The neural microtubule-associated protein tau is critical for neuronal structure and function. Tau is a potent regulator of microtubule dynamics and plays a key role in organizing the uniformly spaced microtubule bundles observed in axons, despite the fact that each tau molecule possesses only one microtubule-binding region. Here we describe our attempts to better understand tau structure and function. A novel model for tau dimerization was developed from analysis using a surface forces apparatus and directly tested using biochemical techniques such as native and denaturing electrophoresis and Ferguson plots. Next, the hypothesis that tau dimerization is important for tau action was tested by assaying tau-mediated microtubule assembly and bundling activities via light scattering and electron microscopy. Our data support the model that tau oligomerizes as part of its normal action and that inhibition of oligomerization can poison tau activity. Together, our results suggest a possible role for oligomerization in normal tau action, which may also be relevant to pathological tau action in Alzheimer's disease and related dementias.