Resting-state functional networks such as the default mode network (DMN) dominate spontaneous brain dynamics. To date, the mechanisms linking brain structure and brain dynamics and functions in cognition, perception, and action remain unknown, mainly due to the uncontrolled and erratic nature of the resting state. Here we used a stimulation paradigm to probe the brain’s resting behavior, providing insights on state-space stability and multiplicity of network trajectories after stimulation. We performed explorations on a mouse model to map spatiotemporal brain dynamics as a function of the stimulation site. We demonstrated the emergence of known functional networks in brain responses. Several responses heavily relied on the DMN and were suggestive of the DMN playing a mechanistic role between functional networks. We probed the simulated brain responses to the stimulation of regions along the information processing chains of sensory systems from periphery up to primary sensory cortices. Moreover, we compared simulated dynamics against in vivo brain responses to optogenetic stimulation. Our results underwrite the importance of anatomical connectivity in the functional organization of brain networks and demonstrate how functionally differentiated information processing chains arise from the same system. Author Summary We demonstrate how functionally differentiated information processing chains arise from the same anatomical network. The main result of the in-silico mouse brain simulations is the emergence of specific functional networks based on structural data from the mouse brain. When the brain is stimulated, for example, by sensory inputs or direct electrical stimulation, the brain initially responds with activities in specific regions. The brain’s anatomical connectivity constrains the subsequent pattern formation. We built a high-resolution mouse brain network model. The model structure originated from experimental data. We systematically explored the mouse model and investigated the simulated brain dynamics after stimulation. Known functional networks emerged in the simulated brain responses. The default mode network occurred in almost all characteristic response patterns. Simulated brain response dynamics and in-vivo response dynamics of the mouse brain to optogenetic stimulation showed similarities even without parameter tuning. Anatomical connectivity and dynamics shape the functional organization of brain networks.