Human brain function results from continuous activity flowing through specific cells, guided by specific synaptic arrangements. Therefore, determining the architecture and properties of functioning microcircuits is fundamental to understand the brain’s action. However, our current knowledge of human microcircuits is extremely limited, and relies heavily on assumptions from rodent research. Using tissue resected from 13 temporal lobe epilepsy patients, we perform multicellular patch-clamp based microcircuit analysis (n=80 recordings) to characterize synaptic connectivity in the human hippocampal CA3, a fundamental brain region for memory. In contrast to neocortical microcircuits, CA3 synaptic connectivity sparsifies from the rodent to the human hippocampus. Anatomical analysis estimates that the number of inputs per human CA3 pyramidal neuron (~17k) expands only minimally from mice (~13k), and is eclipsed by a dramatic expansion in cell number in the human brain. These findings support the model of CA3 as a broad associative network, with a very different building plan from neocortical recurrent networks. This architecture has important implications for associational memory, and shows optimal storage capacity in network models. Together, our data provide a cross-species characterization of hippocampal microcircuit architecture, and begin to reveal the fundamental building blocks of human brain function.