EEG Manifestations of Phonemic Processing in Severe Brain Injury

Low-level language processing in brain-injured patients

Parul Jain, Mary M. Conte, Henning U. Voss, Jonathan D. Victor, and Nicholas D. Schiff

Brain Communications 5, fcad094 doi: 10.1093/braincomms/fcad094 (2023)

Abstract

Assessing cognitive function – especially language processing – in severely brain-injured patients is critical for prognostication, care, and development of communication devices (e.g., brain-computer interfaces).

In patients with diminished motor function, language processing has been probed using EEG measures of command following in motor imagery tasks. While such tests eliminate the need for a motor response, they require sustained attention. However, passive listening tasks, along with an EEG response measure, can reduce both the motor and attentional demands. These considerations motivated the development of two assays of low-level language processing – identification of differential phoneme-class responses (DPR) and tracking of the natural speech envelope (NSE).

This cross-sectional study looks at a cohort of 26 severely brain-injured patient subjects and 10 healthy controls. Patients’ level of function was assessed via the Coma Recovery Scale – Revised (CRS-R) at bedside, and all patient subjects were also tested for command following via EEG and/or MRI assays of motor imagery. For the DPR and NSE assays, EEG was recorded during presentation of a 148 s audio clip of Alice in Wonderland. Time-locked EEG responses to phoneme classes were extracted. Tracking of NSE was assessed from the same recordings, and was measured by cross-correlating the EEG response with the speech envelope. In healthy controls, the dynamics of the two measures were temporally similar but spatially different: a central parieto-occipital DPR component was absent in the NSE tracking response.

The DPR was present in all patient subjects, including the six classified as vegetative state/unresponsive wakefulness syndrome by behavioral assessment. However, patient subjects with evidence of language processing either by behavioral assessment or via motor imagery tests had an early bilateral response in the first 50 ms that was lacking in patient subjects without any evidence of language processing.

The NSE tracking response was also present in all patient subjects, and responses in the first 100 ms distinguished patient subjects with evidence of language processing. Specifically, patient subjects with evidence of language processing had a more global response in the first 100 ms whereas those without evidence of language processing had a frontopolar response in the first 100 ms.

In summary, we developed two passive EEG-based methods to probe low-level language processing in severely brain-injured patients. In our cohort, both assays showed a difference between patient subjects with evidence of command following and those with no evidence of command following: a more prominent early bilateral response component.


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