Parallel encoding of speech in human frontal and temporal lobes

Models of speech perception are centered around a hierarchy in which auditory representations in the thalamus propagate to primary auditory cortex, then to the lateral temporal cortex, and finally through lateral cortical areas to reach the frontal lobe. However, it is unclear if speech-evoked activity in frontal cortex strictly reflects downstream processing from this hierarchical pathway or whether there are long-range parallel connections from the low-level areas (thalamus, primary auditory cortex) to the frontal lobe. Here, we used high-density direct cortical recordings, high-resolution diffusion tractography, and hemodynamic functional connectivity to evaluate for evidence of direct parallel inputs to frontal cortex from low-level areas. We found that neural populations in the frontal lobe show speech-evoked responses that are synchronous with the shortest-latency responses in the superior temporal gyrus (STG) and encode spectrotemporal speech content indistinguishable from spectrotemporal encoding patterns observed in the STG. Additionally, we find white matter tractography and functional connectivity patterns that connect the auditory nucleus of the thalamus and the primary auditory cortex to the frontal lobe. Together, these results support the existence of robust long-range parallel inputs from low-level auditory areas to apical areas in the frontal lobe of the human speech network.