BACKGROUND: The annual James Arthur lecture series on the Evolution of the Human Brain was inaugurated at the American Museum of Natural History in 1932, through a bequest from a successful manufacturer with a particular interest in mechanisms. Karl Pribram's thirty-ninth lecture of the series, delivered in 1970, was a seminal event that heralded much of the research agenda, since pursued by representatives of diverse disciplines, that touches on the evolution of human uniqueness. DISCUSSION: In his James Arthur lecture Pribram raised questions about the coding of information in the brain and about the complex association between language, symbol, and the unique human cognitive system. These questions are as pertinent today as in 1970. The emergence of modern human symbolic cognition is often viewed as a gradual, incremental process, governed by inexorable natural selection and propelled by the apparent advantages of increasing intelligence. However, there are numerous theoretical considerations that render such a scenario implausible, and an examination of the pattern of acquisition of behavioral and anatomical novelties in human evolution indicates that, throughout, major change was both sporadic and rare. What is more, modern bony anatomy and brain size were apparently both achieved well before we have any evidence for symbolic behavior patterns. This suggests that the biological substrate underlying the symbolic thought that is so distinctive of Homo sapiens today was exaptively achieved, long before its potential was actually put to use. In which case we need to look for the agent, perforce a cultural one, that stimulated the adoption of symbolic thought patterns. That stimulus may well have been the spontaneous invention of articulate language.