Positron Emission Tomography Imaging Reveals Auditory and Frontal Cortical Regions Involved with Speech Perception and Loudness Adaptation

Abstract

Considerable progress has been made in the treatment of hearing loss with auditory implants. However, there are still many implanted patients that experience hearing deficiencies, such as limited speech understanding or vanishing perception with continuous stimulation (i.e., abnormal loudness adaptation). The present study aims to identify specific patterns of cerebral cortex activity involved with such deficiencies. We performed O-15-water positron emission tomography (PET) in patients implanted with electrodes within the cochlea, brainstem, or midbrain to investigate the pattern of cortical activation in response to speech or continuous multi-tone stimuli directly inputted into the implant processor that then delivered electrical patterns through those electrodes. Statistical parametric mapping was performed on a single subject basis. Better speech understanding was correlated with a larger extent of bilateral auditory cortex activation. In contrast to speech, the continuous multi-tone stimulus elicited mainly unilateral auditory cortical activity in which greater loudness adaptation corresponded to weaker activation and even deactivation. Interestingly, greater loudness adaptation was correlated with stronger activity within the ventral prefrontal cortex, which could be up-regulated to suppress the irrelevant or aberrant signals into the auditory cortex. The ability to detect these specific cortical patterns and differences across patients and stimuli demonstrates the potential for using PET to diagnose auditory function or dysfunction in implant patients, which in turn could guide the development of appropriate stimulation strategies for improving hearing rehabilitation. Beyond hearing restoration, our study also reveals a potential role of the frontal cortex in suppressing irrelevant or aberrant activity within the auditory cortex, and thus may be relevant for understanding and treating tinnitus.

Auditory and audio–visual processing in patients with cochlear, auditory brainstem, and auditory midbrain implants: An EEG study

“…Previous studies also revealed areas like the frontal cortex to show changes in activity related to the auditory status. Findings include both, hearing impaired [Campbell and Sharma, ] and auditory implant patients [Berding et al, ], and suggest compensation by and resource allocation to frontal regions, when confronted with diminished auditory input.…”

“…Efforts to understand and improve speech perception in patients with central auditory implants are of utmost importance. To better understand the special requirements for electrical stimulation, previous radiotracer imaging studies exploring the cortical response patterns in CI, ABI, and AMI patients could show bilateral recruitment of the auditory cortex to speech and non‐speech sounds in all groups of patients [Berding et al, ; Coez et al, ; Miyamoto et al, ; Miyamoto and Wong, ; Di Nardo et al, ]. First studies have proven the feasibility of recordings of electrically evoked auditory brainstem, mid‐latency and cortical auditory responses in ABI [He et al, ; Herrmann et al, ; O'Driscoll et al, ] and AMI patients [Colletti et al, ].…”

Early cortical metabolic rearrangement related to clinical data in idiopathic sudden sensorineural hearing loss

“…Regarding this, up to now, neither neuroimaging studies have been implemented in the very first hours of the disease nor have metabolic techniques been used in order to discover possible ISSNHL-related cortical changes. In fact -amongst others -studies of the auditory system during ISSNHL have been conducted exclusively by means of MRI-related techniques (Berding et al, 2015;Boyen et al, 2013;Fan et al, 2015;Yang et al, 2014).…”

“…Starting from the 1980s, [ 18 F]fluorodeoxyglucose (FDG) positron emission tomography (PET)/computer tomography (CT) has been used as a valuable tool for functional neuroanatomy imaging (Berding et al, 2015;Frackowiak and Friston, 1994) and many studies consider that it offers considerable advantages when studying the auditory system (Berding et al, 2015;Talavage et al, 2014). In fact, it has been demonstrated as a quiet and reliable imaging technique for overcoming possible unintended sensory stimulations (Alessandrini et al, 2014a(Alessandrini et al, , 2016Benjamin et al, 2010;Gaab et al, 2008).…”

Imaging in hearing using radiotracers

“…in studies of loudness adaptation, a phenomenon observed in auditory implant users, which is characterized by a loss of loudness perception with a continuous multi-tone stimulus after a particular time period. The phenomenon is associated with lacking activation in auditory regions and additional activation in networks of auditory processing including the ventral frontal cortex [9]. These correlates of deficient processing cannot be observed if e.g.…”