Neural stem and progenitor cells reside within specialized brain niches, yet regenerative output declines with age and may become minimal, silent, or regionally restricted. This decline is usually attributed to intrinsic cellular aging and deterioration of the local niche, including epigenetic, metabolic, inflammatory, vascular, proteostatic, and senescent-like changes. However, neurogenic and formerly neurogenic niches are also embedded within active neural circuits whose signals can regulate progenitor activation, quiescence, survival, maturation, and integration. This review develops a circuit-instructed framework in which regenerative failure can arise from altered circuit signals, altered receiver or niche competence, impaired signal translation, or combinations of these processes. Five operational models are distinguished when neurogenesis declines or becomes silent: circuit withdrawal, persistence without neurogenesis, circuit repurposing, maladaptive communication, and compensatory communication. These models are not assumed to be equally established empirically, and evidence is evaluated according to species, brain region, age, study design, and level of causal support. Evidence from the human hippocampus and ventricular–subventricular zone is therefore considered separately from rodent perturbational evidence, and computational or molecular trajectories are treated as hypothesis-generating rather than proof of lineage progression or causality. Ischemic stroke and traumatic brain injury are used as stress tests of circuit–niche coupling, and a stage-gated preclinical roadmap is proposed in which biological context, failure-mode classification, mechanistic reversibility, intervention matching, functional benefit, and safety must be established sequentially. Artificial intelligence-guided multimodal analysis is positioned as an integrative tool for generating testable hypotheses rather than as an autonomous diagnostic or treatment-selection system. Neural stem cell aging may therefore reflect not only cellular decline but a context-dependent failure of communication among cell state, niche state, and circuit state.