Semantic encoding during language comprehension at single-cell resolution

Mohsen Jamali, Benjamin Grannan, Jing Cai, Arjun R. Khanna, William Muñoz, Irene Caprara, Angelique C. Paulk, Sydney S. Cash, Evelina Fedorenko and Ziv M. Williams ()
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Mohsen Jamali: Harvard Medical School
Benjamin Grannan: Harvard Medical School
Jing Cai: Harvard Medical School
Arjun R. Khanna: Harvard Medical School
William Muñoz: Harvard Medical School
Irene Caprara: Harvard Medical School
Angelique C. Paulk: Harvard Medical School
Sydney S. Cash: Harvard Medical School
Evelina Fedorenko: Massachusetts Institute of Technology
Ziv M. Williams: Harvard Medical School

Nature, 2024, vol. 631, issue 8021, 610-616

Abstract: Abstract From sequences of speech sounds1,2 or letters3, humans can extract rich and nuanced meaning through language. This capacity is essential for human communication. Yet, despite a growing understanding of the brain areas that support linguistic and semantic processing4–12, the derivation of linguistic meaning in neural tissue at the cellular level and over the timescale of action potentials remains largely unknown. Here we recorded from single cells in the left language-dominant prefrontal cortex as participants listened to semantically diverse sentences and naturalistic stories. By tracking their activities during natural speech processing, we discover a fine-scale cortical representation of semantic information by individual neurons. These neurons responded selectively to specific word meanings and reliably distinguished words from nonwords. Moreover, rather than responding to the words as fixed memory representations, their activities were highly dynamic, reflecting the words’ meanings based on their specific sentence contexts and independent of their phonetic form. Collectively, we show how these cell ensembles accurately predicted the broad semantic categories of the words as they were heard in real time during speech and how they tracked the sentences in which they appeared. We also show how they encoded the hierarchical structure of these meaning representations and how these representations mapped onto the cell population. Together, these findings reveal a finely detailed cortical organization of semantic representations at the neuron scale in humans and begin to illuminate the cellular-level processing of meaning during language comprehension.

Date: 2024
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DOI: 10.1038/s41586-024-07643-2

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