Intracranial Mapping of Response Latencies and Task Effects for Spoken Syllable Processing in the Human Brain

Abstract

Prior lesion, noninvasive-imaging, and intracranial-electroencephalography (iEEG) studies have documented hierarchical, parallel, and distributed characteristics of human speech processing. Yet, there have not been direct, intracranial observations of the latency with which regions outside the temporal lobe respond to speech, or how these responses are impacted by task demands. We leveraged human intracranial recordings via stereo-EEG to measure responses from diverse forebrain sites during (i) passive listening to /bi/ and /pi/ syllables, and (ii) active listening requiring /bi/-versus-/pi/ categorization. We find that neural response latency increases from a few tens of ms in Heschls gyrus (HG) to several tens of ms in superior temporal gyrus (STG), superior temporal sulcus (STS), and early parietal areas, and hundreds of ms in later parietal areas, insula, frontal cortex, hippocampus, and amygdala. These data also suggest parallel flow of speech information dorsally and ventrally, from HG to parietal areas and from HG to STG and STS, respectively. Latency data also reveal areas in parietal cortex, frontal cortex, hippocampus, and amygdala that are not responsive to the stimuli during passive listening but are responsive during categorization. Furthermore, multiple regions--spanning auditory, parietal, frontal, and insular cortices, and hippocampus and amygdala--show greater neural response amplitudes during active versus passive listening (a task-related effect). Overall, these results are consistent with hierarchical processing of speech at a macro level and parallel streams of information flow in temporal and parietal regions. These data also reveal regions where the speech code is stimulus-faithful and those that encode task-relevant representations. New & NoteworthyWe leverage direct, intracranial electroencephalography recordings to document speech information flow through diverse sites in the human forebrain, including areas where reported electrode coverage has historically been limited. Our data are consistent with hierarchical processing of speech at a macro level and parallel streams of information flow in temporal and parietal regions. They also reveal regions in the auditory pathway where stimulus-faithful speech codes are transformed to behaviorally relevant representations of speech content.