Abstract
A developing brain shows intense re-organization and heightened neuronal plasticity allowing for environmental modulation of its development. During early life, maternal care is a key factor of this environment and defects in this care can derail adaptive brain development and may result in susceptibility to neuropsychiatric disorders. Nevertheless, the mechanisms by which those maternal interactions immediately impact the offspring’s brain activity to initiate the pathway to pathology are not well understood. We do know that multiple neurotransmitter systems are involved, including the serotonergic system, a key neuromodulator involved in brain development and emotional regulation. We tested the importance of the serotonergic system and pups’ immediate neural response to maternal presence using wireless electrophysiological recordings, a novel approach allowing us to record neural activity during pups’ interactions with their mother.
We found that maternal contact modulates the P10-P12 rat pups’ anterior cingulate cortex activity by notably increasing local field potential power in low-frequency bands. We demonstrated, by blocking serotonergic receptors, that this increase is mediated through 5-HT2 receptors. Finally, we showed in isolated pups that enhancing serotonergic transmission, using a selective-serotonin-reuptake-inhibitor, is sufficient to enhance local field potential power in low frequency bands in a pattern similar to that observed when the mother is in the nest. Our results highlight a significant contribution of the serotonergic system in mediating changes of cortical activity in pups related to maternal presence.
Significance Statement Maternal care is a major environmental factor influencing brain development and deficits in this care can result in maladaptive behaviors in the offspring. While maternal interaction is crucial, little is known about the underlying mechanisms by which it modulates infant/pup brain activity. In this study, using wireless electrophysiological recordings, we show that the mother’s contact regulates the activity of key prefrontal regions of 10-12 D-old rat pups. Regarding mechanisms, we found that the serotonergic system contributes to this modulation, notably through 5HT2 receptors. These results suggest maternal care affects serotonergic neural activity during early life and provide key insights into how maternal care affects the adaptive/maladaptive development of brain circuits implicated in adult pathology.
Footnotes
Authors report no conflict of interest.
This work was funded by NICHD grant R03HD094978 to C.M.T., NIDCD grant R01003906 to D.A.W., NICHD grant R37HD083217 to R.M.S and by NIDCD grant R03DC014540 to E.C.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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