Humans devote much time to the exchange of memories within the context of shared general and personal semantic knowledge. Our hypothesis was that functional imaging in normal subjects would demonstrate the convergence of speech comprehension and production on high-order heteromodal and amodal cortical areas implicated in declarative memory functions. Activity independent of speech phase (that is, comprehension and production) was most evident in the left and right lateral anterior temporal cortex. Significant activity was also observed in the posterior cortex, ventral to the angular gyri. The left and right hippocampus and adjacent inferior temporal cortex were active during speech comprehension, compatible with mnemonic encoding of narrative information, but activity was significantly less during the overt memory retrieval associated with speech production. Therefore, although clinical studies suggest that hippocampal function is necessary for the retrieval as well as the encoding of memories, the former appears to depend on much less net synaptic activity. In contrast, the retrosplenial/posterior cingulate cortex and the parahippocampal area, which are closely associated anatomically with the hippocampus, were equally active during both speech comprehension and production. The results demonstrate why a severe and persistent inability both to understand and produce meaningful speech in the absence of an impairment to process linguistic forms is usually only observed after bilateral, and particularly anterior, destruction of the temporal lobes, and emphasize the importance of retrosplenial/posterior cingulate cortex, an area known to be affected early in the course of Alzheimer's disease, in the processing of memories during communication.