Hight Ariel Edward, Insanally Michele N, Scarpa Julia K, Cheng Yew-Song, Trumpis Michael, Viventi Jonathan, Svirsky Mario A, Froemke Robert C
Translational Neuroscience Institute, New York University Grossman School of Medicine, New York, NY 10016.
Department of Otolaryngology-Head and Neck Surgery, New York University Grossman School of Medicine, New York, NY 10016.
bioRxiv. 2025 Aug 1:2025.08.01.668170. doi: 10.1101/2025.08.01.668170.
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 (μECoG), a form of intracranial electroencephalography (iEEG). We found that there was a limited tonotopic organization 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 might activate the auditory cortex in a cochleotopic manner, the dynamics of network activity are quite distinct, suggesting that pitch percepts from acoustic and electrical stimulation are fundamentally different.
人工耳蜗是一种神经假体装置，可恢复极重度聋人的听力和言语理解能力，是生物医学工程与研究在临床应用中的一个典范。然而，这些装置在许多受试者中的效用有限，这主要是由于缺乏关于神经回路如何对植入物刺激作出反应的信息。最近我们发现，致聋大鼠能够使用人工耳蜗识别声音，并且这种训练改善了初级听觉皮层中单个神经元的反应。在这里，我们使用我们开发的用于皮层表面记录的电极阵列进行微脑电图（μECoG，一种颅内脑电图（iEEG）形式），来研究皮层神经元的局部群体如何表征急性植入物刺激。我们发现，相对于听力正常大鼠中更清晰的音调空间表征，记录位点之间的音调组织有限。对声音输入的单次试验iEEG反应比对人工耳蜗刺激的反应更可靠，尽管在这两种情况下都可以成功解码刺激特征。然而，对声音与人工耳蜗刺激的时空反应模式有很大不同。在声音反应上训练的解码器，在致聋和人工耳蜗刺激后的同一动物中对电刺激反应进行测试时，显示出基本为零的信息传递。因此，虽然急性人工耳蜗刺激可能以耳蜗拓扑方式激活听觉皮层，但网络活动的动态变化非常不同，这表明来自声音和电刺激的音高感知在根本上是不同的。
