The early steps in vertebrate vision require fast interactions between Rh (rhodopsin) and Gt (transducin), which are classically described by a collisional coupling mechanism driven by the free diffusion of monomeric proteins on the disc membranes of rod and cone cells. Recent findings, however, point to a very low mobility for Rh and support a substantially different supramolecular organization. Moreover, Rh-G(t) interactions seem to possibly occur even prior to light stimuli, which is also difficult to reconcile with the classical scenario. We investigated the kinetics of interaction between native Rh and G(t) in different conditions by surface plasmon resonance and analysed the results in the general physiological context by employing a holistic systems modelling approach. The results from the present study point to a mechanism that is intermediate between pure collisional coupling and physical scaffolding. Such a 'dynamic scaffolding', in which prevalently dimeric Rh and G(t) interact in the dark by forming transient complexes (~25% of G(t) is precoupled to Rh), does not slow down the phototransduction cascade, but is compatible with the observed photoresponses on a broad scale of light stimuli. We conclude that Rh molecules and Rh-G(t) complexes can both absorb photons and trigger the visual cascade.