The mTOR pathway is a pivotal cellular signaling pathway that impacts neuronal differentiation and function. Genetic disruptions leading to hyperactivation of the mTOR pathway, termed mTORopathies, represent rare genetic and systemic disorders that are associated with altered brain development and epilepsy. However, the precise mechanisms by which disrupted mTOR signaling affects neuronal network development and signaling remain poorly understood. Human induced pluripotent stem cells (iPSCs) and CRISPR/Cas9 genome editing, allowed the generation of a panel of isogenic iPSC lines carrying mutations in mTOR regulator genes, including RHEB, MTOR, PIK3CA and TSC2. We functionally phenotyped iPSC-derived neuronal networks composed of glutamatergic and GABAergic neurons, a human in vitro model for excitatory/inhibitory balance, on multi electrode arrays. This phenotyping showed that mutations in all mTOR regulator genes induced neuronal network hyperactivity during development. However, the developmental trajectory and degree of hyperactivity were mutation specific. Pharmacological interrogation of the networks during development suggested that delayed or incomplete maturation of GABAergic signaling may contribute significantly to these mutation-specific fingerprints. Additionally, at the structural level we observed mutation-specific alterations in neuronal morphology and glutamatergic and GABAergic synaptic connectivity. Collectively, our functional data and specific structural observations imply that mutation specific hyperactive phenotypes during network development result from an interplay between altered GABAergic signaling and extensive, possibly compensatory, structural network alterations. Our study underscores the complex relationship between genetic factors and mTOR pathway signaling, potentially underlying the clinical complexity of mTORopathies.