Altered cortical and subcortical connectivity due to infrasound administered near the hearing threshold – Evidence from fMRI
The question, whether infrasound (IS; sound in the very low-frequency range – 1 Hz < frequency < 20 Hz) can pose a threat to physical and mental well-being remains a much debated topic. For decades, it has been a widely held view that IS frequencies are too low to be processed by the auditory system, since the human hearing range is commonly quoted to only span frequencies from about 20 to 20000 Hz. This view was supported by a number of studies conducted in animals as well as in humans demonstrating that the auditory system is equipped with several shunting and attenuation mechanisms, which are already involved in early stages of signal processing and make hearing at low frequencies quite insensitive. However, the notion that IS cannot be processed within the auditory system has been contested by several studies, in which IS-induced changes of cochlear function in animals as well as in normally hearing human participants) have been documented. In fact, it has been shown repeatedly that IS can also be perceived by humans, if administered at very high sound pressure levels (SPLs)). More recently, two fMRI studies also revealed that exposure to a monaurally presented 12-Hz IS tone with SPLs of > 110 dB led to bilateral activation of the superior temporal gyrus (STG), which suggests that the physiological mechanisms underlying IS perception may share similarities with those involved in ‘normal hearing’, even at the stage of high-level cortical processing.
Meanwhile, there seems to be a growing consensus that humans are indeed receptive to IS and that exposure to low-frequency sounds (including sounds in the IS frequency spectrum) can give rise to high levels of annoyance and distress. However, IS also came under suspicion of promoting the formation of several full-blown medical symptoms ranging from sleep disturbances, headache and dizziness, over tinnitus and hyperacusis, to panic attacks and depression, which have been reported to occur more frequently in people living close to wind parks. While it has been established that noise produced by wind turbines can indeed have a considerable very low-frequency component, IS emission only reaches SPL-maxima of around 80 to 90 dB, which may not be high enough to exceed the threshold for perception. Taking into consideration such results, Leventhall thus concluded that “if you cannot hear a sound and you cannot perceive it in other ways and it does not affect you”. Importantly, this view also resonates well with the current position of the World Health Organisation (WHO), according to which “there is no reliable evidence that infrasounds below the hearing threshold produce physiological or psychological effects”. However, it appears that the notion, according to which sound needs to be perceived in order to exert relevant effects on the organism, falls short when aiming at an objective risk assessment of IS, especially if one takes into consideration recent advances in research on inner ear physiology as well as on the effects of subliminal auditory stimulation (i.e. stimulation below the threshold of perception). For example, 5-Hz IS exposure presented at SPLs as low as 60–65 dB has been shown to trigger the response of inner ear components such as the outer hair cells in animals and it has been suggested that outer hair cell stimulation may also exert a broader influence on the nervous system via the brainstem. In addition, there is the well documented effect in cognitive science that brain physiology and behavior can be influenced by a wide range of subliminally presented stimuli, including stimuli of the auditory domain.
We therefore set out to address the question, whether IS near the hearing threshold can also exert an influence on global brain activity and whether the effects of stimulation significantly differ from those induced by supra-threshold IS. …
Regional homogeneity analysis: In summary, it could be demonstrated that prolonged supra-threshold IS stimulation clearly perceived by all participants did not result in statistically significant activations anywhere in the brain. In contrast, near-threshold stimulation led to higher local connectivity in multiple brain areas, compared to both the no-tone as well as the supra-threshold condition. …
Independent component analysis: Decreased functional connectivity – as compared to the no-tone condition – was found during resting state with near-threshold tone presentation in the right amygdala (rAmyg) in the sensorimotor network. Resting state sessions with near-threshold tone presentation were associated with increased functional connectivity in the right superior frontal cortex in the left executive control network when compared to the no-tone condition. In addition, there was increased functional connectivity in the lobule IV and V of the left cerebellum in the default mode networks for near-threshold sessions compared to supra-threshold ones. …
The results of the present study can be summed up in the following way: Prolonged IS exposure near the participants’ individual hearing threshold led to higher local connectivity in three distinct brain areas – rSTG, anterior cingulate cortex (ACC) and rAmyg – while no such effect was observed for stimulation above the hearing threshold. Our data also show that near-threshold IS was associated with connectivity changes on the network level, emphasizing the role of the rAmyg in IS processing. To our knowledge, this study is the first to demonstrate not only that near-threshold IS produces physiological effects, but that the neural response involves the activation of brain areas that are important [not only] for auditory processing but also for emotional and autonomic control. These findings thus allow us to reflect on how (sub)-liminal IS could give rise to a number of physiological as well as psychological health issues, which until now have only been loosely attributed to noise exposure in the low- and very low-frequency spectrum. …
The ACC is generally regarded as a key player in the monitoring and resolution of cognitive, as well as emotional conflicts. Interestingly, a recent meta-analysis by Meneguzzo et al. also revealed that the ACC reliably exhibits activation in response to both sub- as well as supraliminally presented arousing stimuli, which led the authors to suggest that this brain area may function as a gateway between automatic (‘pre-attentive’) affective states and higher order cognitive processes, particularly when affect and cognition are in conflict. In addition, the authors explicitly gave credit to the fact that the term ‘conflict’ may also include unexpected perturbations of the body’s physiology in the absence of conscious awareness. Moreover, another line of research also highlights the ACC’s involvement in autonomic control via its extensive connections with the insula, prefrontal cortex, amygdala, hypothalamus and the brainstem. ACC activation in response to near-threshold IS stimulation could therefore be interpreted as a conflict signaling registration of the stimulus which, if not resolved, may lead to changes of autonomic function.
Similarly, the amygdala is well know for its involvement in emotional processing, especially with respect to fear conditioning, but also in the broader context of stress- and anxiety-related psychiatric disorders. Several studies have documented activation of the amygdala in response to aversive sensory stimuli across different modalities, such as odorants, tastes, visual stimuli, as well as in response to emotional vocalization and unconditioned sounds that are experienced as aversive. Activation of the rAmyg during near-threshold IS exposure may be of particular interest for a risk assessment regarding IS, because the amygdala is known to be involved in auditory processing and may also play a major role in debilitating tinnitus and hyperacusis. It is a fairly established finding that auditory input can be processed along two separate neural pathways, the classical (lemniscal) and the non-classical (extralemniscal) pathway. While signals travelling along the classical pathway are relayed via ventral thalamic nuclei mostly to the primary auditory cortex, signals traveling along the non-classical pathway are bypassing the primary auditory cortex as dorsal thalamic nuclei project to secondary- and association cortices and also to parts of the limbic structure such as the amygdala. Importantly, the non-classical pathway (frequently called the ‘low route’) allows for direct subcortical processing of the stimulus in the amygdala, without the involvement of cortical areas and may therefore play a crucial role in the subliminal registration of ‘biologically meaningful’ stimuli, such as near-threshold IS. In fact, it has been suggested that in certain forms of tinnitus, activation of the non-classical pathway can mediate fear without conscious control and, via its connections to the reticular formation, also exert influences on wakefulness and arousal. … Interestingly, it could be shown that the left amygdala decodes the arousal signaled by the specific stimulus (linked to a conscious fear response), whereas the rAmyg provides a global level of autonomic activation triggered automatically by any arousing stimulus (linked to a subconscious fear response). It is particularly noteworthy that while the rAmyg exhibited increased local connectivity in response to near-threshold IS, independent component analysis revealed a decoupling of the rAmyg from the sensorimotor network in comparison to the no-tone condition. It has been repeatedly argued that decoupling of the amydgala from areas involved in executive control may enable an organism to sustain attention and supports working memory, thus potentially aiding cognitive control processes in the aftermath of stress. Interestingly, the fact that functional connectivity of the rSFG was higher during near-threshold stimulation further substantiates this claim. Again, several studies demonstrate that rSFG and rAmyg share functional connections and that activity between the two regions tends to be negatively correlated. Thus, participants who were left guessing whether stimulation occurred, may have engaged in effortful regulation of affect, trying to minimize the consequences of stress on cognitive control networks.
Finally, our results also allow us to draw some preliminary conclusions on potential long-term health effects associated with (sub-)liminal IS stimulation. It has been reported in several studies that sustained exposure to noise can lead to an increase of catecholamine- and cortisol levels. In addition, changes of bodily functions, such as blood pressure, respiration rate, EEG patterns and heart rate have also been documented in the context of exposure to below- and near-threshold IS. We therefore suggest that several of the above mentioned autonomic reactions could in fact be mediated by the activation of brain areas such as the ACC and the amygdala. While increased local connectivity in ACC and rAmyg may only reflect an initial bodily stress response towards (sub-)liminal IS, we speculate that stimulation over longer periods of time could exert a profound effect on autonomic functions and may eventually lead to the formation of symptoms such as sleep disturbances, panic attacks or depression, especially when additional risk factors, such as an increased sensibility towards noise, or strong expectations about the harmfulness of IS are present.
Markus Weichenberger, Martin Bauer, Robert Kühler, Johannes Hensel, Caroline Garcia Forlim, Albrecht Ihlenfeld, Bernd Ittermann, Jürgen Gallinat, Christian Koch, and Simone Kühn
Department of Psychiatry and Psychotherapy, Charité-Universitätsmedizin Berlin; Physikalisch-Technische Bundesanstalt, Braunschweig and Berlin; and University Clinic Hamburg-Eppendorf, Clinic and Policlinic for Psychiatry and Psychotherapy, Hamburg, Germany
PLoS One. Published: April 12, 2017. doi: 10.1371/journal.pone.0174420
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