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

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

Correlations between loudness adaptation and cortical activation during multi-tone complex stimulation.

<p>A deactivation of the auditory cortex was seen in a patient with complete loudness adaptation (Fig 3A). In this patient, a significant (p<0.001) activation of the ventral frontal cortex was observed (Fig 3B). For the entire group, a significant negative correlation (R² = 0.91, p = 0.045) between loudness maintenance at 35–38 sec presentation of the multi-tone complex (abscissa; taken from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0128743#pone.0128743.g001" target="_blank">Fig 1</a>) and the extent of frontal cortex activation (ordinate; voxels in BA 9 and 10) was observed (Fig 3C). For loudness maintenance at 180 sec, a similar but non-significant trend (R² = 0.80, p = 0.106) was also observed (Fig 3D)</p

Correlation between speech understanding and extent of auditory cortex activation during speech stimulation.

<p>A CI user with good speech understanding (82%) exhibited large bilateral auditory cortex activation (Fig 2A), whereas an AMI user with poor speech understanding (5%) exhibited relatively small activated areas (Fig 2B). For the entire group, a significant correlation (R² = 0.80, p = 0.042) between speech understanding (speech score) and extent of auditory cortex activation was observed for voxels within BA 41, 42, 22 and 21 (i.e., temporal voice area) (Fig 2C). A stronger significant correlation (R² = 0.97, p = 0.002) was observed when plotting voxels only within BA 41 and 42 (Fig 2D).</p

Time course of loudness adaptation in auditory implant users.

<p>Ordinate displays the percentage relative to comfortable loudness that is maintained over time (in seconds along the abscissa) in response to continuous multi-tone complex stimulation. Speech perception scores for each implant user taken from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0128743#pone.0128743.t001" target="_blank">Table 1</a> are listed in the legend to the right of the figure.</p