LAUSR

Significance The variation of pitch in speech not only creates the intonation for affective communication but also signals different meaning of a word in tonal languages, like Chinese. Due to its subtle and brisk pitch contour distinction between tone categories, the underlying neural processing mechanism is largely unknown. Using direct recordings of the human brain, we found categorical neural responses to lexical tones over a distributed cooperative network that included not only the auditory areas in the temporal cortex but also motor areas in the frontal cortex. Strong causal links from the temporal cortex to the motor cortex were discovered, which provides new evidence of top-down influence and sensory–motor interaction during speech perception. In tonal languages such as Chinese, lexical tone with varying pitch contours serves as a key feature to provide contrast in word meaning. Similar to phoneme processing, behavioral studies have suggested that Chinese tone is categorically perceived. However, its underlying neural mechanism remains poorly understood. By conducting cortical surface recordings in surgical patients, we revealed a cooperative cortical network along with its dynamics responsible for this categorical perception. Based on an oddball paradigm, we found amplified neural dissimilarity between cross-category tone pairs, rather than between within-category tone pairs, over cortical sites covering both the ventral and dorsal streams of speech processing. The bilateral superior temporal gyrus (STG) and the middle temporal gyrus (MTG) exhibited increased response latencies and enlarged neural dissimilarity, suggesting a ventral hierarchy that gradually differentiates the acoustic features of lexical tones. In addition, the bilateral motor cortices were also found to be involved in categorical processing, interacting with both the STG and the MTG and exhibiting a response latency in between. Moreover, the motor cortex received enhanced Granger causal influence from the semantic hub, the anterior temporal lobe, in the right hemisphere. These unique data suggest that there exists a distributed cooperative cortical network supporting the categorical processing of lexical tone in tonal language speakers, not only encompassing a bilateral temporal hierarchy that is shared by categorical processing of phonemes but also involving intensive speech–motor interactions over the right hemisphere, which might be the unique machinery responsible for the reliable discrimination of tone identities.