Bill Greenough's work provides a framework for thinking about synaptogenesis not only as a key step in the initial wiring of neural systems according to a species typical plan (i.e., experience-expectant development), but also as a mechanism for storing information based an individual's unique experience over its lifetime (i.e., experience-dependent plasticity). Analysis of synaptic development in vitro brings a new opportunity to test the limits of expectant-expectant development at the level of the individual neuron. We analyzed dendritic growth, synapse formation, and the development of specialized cytoplasmic microdomains during development in cultured hippocampal neurons, to determine if the timing of each of these events is correlated. Taken together, the findings reported here support the hypotheses that (1) dendritic development is rate limiting in synapse formation and (2) synaptic circuits are assembled in a step-wise fashion consistent with a stage-specific shift from genomically pre-programmed to activity-dependent mechanisms. © 2011 Wiley Periodicals, Inc. Dev Psychobiol 53:443–455, 2011.