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

Abstract

Results in studies concerning cortical changes in idiopathic sudden sensorineural hearing loss (ISSNHL) are not homogeneous, in particular due to the different neuroimaging techniques implemented and the diverse stages of ISSNHL studied. Considering the recent advances in state-of-the-art positron emission tomography (PET) cameras, the aim of this study was to gain more insight into the neuroanatomical differences associated with the earliest stages of unilateral ISSNHL and clinical-perceptual performance changes. After an audiological examination including the mean auditory threshold (mean AT), mean speech discrimination score (mean SDS) and Tinnitus Handicap Inventory (THI), 14 right-handed ISSNHL patients underwent brain [F]fluorodeoxyglucose (FDG)-PET within 72 h of the onset of symptoms. When compared to an homogeneous group of 35 healthy subjects by means of statistical parametric mapping, a relative increase in FDG uptake was found in the right superior and medial frontal gyrus as well as in the right anterior cingulate cortex in ISSNHL patients. Conversely, the same group showed a significant relative decrease in FDG uptake in the right middle temporal, precentral and postcentral gyrus as well as in the left posterior cingulate cortex, left lingual, superior, middle temporal and middle frontal gyrus and in the left insula. Regression analysis showed a positive correlation between mean THI and glucose consumption in the right anterior cingulate cortex and a positive correlation between mean SDS and glucose consumption in the left precentral gyrus. The relative changes in FDG uptake found in these brain regions and the positive correlation with mean SDS and THI scores in ISSNHL could possibly highlight new aspects of cerebral rearrangement, contributing to further explain changes in those functions that support speech recognition during the sudden impairment of unilateral auditory input.

Aberrant Functional and Causal Connectivity in Acute Tinnitus With Sensorineural Hearing Loss

“…The AMYG is thought to decode the affective value to the sound perception that is pre-processed, especially in the auditory cortex ( Kumar et al, 2012 ). This is consistent with the findings from previous neuroimaging studies showing that the abnormalities in the AMYG could account for tinnitus and induce chronic depression in tinnitus patients ( Micarelli et al, 2017 ). Activation of the AMYG can augment the central neural plasticity in the auditory cortex ( Froemke and Martins, 2011 ), which could be interpreted as an attempt in conflict monitoring and in informative trace integration coming from sensory error detection, such as those represented by an unexpected auditory input impairment.…”

“…Our study also found that non-auditory associative regions reduced connectivity with the STG, which included the cerebellum, PreCG, and the PoCG. The cerebellum is considered as an important hub in detecting auditory afferent and sound processing (Zhou et al, 2019), as well as plays a critical role in a gating control mechanism (Micarelli et al, 2017). Our finding is in line with this previous study, which shows a reduction of cerebellum activity in acute tinnitus.…”

“…The PreCG is the anatomical location of the primary motor cortex, which is responsible for controlling voluntary motor movement of the body and involved in the executive functioning of response inhibition. This was consistent with a resting state PET study that patients with SSNHL presented Glucose uPTAke reduced in PreCG and suggested PreCG as a vital region in auditory associated events related to word recognition and phonological processing (Micarelli et al, 2017). The disconnection between PreCG and STG may lead to auditory processing functional decline during the acute stage of tinnitus and hearing loss.…”

“…The STG is regarded as a critical region which receives the neuronal projection from auditory pathway (Binder, 2017) and has been reported to be associated with cognitive functions including memory, auditory cognition and semantics (Jackson et al, 2018). Several neurophysiological models related to STG have been raised as being involved in the acute stage of tinnitus and hearing loss (Fan et al, 2015;Micarelli et al, 2017). In addition, hearing loss may lead to a hypofunction of the auditory cortex which consequently presents a decreased FC between the STG and associative regions.…”

Inefficient Involvement of Insula in Sensorineural Hearing Loss

“…Insula neurons have been found to respond directly to acoustic stimuli in a single-cell recording study (Bieser, 1998). Micarelli et al (2017) highlighted hypoperfusion in the insula and auditory cortex in idiopathic sudden SNHL patients, reflecting a “freezing” behavior when auditory deprivation occurred abruptly. The function and structure of the insula were found to be impaired in patients with tinnitus and unilateral hearing loss using resting-state or task-based MRI approaches (Yang et al, 2014).…”