Maintaining balance necessitate an accurate perceptual map of the external world. Neuro-physiological mechanisms of locomotor control, sensory perception and anxiety systems, have been viewed as separate entities that can on occasion affect each other (i.e. walking on ice). Emerging models are more integrated, that envision sensory perception and threat assessment as a fundamental component of balance. Here we present the empirically based theoretical argument, that vestibular cortical areas construct magnitude estimates of the external world via neural integration of incoming sensory signals. In-turn these cortically derived magnitude estimates, construct context-dependent vestibulo-spatial and vestibulo-temporal representational maps of the external world, and, ensure an appropriate online scaling factor for associated action-perceptual risk. Thus, threat signals exert a continuous influence on planning movements, predicting outcomes of motion of self and surrounding objects, and adjusting tolerances for discrepancies between predicted and actual estimates. Such a process affects the degree of conscious attention directed to spatial and temporal aspects of motion stimuli, implying that maintaining balance may follow a Bayesian approach in which the relative weighting of vestibulo-spatial and vestibulo-temporal signals and tolerance for discrepancies are adjusted in accordance with the level of threat assessment. Here, we seek to mechanistically explain this process with our novel empirical concept of a Brainstem Cortical Scaling Metric (BCSM), which we developed from a series of neurophysiological studies illustrating the central role of interhemispheric vestibulo-cortical asymmetries for balance control. We conclude by using the BCSM to derive theoretical predictions of how a dysfunctional BCSM can mechanistically-account for functional dizziness.