. L., & Brown, R. M. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.004 · Cited by 190 · see citing works
Neuroevolutionary sources of laughter and social joy: Modeling primal human laughter in laboratory rats
Panksepp, J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.02.015 · Cited by 184 · see citing works
Developmental Perspectives on Oxytocin and Vasopressin
Hammock, E. A. D. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.120 · Cited by 177 · see citing works
“Further, Brattleboro neonates show disturbances in early odor orienting (Nelson and Panksepp, 1998) and dysregulation of the HPA axis in response to maternal separation as neonates (Fodor and Zelena, 2014).”
Background
Infant bonding and attachment to the caregiver: insights from basic and clinical science
Sullivan, R., Perry, R., Sloan, A., Kleinhaus, K., & Burtchen, N. (2011) · Clinics in Perinatology · doi:10.1016/j.clp.2011.08.011 · Cited by 181 · see citing works
The soothing function of touch: affective touch reduces feelings of social exclusion
Mohr, M. V., Kirsch, L. P., & Fotopoulou, A. (2017) · Scientific Reports · doi:10.1038/s41598-017-13355-7 · Cited by 178 · see citing works
Animal emotions, behaviour and the promotion of positive welfare states
Mellor, D. J. (2011) · New Zealand Veterinary Journal · doi:10.1080/00480169.2011.619047 · Cited by 181 · see citing works
“The salient behaviours expressing separation distress include specific vocalisations, and the affiliative behaviours include rough and tumble play, sexual and parental behaviours, and various forms of physical contact including allogrooming (Nelson and Panksepp 1998).”
BackgroundInfluential
Truth, lies, and intimacy: An attachment perspective
Cassidy, J. A. (2001) · Attachment & Human Development · doi:10.1080/14616730110058999 · Cited by 182 · see citing works
“Changes in oxytocin receptors may be related to induction of maternal behavior: administration of oxytocin to virgin female rats results in a sudden surge of maternal behavior; blocking oxytocin in new rat mothers interferes with maternal behavior (Nelson & Panksepp, 1998).”
Making room for oxytocin in understanding depression
McQuaid, R. J., McInnis, O. A., Abizaid, A. B., & Anisman, H. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.07.005 · Cited by 172 · see citing works
The role of emotion in pain modulation.
Rhudy, J. L., & Meagher, M. W. (2001) · Current Opinion in Psychiatry · doi:10.1097/00001504-200105000-00012 · Cited by 170 · see citing works
Neurobiology of culturally common maternal responses to infant cry
Bornstein, M. H., Putnick, D. L., Rigo, P., Esposito, G., Swain, J. E., Suwalsky, J. T. D., Su, X., Du, X., Zhang, K., Cote, L. R., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1712022114 · Cited by 168 · see citing works
“That is, infant cries and caregiver responses to them constitute an integrated dyadic system that encompasses the infant production of cries as well as the adult anatomy (9–12), physiology (5, 13), and perception, processing, and response apparatus to cries (2, 4, 5, 14–17).”
Background
Association between parental depressive symptoms and impaired bonding with the infant
Kerstis, B., Aarts, C., Tillman, C., Persson, H., Engström, G., Edlund, B., Öhrvik, J., Sylvén, S., & Skalkidou, A. (2016) · Archives of Women's Mental Health · doi:10.1007/s00737-015-0522-3 · Cited by 165 · see citing works
“2003; Field 1995), which stimulates oxytocin and in turn may have a positive effect on attachment (Nelson and Panksepp 1998).”
Background
Birth practices: Maternal‐neonate separation as a source of toxic stress
Bergman, N. (2019) · Birth Defects Research · doi:10.1002/bdr2.1530 · Cited by 165 · see citing works
“In this period immediately after birth, the emotional brain and the social brain are being connected (Nelson & Panksepp, 1998).”
Background
If music is the food of love, what about survival and reproductive success?
Dissanayake, E. (2008) · Musicae Scientiae · doi:10.1177/1029864908012001081 · Cited by 161 · see citing works
“…oxytocin in both maternal behavior and in adult pairbonding, in humans as well as in other animals (see, e.g., Carter, 1998; Insel, 1997; Nelson & Panksepp, 1998; Üvnas-Moberg, 1998), lends additional credence to the evolutionary relationship suggested here between mother-infant…”
Background
Specific reduction in cortisol stress reactivity after social but not attention-based mental training
Engert, V., Kok, B. E., Papassotiriou, I., Chrousos, G. P., & Singer, T. (2017) · Science Advances · doi:10.1126/sciadv.1700495 · Cited by 151 · see citing works
“From a mechanistic perspective, it can be hypothesized on the basis of previous research that the Affect Module stimulates positive affect systems (37) linked to care and affiliation and modulated by oxytocin and opiates (38, 39).”
Background
Enhancing animal welfare by creating opportunities for positive affective engagement
Mellor, D. J. (2014) · New Zealand Veterinary Journal · doi:10.1080/00480169.2014.926799 · Cited by 153 · see citing works
“Indeed, such studies have clarified some neurological foundations of behaviourally linked positive affects, and this is specifically the case for some aspects of exploratory and feeding (Ikemoto and Panksepp 1999; Berridge and Robinson 2003; Panksepp and Zellner 2004), bonding and bond affirming (Nelson and Panksepp 1…”
Background
Panic, suffocation false alarms, separation anxiety and endogenous opioids
Preter, M., & Klein, D. F. (2007) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2007.07.029 · Cited by 152 · see citing works
“This evolutionary, neurobiologic attachment theory has received much empirical support (Nelson and Panksepp, 1998).”
Background
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
“Based on similarities between opiate addiction and social attachment, Panksepp and colleagues (Panksepp et al., 1980; Nelson and Panksepp, 1998) have hypothesized that endogenous opioids mediate the rewarding properties of social affiliation.”
Background
Interface of physical and emotional stress regulation through the endogenous opioid system and μ-opioid receptors
Ribeiro, S. C. M., Kennedy, S. E., Smith, Y. R., Stohler, C. S., & Zubieta, J. (2005) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2005.08.011 · Cited by 147 · see citing works
“…functions (Smith et al., 1998; Drolet et al., 2001), and the adaptation and response to novel and emotionally salient stimuli in animal models (Kalin et al., 1988; Nelson and Panksepp, 1998; Filliol et al., 2000b; Moles et al., 2004) and more recently in humans (Zubieta et al., 2003b).”
Background
Oxytocin׳s role in anxiety: A critical appraisal
MacDonald, K., & Feifel, D. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.025 · Cited by 139 · see citing works
Social touch deprivation during COVID-19: effects on psychological wellbeing and craving interpersonal touch
Mohr, M. V., Kirsch, L. P., & Fotopoulou, A. (2021) · Royal Society Open Science · doi:10.1098/rsos.210287 · Cited by 146 · see citing works

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: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Social Sciences › Psychology › Social Psychology › Attachment and Relationship Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › 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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