Distinct cortical encoding of acoustic and electrical cochlear stimulation

Abstract

Cochlear implants are neuroprosthetic devices that restore hearing and speech comprehension to profoundly deaf humans and represent an exemplar application of biomedical engineering and research to clinical conditions. However, the utility of these devices in many subjects is limited, largely due to lack of information about how neural circuits respond to implant stimulation. Recently we showed that deafened rats can use cochlear implants to recognize sounds, and that this training refined the responses of single neurons in the primary auditory cortex. Here we asked how local populations of cortical neurons represent acute implant stimuli, using electrode arrays we developed for cortical surface recordings for micro-electrocorticography ({micro}ECoG), a form of intracranial electroencephalography (iEEG). We found that there was a coarse, non-random spatial organization with limited evidence for consistent, sharply graded cochleotopy across recording sites, relative to a clearer tonotopic spatial representation in normal-hearing rats. Single-trial iEEG responses to acoustic inputs were more reliable than responses to cochlear implant stimulation, although stimulus identity could be successfully decoded in both cases. However, the spatio-temporal response profiles to acoustic vs cochlear implant stimulation were substantially different. Decoders trained on acoustic responses showed essentially zero information transfer when tested on electrical stimulation responses in the same animals after deafening and cochlear implant stimulation. Thus, while acute cochlear implant stimulation evoked spatially non-random cortical activity with coarse cochleotopic structure, the dynamics of network activity were substantially different from those evoked by acoustic stimulation, with possible implications for perceptual similarity that remain to be tested.