The precise mapping of sensory inputs onto cortical regions is critical for accurate sensory processing, as illustrated in the rodent primary somatosensory cortex (S1), where mystacial and upper lip whiskers are represented into distinct cortical maps: the postero-medial barrel subfield (PMBSF) and the antero-lateral barrel subfield (ALBSF). While the developmental timeline of PMBSF maps across somatosensory pathways is well-characterized, the mechanisms underlying the intra-modal positioning and dedicated cortical territories of these barrel-field patterns remain elusive. Our findings reveal that as early as embryonic day 18 to postnatal day 0, S1 barrel-field territories can be distinguished by facial stimulation-evoked responses and exhibit region-specific transcriptional profiles in the thalamus. To explore the processes driving this segregation, we developed a mouse model in which the mystacial whisker pad was unilaterally ablated during embryonic development. This model uncovered a critical prenatal window during which cortical maps are established, revealing a profound remapping of barrel-field territories. Specifically, ALBSF barrels, typically smaller and less distinct than the large, sharply defined PMBSF barrels, exhibited enhanced size and definition. These differences, traditionally attributed to variations in receptor density and input type, are instead driven by prenatal mechanisms regulating cortical development and spatial resolution independently of sensory experience. Notably, this reorganization is mediated by transcriptional programs in the thalamus, with neurons receiving upper lip inputs adopting a mystacial-like transcriptional profile. Furthermore, spontaneous activity patterns in the thalamic region corresponding to upper lip mimic mystacial-like frequencies, potentially contributing to the improved spatial resolution of this map. However, ALBSF reorganization occurs independently of this activity. These findings highlight the developmental plasticity of the somatosensory system, providing insights into the intrinsic molecular mechanisms shaping sensory maps and advancing our understanding of cortical development and plasticity in both normal and injury contexts.
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