Testosterone administration modulates neural responses to crying infants in young females
Abstract
Parental responsiveness to infant vocalizations is an essential mechanism to ensure parental care, and its importance is reflected in a specific neural substrate, the thalamocingulate circuit, which evolved through mammalian evolution subserving this responsiveness. Recent studies using functional Magnetic Resonance Imaging (fMRI) provide compelling evidence for a comparable mechanism in humans by showing thalamocingulate responses to infant crying. Furthermore, possibly acting on this common neural substrate, steroid hormones such as estradiol and testosterone, seem to mediate parental behavior both in humans and other animals. Estradiol unmistakably increases parental care, while data for testosterone are less unequivocal. In humans and several other animals, testosterone levels decrease both in mothers and fathers during parenthood. However, exogenous testosterone in mice seems to increase parenting, and infant crying leads to heightened testosterone levels in human males. Not only is the way in which testosterone is implicated in parental responsiveness unresolved, but the underlying mechanisms are fully unknown. Accordingly, using fMRI, we measured neural responses of 16 young women who were listening to crying infants in a double blind, placebo-controlled, counterbalanced, testosterone administration experiment. Crucially, heightened activation in the testosterone condition compared to placebo was shown in the thalamocingulate region, insula, and the cerebellum in response to crying. Our results by controlled hormonal manipulation confirm a role of the thalamocingulate circuit in infant cry perception. Furthermore, the data also suggest that exogenous testosterone, by itself or by way of its metabolite estradiol, in our group of young women acted on this thalamocinculate circuit to, provisionally, upregulate parental care.
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Testosterone treatment modulated neural responses to crying infants in women.
“to crying infants in women [7]”
From Effects of sex and gonadectomy on social investigation and social recognition in mice (2015) · cites this paper as [7]
Acute testosterone administration increases insula response to infant cries in nulliparous healthy women (Bos et al., 2010).
“Similarly, acute testosterone was also found to increase insula response to infant cries (Bos et al., 2010) in nulliparous healthy women.”
From Approaching the biology of human parental attachment: Brain imaging, oxytocin and coordinated assessments of mothers and fathers (2014) · cites this paper as Bos et al., 2010
Cites
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., & Joliot, M. (2002) · NeuroImage · doi:10.1006/nimg.2001.0978 · Cited by 16,319 · see citing works
How do you feel — now? The anterior insula and human awareness
(Bud) Craig, A. D. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2555 · Cited by 6,657 · cited 1× · see citing works
“, 2008) adding to the growing view of the insular cortex as an emotion processing structure (Wager and Barrett, 2004; Craig, 2009).”
BackgroundCerebellum and nonmotor function
Strick, P. L., Dum, R. P., & Fiez, J. A. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125606 · Cited by 1,777 · see citing works
Circuitry and functional aspects of the insular lobe in primates including humans
AUGUSTINE, J. (1996) · Brain Research Reviews · doi:10.1016/s0165-0173(96)00011-2 · Cited by 1,776 · see citing works
The neural correlates of maternal and romantic love
Bartels, A., & Zeki, S. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.11.003 · Cited by 1,448 · 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
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
The neurobiology of attachment
Insel, T. R., & Young, L. J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35053579 · Cited by 1,173 · see citing works
Cerebrocerebellar communication systems.
Allen, G. I., & Tsukahara, N. (1974) · Physiological Reviews · doi:10.1152/physrev.1974.54.4.957 · Cited by 1,066 · see citing works
The triune brain in evolution: Role in paleocerebral functions
Legg, C. R. (1990) · Biological Psychology · doi:10.1016/0301-0511(90)90083-9 · Cited by 981 · see citing works
(1990) · Medical Entomology and Zoology · Cited by 919 · see citing works
Nelson, E. E., & Panksepp, J. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(97)00052-3 · Cited by 688 · cited 2× · see citing works
“Especially in rodents, parental care and bonding is strongly under hormonal control (Nelson and Panksepp, 1998; Insel and Young, 2001; Curley and Keverne, 2005).”
BackgroundForebrain emotional asymmetry: a neuroanatomical basis?
Craig, A. D. (. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2005.10.005 · Cited by 626 · see citing works
Hemispheric lateralization of functions related to emotion
Silberman, E. K., & Weingartner, H. (1986) · Brain and Cognition · doi:10.1016/0278-2626(86)90035-7 · Cited by 611 · see citing works
Hormonal correlates of paternal responsiveness in new and expectant fathers
Storey, A. (2000) · Evolution and Human Behavior · doi:10.1016/s1090-5138(99)00042-2 · Cited by 536 · cited 1× · see citing works
“In most male and female mammals including humans, testosterone levels decrease during parenting (Storey et al., 2000; WynneEdwards and Reburn, 2000; Fleming et al., 2002; Gray et al., 2007), however, exogenous testosterone in male mice seems to potentiate parental behavior, presumably by conversion to estradiol (Train…”
BackgroundEndogenous 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
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
Brain evolution relating to family, play, and the separation call.
Maclean, P. (1985) · Archives of General Psychiatry · doi:10.1001/archpsyc.1985.01790270095011 · Cited by 406 · see citing works
Testosterone and prolactin are associated with emotional responses to infant cries in new fathers
Fleming, A. S., Corter, C., Stallings, J., & Steiner, M. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2002.1840 · Cited by 401 · see citing works
Oxytocin, motherhood and bonding
Kendrick, K. M. (2000) · Experimental Physiology · doi:10.1111/j.1469-445x.2000.tb00014.x · Cited by 378 · see citing works
Seifritz, E., Esposito, F., Neuhoff, J. G., Lüthi, A., Mustovic, H., Dammann, G., von Bardeleben, U., Radue, E. W., Cirillo, S., Tedeschi, G., et al. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00697-8 · Cited by 373 · see citing works
A potential role for thalamocingulate circuitry in human maternal behavior
Lorberbaum, J. P., Newman, J. D., Horwitz, A. R., Dubno, J. R., Lydiard, R. B., Hamner, M. B., Bohning, D. E., & George, M. S. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01284-7 · Cited by 359 · see citing works
Hermans, E. J., Ramsey, N. F., & van Honk, J. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.05.013 · Cited by 339 · see citing works
Self-citationThe Functional Neuroanatomy of Maternal Love: Mother’s Response to Infant’s Attachment Behaviors
Noriuchi, M., Kikuchi, Y., & Senoo, A. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.05.018 · Cited by 334 · see citing works
Time Course of Effects of Testosterone Administration on Sexual Arousal in Women
Tuiten, A., Van Honk, J., Koppeschaar, H., Bernaards, C., Thijssen, J., & Verbaten, R. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.2.149 · Cited by 288 · see citing works
Brain vasopressin is an important regulator of maternal behavior independent of dams’ trait anxiety
Bosch, O. J., & Neumann, I. D. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807412105 · Cited by 280 · see citing works
van Honk, J., Peper, J. S., & Schutter, D. J. L. G. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.04.003 · Cited by 266 · see citing works
Farmer, C. G. (2000) · The American Naturalist · doi:10.1086/303323 · Cited by 266 · see citing works
The cerebellum on the rise in human emotion
Schutter, D. J. L. G., & Van Honk, J. (2005) · The Cerebellum · doi:10.1080/14734220500348584 · Cited by 261 · see citing works
Testosterone promotes paternal behaviour in a monogamous mammal via conversion to oestrogen
Trainor, B. C., & Marler, C. A. (2002) · Proceedings of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rspb.2001.1954 · Cited by 238 · 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
Mother and newborn baby: Mutual regulation of physiology and behavior— A selective review
Winberg, J. (2005) · Developmental Psychobiology · doi:10.1002/dev.20094 · Cited by 232 · see citing works
Testosterone administration reduces empathetic behavior: A facial mimicry study
Hermans, E. J., Putman, P., & van Honk, J. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2006.04.002 · Cited by 231 · see citing works
Self-citationCornil, C. A., Ball, G. F., & Balthazart, J. (2006) · Brain Research · doi:10.1016/j.brainres.2006.07.098 · Cited by 223 · see citing works
Genes, brains and mammalian social bonds
Curley, J. P., & Keverne, E. B. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.05.018 · Cited by 214 · see citing works
PANKSEPP, 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
Biological Aspects of Social Bonding and the Roots of Human Violence
Pedersen, C. A. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1330.006 · Cited by 209 · see citing works
Maternal brain response to own baby‐cry is affected by cesarean section delivery
Swain, J. E., Tasgin, E., Mayes, L. C., Feldman, R., Todd Constable, R., & Leckman, J. F. (2008) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2008.01963.x · Cited by 206 · see citing works
From affect to control: Functional specialization of the insula in motivation and regulationPreprint
Wager, T. D., & Barrett, L. F. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/102368 · Cited by 200 · 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
Ascending Endorphin Inhibition of Distress Vocalization
Herman, B. H., & Panksepp, J. (1981) · Science · doi:10.1126/science.7466377 · Cited by 191 · see citing works
Water diffusion, T2, and compartmentation in frog sciatic nerve
Peled, S., Cory, D. G., Raymond, S. A., Kirschner, D. A., & Jolesz, F. A. (1999) · Magnetic Resonance in Medicine · doi:10.1002/(sici)1522-2594(199911)42:5 · Cited by 189 · see citing works
Lenzi, D., Trentini, C., Pantano, P., Macaluso, E., Iacoboni, M., Lenzi, G. L., & Ammaniti, M. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn153 · Cited by 174 · see citing works
Sex differences in vasopressin and oxytocin innervation of the brain
DEVRIES, G. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00402-0 · Cited by 169 · see citing works
Testosterone Reduces Conscious Detection of Signals Serving Social Correction
van Honk, J., & Schutter, D. J. L. G. (2007) · Psychological Science · doi:10.1111/j.1467-9280.2007.01955.x · Cited by 142 · see citing works
Three-dimensional functional magnetic resonance imaging of human brain on a clinical 1.5-T scanner.
van Gelderen, P., Ramsey, N. F., Liu, G., Duyn, J. H., Frank, J. A., Weinberger, D. R., & MOONEN, C. T. W. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.15.6906 · Cited by 140 · see citing works
Self-citationFrom Affective Valence to Motivational Direction
van Honk, J., & Schutter, D. J. L. G. (2006) · Psychological Science · doi:10.1111/j.1467-9280.2006.01813.x · Cited by 137 · see citing works
Hormonal correlates of human paternal interactions: A hospital-based investigation in urban Jamaica
Gray, P. B., PARKIN, J., & Samms‐Vaughan, M. E. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.07.005 · Cited by 135 · see citing works
Behavioral endocrinology of mammalian fatherhood
Wynne‐Edwards, K. E., & Wheaton, C. J. (2000) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(00)01972-8 · Cited by 126 · see citing works
FMRI activations of amygdala, cingulate cortex, and auditory cortex by infant laughing and crying
Sander, K., Frome, Y., & Scheich, H. (2007) · Human Brain Mapping · doi:10.1002/hbm.20333 · Cited by 121 · see citing works
Neggers, S. F. W., Hermans, E. J., & Ramsey, N. F. (2008) · NMR in Biomedicine · doi:10.1002/nbm.1235 · Cited by 114 · see citing works
Self-citationRamsey, N. F., van den Brink, J. S., van Muiswinkel, A. M., Folkers, P. J. M., MOONEN, C. T. W., Jansma, J. M., & Kahn, R. S. (1998) · NeuroImage · doi:10.1006/nimg.1998.0358 · Cited by 103 · see citing works
Self-citationWhy do mothers cradle babies on their left?
Sieratzki, J. S., & Woll, B. (1996) · The Lancet · doi:10.1016/s0140-6736(96)90813-2 · Cited by 98 · see citing works
Steroidal/neuropeptide interactions in hypothalamus and amygdala related to social anxiety
CHOLERIS, E., DEVIDZE, N., KAVALIERS, M., & PFAFF, D. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00424-x · Cited by 75 · see citing works
Giardino, J., González, A., Steiner, M. S., & Fleming, A. S. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.09.010 · Cited by 74 · see citing works
Does having a twin brother make for a bigger brain?
Peper, J. S., Brouwer, R. M., van Baal, G. C. M., Schnack, H. G., van Leeuwen, M., Boomsma, D. I., Kahn, R. S., & Pol, H. E. H. (2009) · European Journal of Endocrinology · doi:10.1530/eje-08-0915 · Cited by 45 · see citing works
Side biases for holding and carrying infants: Reports from the past and possible lessons for today
Harris, L. J. (2009) · Laterality Asymmetries of Body Brain and Cognition · doi:10.1080/13576500802584371 · Cited by 44 · see citing works
Ikeda, Y., & Nagai, A. (2006) · Brain Research · doi:10.1016/j.brainres.2006.02.025 · Cited by 41 · see citing works
Furedy, J. J., Fleming, A. S., Ruble, D. N., Scher, H., Daly, J., Day, D. M., & Loewen, R. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90056-5 · Cited by 19 · see citing works
Lorberbaum (1999) · doi:10.1002/(sici)1520-6394(1999)10:3
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Self-citationRiem, M. M. E., Bakermans-Kranenburg, M. J., Pieper, S., Tops, M., Boksem, M. A. S., Vermeiren, R. R. J. M., van IJzendoorn, M. H., & Rombouts, S. A. R. B. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.02.006 · Cited by 366 · see citing works
van Anders, S. M., Goldey, K. L., & Kuo, P. X. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.06.001 · Cited by 321 · see citing works
Swain, J. E., Kim, P., Spicer, J., Ho, S. S., Dayton, C. J., Elmadih, A., & Abel, K. M. (2014) · Brain Research · doi:10.1016/j.brainres.2014.03.007 · Cited by 290 · see citing works
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- Authors
- Bos, P. A., Hermans, E. J., Montoya, E. R., Ramsey, N. F., & van Honk, J.
- Affiliations
- Utrecht University (NL)
- Radboud University Nijmegen (NL)
- University Medical Center Utrecht (NL)
- Corresponding author
- Bos, Peter A.
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2010-01
- Volume
- 35
- Issue
- 1
- Pages
- 114-121
- ISSN
- 0306-4530 (ISSN-L)
- OpenAlex
- W2009497059
- Cited by
- 99
- References
- 60
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 5 · 2023: 5 · 2022: 5 · 2021: 4 · 2020: 5 · 2019: 9 · 2018: 4 · 2017: 8 · 2016: 10 · 2015: 11 · 2014: 7 · 2013: 5 · 2012: 8
- FWCI
- 6.94
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Funders
- Universiteit Utrecht
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Health Sciences › Health Professions › Pharmacy › Infant Health and Development
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Keywords
- testosterone, infant crying, parental responsiveness, estradiol, exogenous hormone administration, insula, cerebellum, parental care, young women
- MeSH terms
- Anxiety, Separation, Crying, Data Interpretation, Statistical, Female, Humans, Image Processing, Computer-Assisted, Infant, Magnetic Resonance Imaging, Male, Neural Pathways, Psychomotor Performance, Testosterone, Cross-Over Studies, Young Adult
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