Differential sex-independent amygdala response to infant crying and laughing in parents versus nonparents
Abstract
Background Animal and human studies implicate forebrain neural circuits in maternal behavior. Here, we hypothesized that human brain response to emotional stimuli relevant for social interactions between infants and adults are modulated by sex- and experience-dependent factors.Methods We used functional magnetic resonance imaging and examined brain response to infant crying and laughing in mothers and fathers of young children and in women and men without children.Results Women but not men, independent of their parental status, showed neural deactivation in the anterior cingulate cortex, as indexed by decreased blood oxygenation level-dependent signal, in response to both infant crying and laughing. The response pattern changed fundamentally with parental experience: in the amygdala and interconnected limbic regions, parents (independent of sex) showed stronger activation from crying, whereas nonparents showed stronger activation from laughing.Conclusions Our data show sex- and experience-dependent modulation of brain response to infant vocalizations. Successful recognition and evaluation of infant vocalizations can be critical for bonding mechanisms and for offspring well-being and survival. Thus, the modulation of responses by experience seems to represent an adaptive mechanism that can be related to reproductive fitness.
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In response to infant stimuli, infant cry and smiles activate the amygdala.
“In response to infant stimuli, infant cry and smiles activate the amygdala (Barrett et al., 2012; Seifritz et al., 2003; Swain et al., 2008), which has often been interpreted as a sign of emotional salience (Seifritz et al., 2003; Strathearn and Kim, 2013) or positive emotion associated with attachment (Leibenluft et al., 2004).”
From The maternal brain and its plasticity in humans (2016) · cites this paper as Seifritz et al., 2003
Women as a group including parents and non-parents, but not males, had a decrease in activity in response to both baby cry and laughter in the subgenual anterior cingulate cortex.
“They also reported that women as a group including, parents and non-parents (but not males), had a decrease in activity in response to both baby cry and laughter in the subgenual anterior cingulate cortex.”
From The human parental brain: In vivo neuroimaging (2011) · cites this paper as Seifritz et al., 2003
Within-group analyses showed that parents activated more to infant crying than laughing in the right amygdala, while non-parent response was greater for infant laughing than crying.
“Finally, within-group analyses showed that parents activated more to infant crying than laughing in the right amygdala, while non-parent response was greater for infant laughing then crying (Seifritz et al., 2003).”
From The human parental brain: In vivo neuroimaging (2011) · cites this paper as Seifritz et al., 2003
Over the entire sample, intensity-matched baby sounds of crying and laughing compared to neutral sounds produced more brain activity in bilateral temporal regions.
“Over the entire sample, intensity-matched baby sounds of crying and laughing compared to “neutral” sounds (white noise pulsed at 5-Hz with an averaged frequency spectrum similar to the infant vocalizations) produced more brain activity in bilateral temporal regions.”
From The human parental brain: In vivo neuroimaging (2011) · cites this paper as Seifritz et al., 2003
Mothers and fathers have been grouped together to look for common parental brain responses suggesting commonalities across sex.
“Mothers and fathers have been grouped together to look for common parental brain responses suggesting commonalities across sex.”
From The human parental brain: In vivo neuroimaging (2011) · cites this paper as Seifritz et al. (2003)
Over the entire sample, intensity-matched baby sounds of crying and laughing compared to neutral sounds produced more brain activity in bilateral temporal regions.
“Over the entire sample, intensity-matched baby sounds of crying and laughing compared to “neutral” sounds (white noise pulsed at 5-Hz with an averaged frequency spectrum similar to the infant vocalizations) produced more brain activity in bilateral temporal regions.”
From Approaching the biology of human parental attachment: Brain imaging, oxytocin and coordinated assessments of mothers and fathers (2014) · cites this paper as Seifritz et al., 2003
Parents activated more to infant crying than laughing in the right amygdala, while non-parent response was greater for infant laughing than crying.
“Their within-group analyses reported that parents activated more to infant crying than laughing in the right amygdala, while non-parent response was greater for infant laughing than crying (Seifritz et al., 2003).”
From Approaching the biology of human parental attachment: Brain imaging, oxytocin and coordinated assessments of mothers and fathers (2014) · cites this paper as Seifritz et al., 2003
Women as a group including parents and non-parents (but not men) showed decreased activity in response to both baby cry and laughter in the subgenual anterior cingulate cortex.
“They also reported that women as a group including, parents and non-parents (but not men), showed decreased activity in response to both baby cry and laughter in the subgenual anterior cingulate cortex.”
From Approaching the biology of human parental attachment: Brain imaging, oxytocin and coordinated assessments of mothers and fathers (2014) · cites this paper as Seifritz et al., 2003
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- Authors
- Seifritz, E., Esposito, F., Neuhoff, J. G., Lüthi, A., Mustovic, H., Dammann, G., von Bardeleben, U., Radue, E. W., Cirillo, S., Tedeschi, G., & Di Salle, F.
- Affiliations
- University of Basel (CH)
- University of Campania "Luigi Vanvitelli" (IT)
- College of Wooster (US)
- Corresponding author
- Seifritz, Erich
- ORCID
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2003-12
- Volume
- 54
- Issue
- 12
- Pages
- 1367-1375
- ISSN
- 0006-3223 (ISSN-L)
- OpenAlex
- W1967601351
- Semantic Scholar
- 04cb4b3404770857e9c4b2cc888df401b25c1ce7
- Cited by
- 373
- References
- 68
- Citations by year
- 2026: 10 · 2025: 6 · 2024: 11 · 2023: 5 · 2022: 15 · 2021: 20 · 2020: 30 · 2019: 24 · 2018: 19 · 2017: 25 · 2016: 21 · 2015: 24 · 2014: 19 · 2013: 23 · 2012: 24
- FWCI
- 25.65
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Health Professions › Pharmacy › Infant Health and Development
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Keywords
- amygdala, infant crying, infant laughter, parental experiences, sex differences, maternal behavior, anterior cingulate cortex, neural deactivation, infant vocalizations, parent-infant bonding, limbic system, reproductive fitness
- MeSH terms
- Acoustic Stimulation, Adult, Amygdala, Child, Preschool, Crying, Female, Gyrus Cinguli, Humans, Infant, Functional Laterality, Laughter, Magnetic Resonance Imaging, Male, Parent-Child Relations, Sex Characteristics, Time Factors
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