There are significant structural and functional differences between primate calls and human speech. In addition, these two forms of vocal communication appear to largely depend on nonhomologous brain structures. However, an analysis of the underlying axonal circuitry of these brain systems suggests that there are significant interrelationships between them, both in functional and in evolutionary terms. Based on both primate neuroanatomical studies and human in vivo mapping studies it is argued that the ventral prefrontal area is the critical link, both functionally and anatomically between these distinct vocal systems. A model of human brain evolution with respect to language is proposed in which limbic-midbrain vocalization circuits became progressively subordinated to the activity of prefrontal-midbrain and frontal-motor circuits for regulating facial gesture, skilled oral food manipulation, and conditional association learning.Quantitative and developmental data are used to suggest that this resulted from the relative enlargement of prefrontal areas and the consequences this has on the relative proportions of different cortico-midbrain and diencephalic-midbrain projections. Although humans exhibit a significantly reduced call repertoire, it is argued that the display-vocalization circuits that play the central role in all other primate communication have neither been eliminated, supplanted nor suppressed by language systems. They have instead become integrated into the more distributed language circuits and play a ubiquitous though subordinate role in all normal language processes.