We investigated the brain systems engaged during propositional speech (PrSp) and two forms of non- propositional speech (NPrSp): counting and reciting overlearned nursery rhymes. Bilateral cerebral and cerebellar regions were involved in the motor act of articulation, irrespective of the type of speech. Three additional, left-lateralized regions, adjacent to the Sylvian sulcus, were activated in common: the most posterior part of the supratemporal plane, the lateral part of the pars opercularis in the posterior inferior frontal gyrus and the anterior insula. Therefore, both NPrSp and PrSp were dependent on the same discrete subregions of the anatomically ill-defined areas of Wernicke and Broca. PrSp was also dependent on a predominantly left-lateralized neural system distributed between multi-modal and amodal regions in posterior inferior parietal, anterolateral and medial temporal and medial prefrontal cortex. The lateral prefrontal and paracingulate cortical activity observed in previous studies of cued word retrieval was not seen with either NPrSp or PrSp, demonstrating that normal brain- language representations cannot be inferred from explicit metalinguistic tasks. The evidence from this study indicates that normal communicative speech is dependent on a number of left hemisphere regions remote from the classic language areas of Wernicke and Broca. Destruction or disconnection of discrete left extrasylvian and perisylvian cortical regions, rather than the total extent of damage to perisylvian cortex, will account for the qualitative and quantitative differences in the impaired speech production observed in aphasic stroke patients.