DEVELOPMENTAL MATURATION OF LAYER 1 INTERNEURONS IN THE AUDITORY CORTEX

During early postnatal development, inhibitory circuits undergo profound refinement that shapes sensory processing in the auditory cortex. While the maturation of pyramidal neurons and inhibitory interneurons in deeper layers has been well studied, the developmental trajectory of layer 1 (L1) interneurons remains largely unknown. These L1 neurons, particularly neurogliaform cells (NGFs), are strategically positioned to modulate auditory processing, as they receive both bottom-up sensory inputs and top-down modulatory inputs. However, it remains unclear how their functional properties mature across development and how they compare with those of excitatory neurons in layer 2/3 (L2/3). Using in vivo two-photon calcium imaging, we recorded spontaneous and sensory-evoked activity from NGFs in L1 and L2/3 excitatory cells in the auditory cortex from early postnatal stages to adulthood. Analysis of spontaneous activity showed that, in both L1 and L2/3, neuronal activity is more highly correlated during development than in adulthood. In particular, spontaneous activity decorrelates more rapidly in NGFs than in L2/3 neurons, accompanied by a decrease in population coupling. In parallel, we observed an increase in network dimensionality in both layers, consistent with a transition towards more complex activity patterns in adults. During single-tone stimulation, NGFs showed a reduction in the number of responsive trials and an increase in the proportion of highly selective cells, compared to development. Together, these results suggest that changes in spontaneous activity across development reflect the maturation of cortical circuit organization, which supports the emergence of mature auditory processing.