High resolution laminar fMRI is beginning to probe responses in the different layers of cortex. What can we expect this exciting new technique to discover about cortical processing and how can we verify that it is producing an accurate picture of the underlying laminar differences in neural processing? This review will address our knowledge of laminar cortical circuitry gained from electrophysiological studies in macaque monkeys with a focus on the primary visual cortex, as this area has been most often targeted in both laminar electrophysiological and fMRI studies. We will review how recent studies are attempting to verify the accuracy of laminar fMRI by recreating the known laminar profiles of various neural tuning properties. Furthermore, we will examine how feedforward and feedback-related neural processes engage different cortical layers, producing canonical patterns of spiking and synaptic activity as estimated by the analysis of current-source density. These results provide a benchmark for recent studies aiming to examine the profiles of bottom-up and top-down processes with laminar fMRI. Finally, we will highlight particularly useful paradigms and approaches which may help us to understand processing in the different layers of the human cerebral cortex.