Direct Recordings from the Auditory Cortex in a Cochlear Implant User

Abstract

Electrical stimulation of the auditory nerve with a cochlear implant (CI) is the method of choice for treatment of severe-to-profound hearing loss. Understanding how the human auditory cortex responds to CI stimulation is important for advances in stimulation paradigms and rehabilitation strategies. In this study, auditory cortical responses to CI stimulation were recorded intracranially in a neurosurgical patient to examine directly the functional organization of the auditory cortex and compare the findings with those obtained in normal-hearing subjects. The subject was a bilateral CI user with a 20-year history of deafness and refractory epilepsy. As part of the epilepsy treatment, a subdural grid electrode was implanted over the left temporal lobe. Pure tones, click trains, sinusoidal amplitude-modulated noise, and speech were presented via the auxiliary input of the right CI speech processor. Additional experiments were conducted with bilateral CI stimulation. Auditory event-related changes in cortical activity, characterized by the averaged evoked potential and eventrelated band power, were localized to posterolateral superior temporal gyrus. Responses were stable across recording sessions and were abolished under general anesthesia. Response latency decreased and magnitude increased with increasing stimulus level. More apical intracochlear stimulation yielded the largest responses. Cortical evoked potentials were phaselocked to the temporal modulations of periodic stimuli and speech utterances. Bilateral electrical stimulation resulted in minimal artifact contamination. This study demonstrates the feasibility of intracranial electrophysiological recordings of responses to CI stimulation in a human subject, shows that cortical response properties may be similar to those obtained in normal-hearing individuals, and provides a basis for future comparisons with extracranial recordings.

Rapid bilateral improvement in auditory cortex activity in postlingually deafened adults following cochlear implantation

“…This finding may point to limited cortical adaptation to the implant signal, which confirms the reduced auditory discrimination ability observed in these individuals. Similarly, longer N1 latency and reduced ability to discriminate complex sounds has been previously observed in CI users (Timm et al, 2012), although some CI users may show similar N1 latencies compared with NH listeners (Jordan et al, 1997;Sandmann et al, 2009), in particular after long history of CI use (Nourski et al, 2013). It can be speculated that the N1 latency of our participants reduced beyond one year of CI use.…”

Selective Neuronal Activation by Cochlear Implant Stimulation in Auditory Cortex of Awake Primate

“…At high sound levels (Ն60 dB SPL), animals not treated with intrascalar injections of neomycin sulfate had prominent short latency responses Ͻ2.5 ms, likely reflecting the cochlear microphonic and auditory nerve compound action potentials and some degree of residual hearing. High thresholds for response were likely due to electrode insertion trauma and cochlear hair cell loss (Kennedy, 1987;Ni et al, 1992). In all animals, the implanted ear was occluded with ear impression material during neural recording sessions.…”

“…Several PET studies in CI users have shown dominant contralateral activation (Naito et al, 1995;Hirano et al, 1997), although one PET study in CI subjects early after implantation (Ͻ2 months) showed ipsilateral dominance of CI stimulation (Ito et al, 2004). There is evidence that in some users unilateral CI stimulation causes bilateral activation in auditory cortex (Herzog et al, 1991;Limb et al, 2010).…”

“…A number of studies using PET (Fujiki et al, 1999;Giraud et al, 2001;Green et al, 2005;Mortensen et al, 2006) and auditory evoked potentials (Zhang et al, 2010;Sharma et al, 2011) suggest that the extent and strength of cortical activation are associated with CI performance. Naito et al (1997) and Green et al (2005) have shown CI users with poor speech recognition through their device have less activation in auditory association areas than control subjects and CI users with good speech (Naito et al, 1997;Green et al, 2005). Green et al (2005Green et al ( , 2008 showed bilateral cortical activation of good performers, whereas poor performers showed much less (mostly contralateral) activation (Green et al, 2005(Green et al, , 2008.…”

“…Although such perceptual deficits likely have peripheral causes, our understanding of how they impact the central auditory system is limited. The success of a CI relies on the ability of the central auditory system to adequately resolve and process electric stimuli (Middlebrooks et al, 2005;Moore and Shannon, 2009). The observation that CI performance can improve markedly over time after the device is activated also attests to the importance of plasticity and perceptual learning (Wilson et al, 2011;Blamey et al, 2013).…”