Mutations in SYNGAP1 gene represent one of the most frequent genetic causes of neurodevelopmental disorders. De novo heterozygous SYNGAP1 variants are associated with a complex clinical presentation, characterized by intellectual disability, epileptic encephalopathy, hyperactivity, sleep and language disorder, and autism spectrum disorder. The SynGAP protein is highly expressed in excitatory neurons and localized mainly to synapses as a core post-synaptic density protein. Here, it acts as a potent regulator of the RAS/ERK signalling pathway, regulating synaptic plasticity and neuronal homeostasis. In addition, recent studies started revealing the polyhedric nature of SynGAP, highlighting its role in modulating interneuron development and activity, as well as its synaptic-independent role in shaping early phases of brain development. In this study, we employed a systematic approach to advance our understanding of the effects of patient-specific SYNGAP1 mutations during brain development. Through 3D protein modeling, we predicted the effects of different mutations on the protein structure, concurrently investigating their effects on interactions with established SynGAP interactors. Moreover, we generated human induced pluripotent stem cells (hiPSCs) derived from patients' fibroblasts. To assess how these patient-specific SYNGAP1 mutations influence the functional development and maturation of neuronal and non-neuronal populations, we generated 2D in vitro models from hiPSCs. We tracked the maturation process and characterized the expression of known excitatory and inhibitory synaptic markers at multiple time points during development. Additionally, we conducted patch clamp recordings to examine synaptic transmission and membrane excitability at single-cell resolution, while employing multi-electrode array recordings to investigate global circuit activity in parallel.