Air-conducted ultrasound below the hearing threshold elicits functional changes in the cognitive control network

Abstract

Air-conducted ultrasound (> 17.8 kHz; US) is produced by an increasing number of technical devices in our daily environment. While several studies indicate that exposure to US in public spaces can lead to subjective symptoms such as ‘annoyance’ or ‘difficulties in concentration’, the effects of US on brain activity are poorly understood. In the present study, individual hearing thresholds (HT) for sounds in the US frequency spectrum were assessed in 21 normal-hearing participants. The effects of US were then investigated by means of functional magnetic resonance imaging (fMRI). 15 of these participants underwent three resting-state acquisitions, two with a 21.5 kHz tone presented monaurally at 5 dB above (ATC) and 10 dB below (BTC) the HT and one without auditory stimulation (NTC), as well as three runs of an n-back working memory task involving similar stimulus conditions (n-ATC, n-BTC, n-NTC). Comparing data gathered during n-NTC vs. fixation, we found that task performance was associated with the recruitment of regions within the cognitive control network, including prefrontal and parietal areas as well as the cerebellum. Direct contrasts of the two stimulus conditions (n-ATC & n-BTC) vs. n-NTC showed no significant differences in brain activity, irrespective of whether a whole-brain or a region of interest approach with primary auditory cortex as the seed was used. Likewise, no differences were found when the resting-state runs were compared. However, contrast analysis (n-BTC vs. n-ATC) revealed a strong activation in bilateral inferior frontal gyrus (IFG, triangular part) only when US was presented below the HT (p < 0.001, cluster > 30). In addition, IFG activation was also associated with faster reaction times during n-BTC (p = 0.033) as well as with verbal reports obtained after resting-state, i.e., the more unpleasant sound was perceived during BTC vs. ATC, the higher activation in bilateral IFG was and vice versa (p = 0.003). While this study provides no evidence for activation of primary auditory cortex in response to audible US (even though participants heard the sounds), it indicates that US can lead to changes in the cognitive control network and affect cognitive performance only when presented below the HT. Activation of bilateral IFG could reflect an increase in cognitive demand when focusing on task performance in the presence of slightly unpleasant and/or distracting US that may not be fully controllable by attentional mechanisms.