Schiff Hillary, Maffei Arianna
bioRxiv. 2025 Sep 11:2025.09.11.675590. doi: 10.1101/2025.09.11.675590.
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.
We 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.
感觉区域的皮质神经元经历一个漫长的出生后成熟过程，包括膜特性、突触驱动和连接性的变化。这个过程的完成与依赖经验的可塑性敏感窗口的关闭有关。断奶是味觉回路发育中的一个关键时期，因为动物从依赖母亲获取营养过渡到独立进食。虽然有一些证据表明味蕾神经支配以及脑干味觉回路中神经元的膜特性存在发育变化，但对于味觉的主要皮质区域——味觉皮质（GC）在出生后的变化却知之甚少。在这里，我们聚焦于GC深层的锥体神经元，并比较了断奶前后年龄组它们的膜特性。我们报告了随着锥体神经元达到其年轻成年特性，其内在兴奋性的动态变化以及兴奋/抑制（E/I）平衡向抑制的逐渐转变。抑制性驱动的增加伴随着由表达小白蛋白的神经元（PV神经元）介导的抑制性回路出生后成熟的漫长过程，PV神经元与神经元周围网（PNN）的关联逐渐增加，并且它们与锥体神经元的连接得到细化。总之，我们的结果表明GC神经元经历了漫长的出生后成熟过程，这可能会影响向独立进食过渡时的味觉反应特性。
我们表明味觉皮质中的回路经历了一个延伸至成年期的漫长成熟过程，通过锥体神经元膜特性的变化、增加的抑制性突触驱动以及小白蛋白神经元连接的细化，逐渐将GC的兴奋性转向抑制。这个成熟过程超出了先前报道的其他感觉皮质回路的发育窗口，并且与最近确定的味觉偏好发展关键期重叠。由于寻找营养食物来源可能需要整合视觉、听觉、躯体感觉和嗅觉，味觉皮质回路的延长成熟过程可能有助于整合感觉信息以识别食物并决定摄取它。
