Defining the relationship between maternal care, sensory development and brain gene expression in neonates is important to understand the impact of environmental challenges during sensitive periods in early life. In this study, we used a selection approach to test the hypothesis that variation in maternal licking and grooming (LG) during the first week of life influences sensory development in Wistar rat pups. We tracked the onset of the auditory brainstem response (ABR), the timing of eye opening (EO), middle ear development with micro-CT X-ray tomography, and used qRT-PCR to monitor changes in gene expression of the hypoxia-sensitive pathway and neurotrophin signaling in pups reared by low-LG or high-LG dams. The results show the first evidence that the transcription of genes involved in the hypoxia-sensitive pathway and neurotrophin signaling is regulated during separate sensitive periods that occur before and after hearing onset, respectively. Although the timing of ABR onset, EO, and the relative mRNA levels of genes involved in the hypoxia-sensitive pathway did not differ between pups from different LG groups, we found statistically significant increases in the relative mRNA levels of four genes involved in neurotrophin signaling in auditory brain regions from pups of different LG backgrounds. These results suggest that sensitivity to hypoxic challenge might be widespread in the auditory system of neonate rats before hearing onset, and that maternal LG may affect the transcription of genes involved in experience-dependent neuroplasticity.

The experience of variation in maternal licking and grooming (LG) is considered a critical influence in neurodevelopment related to stress and cognition, but little is known about its relationship to early sensory development. In this study, we used a maternal selection approach to test the hypothesis that differences in LG during the first week of life influence the timing of hearing onset in Wistar rat pups. We performed a range of tests, including auditory brainstem responses (ABR), tracking of eye opening (EO), micro-CT X-ray tomography, and qRT-PCR to monitor neurodevelopmental changes in the female and male progeny of low-LG and high-LG dams. Our results show that variation in maternal LG is not overtly associated with different timing of ABR onset and EO in the progeny. However, the data provide insight on the delay between hearing onset and EO, on key functional and structural properties that define hearing onset at the auditory periphery, and on changes in brain gene expression that include the first evidence that: a) the hypoxia-sensitive pathway is regulated in subcortical and cortical auditory brain regions before hearing onset, and b) implicates maternal LG in regulation of Bdnf signaling in auditory cortex after hearing onset. Altogether, these findings provide a baseline to evaluate how factors that severely disrupt the early maternal environment may affect the expression of robust developmental sensory programs.SIGNIFICANCE STATEMENTEarly life experience during sensitive developmental periods can induce long-term effects on the neurobiological development of the offspring. In the present work we tested the hypothesis that variation in maternal licking and grooming (LG) affects the timing of hearing onset in Wistar rat pups. To our surprise the results did not support the hypothesis. Instead, we found a robust range of early and late auditory development that was independent of maternal LG. Nevertheless, the study provides new findings on the delay between hearing onset and eye opening, on key functional and structural properties that define hearing onset at the auditory periphery, and the first evidence that a) the hypoxia-sensitive pathway is regulated in the central auditory system during the sensitive period before hearing onset, and b) maternal LG is implicated in regulation of Bdnf signaling during the sensitive period after hearing onset. These findings provide a baseline to evaluate how factors that severely disrupt the early maternal environment may affect the expression of robust developmental sensory programs.