Postnatal development of pyramidal neurons excitability and synaptic inputs in mouse gustatory cortical circuits

Cortical neurons in sensory areas undergo a protracted process of postnatal maturation that includes changes in membrane properties, synaptic drive and connectivity. The completion of this process is associated with the closure of sensitive windows for experience-dependent plasticity. Weaning is a critical time in the development of taste circuits as animals transition from depending on the mother for nutrition to eating independently. While there is some evidence for developmental changes in taste bud innervation and in membrane properties of neurons in brainstem circuits for taste, very little is known about postnatal changes in the gustatory cortex (GC), the primary cortical region for taste and taste-guided behaviors. Here, we focused on pyramidal neurons in the deep layers of GC and compared their membrane properties in pre- and postweaning age groups. We report dynamic changes in intrinsic excitability and a progressive shift of the excitation/inhibition (E/I) balance toward inhibition as pyramidal neurons reach their young adult properties. The increase in inhibitory drive accompanied a protracted process of postnatal maturation of inhibitory circuits mediated by parvalbumin expressing neurons (PV neurons) that showed a progressive increase in their association with perineuronal nets (PNNs) and refinement of their connectivity onto pyramidal neurons. Together, our results indicate that GC neurons undergo protracted postnatal maturation that may influence taste response properties at the transition to independent feeding. Significance StatementWe show that the circuit in the gustatory cortex undergoes a protracted maturation process that extends into adulthood and progressively shifts the excitability of GC toward inhibition through changes in pyramidal neurons membrane properties, increased inhibitory synaptic drive and refinement of parvalbumin neurons connectivity. This maturation process extends beyond the developmental windows previously reported for other sensory cortical circuits and overlaps with the recently identified critical period for the development of taste preferences. As finding nutritious food sources may require the integration of vision, audition, somatosensation and olfaction, the extended maturation process for taste cortical circuits may facilitate the integration of sensory information for the identification of food and the decision to ingest it.