Maternal regulation of infant brain state
Open accessAbstract
Patterns of neural activity are critical for sculpting the immature brain, and disrupting this activity is believed to underlie neurodevelopmental disorders [1-3]. Neural circuits undergo extensive activity-dependent postnatal structural and functional changes [4-6]. The different forms of neural plasticity [7-9] underlying these changes have been linked to specific patterns of spatiotemporal activity. Since maternal behavior is the mammalian infant's major source of sensory-driven environmental stimulation and the quality of this care can dramatically affect neurobehavioral development [10], we explored, for the first time, whether infant cortical activity is influenced directly by interactions with the mother within the natural nest environment. We recorded spontaneous neocortical local field potentials in freely behaving infant rats during natural interactions with their mother on postnatal days ∼12-19. We showed that maternal absence from the nest increased cortical desynchrony. Further isolating the pup by removing littermates induced further desynchronization. The mother's return to the nest reduced this desynchrony, and nipple attachment induced a further reduction but increased slow-wave activity. However, maternal simulation of pups (e.g., grooming and milk ejection) consistently produced rapid, transient cortical desynchrony. The magnitude of these maternal effects decreased with age. Finally, systemic blockade of noradrenergic beta receptors led to reduced maternal regulation of infant cortical activity. Our results demonstrate that during early development, mother-infant interactions can immediately affect infant brain activity, in part via a noradrenergic mechanism, suggesting a powerful influence of the maternal behavior and presence on circuit development.
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During the preweaning period, LFP recordings from mediofrontal cortex exhibit event-related reductions in theta power in response to maternal separation.
“During the preweaning period, local field potential (LFP) recordings from depth electrodes within mediofrontal cortex exhibit event-related reductions in theta power in response to periods of maternal separation (Courtiol et al., 2018; Sarro et al., 2014).”
From Adolescent cognitive control and mediofrontal theta oscillations are disrupted by neglect: Associations with transdiagnostic risk for psychopathology in a randomized controlled trial (2020) · cites this paper as Sarro et al., 2014
There is evidence for a sensitive period in the rodent, as maternal separation is less likely to influence mediofrontal theta if separations occur at older compared to younger ages.
“there is evidence for a sensitive period in the rodent, as maternal separation is less likely to influence mediofrontal theta if separations occur at older compared to younger ages (Sarro et al., 2014)”
From Adolescent cognitive control and mediofrontal theta oscillations are disrupted by neglect: Associations with transdiagnostic risk for psychopathology in a randomized controlled trial (2020) · cites this paper as Sarro et al., 2014
The current findings bear similarity to reports of reduced mediofrontal theta in rodent models of neglect/maternal separation.
“The current findings bear similarity to reports of reduced mediofrontal theta in rodent models of neglect/ maternal separation (Courtiol et al., 2018; Reincke and Hanganu-Opatz, 2017; Sarro et al., 2014)”
From Adolescent cognitive control and mediofrontal theta oscillations are disrupted by neglect: Associations with transdiagnostic risk for psychopathology in a randomized controlled trial (2020) · cites this paper as Sarro et al., 2014
In rodents, maternal presence/absence drives event-related increases/decreases in mediofrontal theta.
“maternal presence/absence drives event-related increases/decreases in mediofrontal theta (Courtiol et al., 2018; Sarro et al., 2014).”
From Adolescent cognitive control and mediofrontal theta oscillations are disrupted by neglect: Associations with transdiagnostic risk for psychopathology in a randomized controlled trial (2020) · cites this paper as Sarro et al., 2014
During the preweaning period, maternal presence is associated with event-related increases in mediofrontal theta of rat pups, compared to reductions when the mother is absent or when the rat pup is removed from the nest.
“During the preweaning period, maternal presence is associated with event-related increases in mediofrontal theta of rat pups, compared to reductions when the mother is absent or when the rat pup is removed from the nest (Courtiol et al., 2018; Sarro et al., 2014).”
From Adolescent cognitive control and mediofrontal theta oscillations are disrupted by neglect: Associations with transdiagnostic risk for psychopathology in a randomized controlled trial (2020) · cites this paper as Sarro et al., 2014
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Neurobiology of Parental Regulation of the Infant and Its Disruption by Trauma Within Attachment
Graf, N., Zanca, R. M., Song, W., Zeldin, E., Raj, R., & Sullivan, R. M. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.806323 · Cited by 11 · see citing works
Self-citationInvestigating default mode network connectivity disruption in children of mothers with depression
Zeev‐Wolf, M., Dor‐Ziderman, Y., Pratt, M., Goldstein, A., & Feldman, R. (2021) · The British Journal of Psychiatry · doi:10.1192/bjp.2021.164 · Cited by 10 · see citing works
Xu, X., Buzzell, G. A., Bowers, M. E., Shuffrey, L. C., Leach, S. C., McSweeney, M., Yoder, L., Fifer, W. P., Myers, M. M., Elliott, A. J., et al. (2024) · Development and Psychopathology · doi:10.1017/s0954579424000816 · Cited by 7 · see citing works
Perinatal exposure to omega-3 fatty acid imbalance leads to early behavioral alterations in rat pups
Colucci, P., Castro, V. D., Peloso, A., Splendori, M., Trezza, V., & Campolongo, P. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112723 · Cited by 7 · see citing works
Duan, T. Q., Hagenauer, M. H., Flandreau, E. I., Bader, A., Nguyen, D. M., Maras, P. M., de Lima, R. M. S., Gyles, T. M., Mclain, C., Meaney, M. J., et al. (2025) · Brain and Behavior · doi:10.1002/brb3.70608 · Cited by 6 · see citing works
Child‐parent cardiac transference is decreased following disrupted/absent early care
Callaghan, B. L., Pini, N., Silvers, J. A., Tieghem, M. V., Choy, T., O’Sullivan, K., Fifer, W. P., & Tottenham, N. (2021) · Developmental Psychobiology · doi:10.1002/dev.22102 · Cited by 4 · see citing works
Fitzgerald, M. (2024) · The Journal of Physiology · doi:10.1113/jp283994 · Cited by 3 · see citing works
Neurodevelopmental effects of early life stress: PFC and cognition
Rachmany, L., de Abreu, F. F., Walker, V., O'Neill, O. S., Sargin, D., & Teixeira, C. M. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106663 · Cited by 4 · see citing works
Ranger, M., Behring, T. B., Kaidbey, J. H., Anwar, M., Lipshutz, A. B., Mollicone, I., Hassan, G., Fasano, K. M., Hinz, N. K., Ludwig, R. J., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.19.444831 · Cited by 2 · see citing works
Early life adversity impairs visually evoked innate defensive behaviors via oxytocin signaling
Tan, H., Su, J., Ma, S., Chen, S., Liu, Q., Yang, X., & Wang, L. (2026) · Communications Biology · doi:10.1038/s42003-026-09738-0 · Cited by 1 · see citing works
Posttraumatic Stress Disorder: From Neurobiology to Cycles of Violence
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Neural Maturation of Breastfed Infants
PEHLEVAN, Ö. S., Kara, B., & Briana, D. D. (2023) · Springer eBooks · doi:10.1007/978-3-031-33278-4_22
Early-Life Stress and Psychiatric-Like Behaviors in Rodents: Reconsidering Sensitive Periods
Kajita, Y. (2026) · IntechOpen eBooks · doi:10.5772/intechopen.1014613
Trauma in Attachment: Understanding the First Relationship Through Neurobiology and Psychodynamics
Chambers, J. E., & Sullivan, R. (2026) · Psychodynamic Psychiatry · doi:10.1521/pdps.2026.54.2.249
Self-citationMaturation of social adaptation circuits from ontogeny to pathology
Gleske, M., Jeanneteau, F. D., Opendak, M. M., & Coutellier, L. D. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106874
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- Authors
- Sarro, E. C., Wilson, D. A., & Sullivan, R. M.
- Affiliations
- Nathan Kline Institute for Psychiatric Research (US)
- Corresponding author
- Sarro, Emma C.
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2014-07
- Volume
- 24
- Issue
- 14
- Pages
- 1664-1669
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC4108557
- OpenAlex
- W2062592498
- Cited by
- 61
- References
- 50
- Citations by year
- 2026: 6 · 2025: 2 · 2024: 5 · 2023: 3 · 2022: 4 · 2021: 5 · 2020: 6 · 2019: 3 · 2018: 5 · 2017: 6 · 2016: 7 · 2015: 8 · 2014: 1
- FWCI
- 4.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH091451)
- National Institute on Deafness and Other Communication Disorders (R01DC009910)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- maternal behavior, infant brain development, local field potentials, mother-infant interaction, nest environment, slow-wave activity, neuroplasticity, postnatal development, infant rats, neurodevelopmental disorders
- MeSH terms
- Animals, Animals, Newborn, Brain, Feeding Behavior, Grooming, Maternal Behavior, Nervous System Physiological Phenomena, Neural Pathways, Neuronal Plasticity, Rats, Brain Waves, Adrenergic Neurons
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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