Resilience and vulnerability of speech neural tracking to early auditory deprivation

Infants are born with biologically constrained biases that favor language acquisition. One is the auditory system’s ability to track the envelope of continuous speech. However, to what extent the synchronization between brain activity and this pivotal speech feature relies on postnatal auditory experience remains unknown. To uncover this, we studied individuals with or without access to functional hearing in the first year of life after they received cochlear implants (CIs) for hearing restoration. We measured the neural synchronization with continuous speech envelope in children with congenital bilateral profound deafness (CD; minimum auditory deprivation 11 months) or who acquired profound deafness later in development (AD; minimum auditory experience after birth 12 months), as well as in hearing controls (HC). Speech envelope tracking was unaffected by the absence of auditory experience in the first year of life. At short timescales, neural tracking had a similar magnitude in CI users and HC. However, in CI users, it was substantially delayed, and its timing depended on the age of hearing restoration. Conversely, we observed alterations at longer timescales, possibly accounting for the comprehension deficits observed in children with CI. These findings highlight (i) the resilience of sensory components of speech envelope tracking to the lack of hearing in the first year of life, supporting its strong biological bias, (ii) the crucial role of when functional hearing restoration takes place in mitigating the impact of atypical auditory development, (iii) the vulnerability of higher hierarchical levels of speech- envelope tracking in CI users. Neural tracking of continuous speech could provide biomarkers along the processing hierarchy between sensory and core linguistic operations, even after cochlear implantation.