Brain-environment synchrony and the auditory perception problem

Project Information

BRAINSYNC

Grant agreement ID: 804029

DOI

10.3030/804029

Project closed

EC signature date 29 October 2018

Start date 1 April 2019

End date 31 March 2024

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 1 500 000,00

EU contribution

€ 1 500 000,00

Coordinated by

MAX-PLANCK-GESELLSCHAFT ZUR FORDERUNG DER WISSENSCHAFTEN EV
Germany

Periodic Reporting for period 4 - BRAINSYNC (Brain-environment synchrony and the auditory perception problem)

Reporting period: 2023-10-01 to 2024-03-31

Summary of the context and overall objectives of the project

Auditory perception is at the very root of our human ability to communicate – without the ability to make sense of the auditory world, we would be unable to understand speech or to enjoy music. One feature of the auditory environment that has important implications for the neural processing of sound is that sounds necessarily evolve over time. What’s more, the information-carrying fluctuations of loudness or pitch that characterize sounds often convey rhythmic structure. In turn, rhythmic neural activity synchronizes with the rhythmic structure of sounds. The fidelity of brain–environment synchronization predicts important aspects of our ability to process features of the auditory environment. However, we are currently lacking a mechanistic understanding of why and how brain–environment synchrony might fail, leading to deficits in auditory perception that may take a toll on quality of life in older age.

This research program seeks to characterize the properties of neural oscillators – brain regions and networks that produce oscillatory neural activity – that predict the fidelity of brain–environment synchrony and success in real-world listening situations. Moreover, the work seeks to pioneer investigations into the possibility of noninvasive brain stimulation as an intervention. Overall, the research program has the potential to improve quality of life and social health of many aging adults who struggle with auditory perception, whether or not they present with hearing loss.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

A major success of the work was to develop new behavioral measures of preferred rate and flexibility. We have developed and established the test–retest reliability of four novel measures of preferred rate; all measures have been collected alongside a classical measure of preferred rate referred to as “spontaneous motor tempo” (SMT) measure so that we can compare our novel measures to classical, albeit unidimensional, SMT measures. We pared down and combined our newly tested preferred rate measures into a streamlined test that has been made available for public use. Moreover, we have developed and validated an efficient behavioral test of oscillator flexibility across seven different experiments, conducted both in-lab and online, and using different response modalities. Critically, we found that flexibility was the most important parameter that decreased with age and contributed to failures interacting with auditory rhythms. We are aware of several other labs internationally that have begun to use our published paradigm in their own work.

Our work revealed that oscillator flexibility is a critical aspect of neural oscillators that is reduced gradually with advancing age; decreases in flexibility led to deteriorating performance both listening to auditory rhythms and producing rhythmic behaviors. This is a novel finding that suggests more attention should be paid to how a system adapts in response to a dynamically changing auditory environment, rather than just how strongly brain rhythms synchronize with the environment under undemanding listening conditions. We also laid important groundwork demonstrating that noninvasive brain stimulation can modulate brain–environment synchrony – brain stimulation was not able to "push around" the brain rhythm's temporal relation to the sound, but was able to increase or decrease entrainment strength via constructive and destructive interference with the auditory rhythm, respectively. We used noninvasive brain stimulation to probe the preferred rates of individual auditory oscillators, and demonstrated that brain–environment synchrony is most successful when the environmental rhythm matches the neural rhythm's preference.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

No work to date had examined the extent to which brain–environment synchrony is stable, or reliable, from day to day. This is despite calls for using rhythmic auditory or electrical stimulation as an intervention to interfere with or improve brain–environment synchrony, which hinges on having a stable target. We showed strong reliability of both the behavioral and neural measures of brain–environment synchrony. The demonstration that brain–environment synchrony is reliable over days and weeks is absolutely critical to establish prior to attempting to use a noninvasive brain stimulation technique to interfere with entrainment.

We also conducted a multi-session study where we acquired two special types of structural brain images as well as functional images using magnetic resonance imaging (MRI); functional data were acquired while participants performed the core task. Using these structural and functional data, we used advanced modeling techniques to simulate how electric field travels through the skin, skull, cerebrospinal fluid, and brains of each individual listener, given their own personal anatomy. From these simulations, we determined the optimal positioning of the electrodes that we use to apply electrical current using transcranial alternating current stimulation (tACS) to interfere with task performance. We compared this group of participants to another group for which we used a standard out-of-the-box electrode placements. The results indicated that tACS was capable of modulating brain–environment synchrony, but not "rewriting" what the brain was naturally doing. This demonstrates that tACS can reliably be used to increase the strength of brain–environment synchrony. Although the two participant groups with different electrode montages did not differ significantly in terms of the strength of tACS effects, using individual montages reduced inter-individual variability, which is crucial given the weak and highly variable nature of tACS effects in the literature. We conducted post-hoc electric field modeling to try to predict the strength of tACS effects on an individual-by-individual basis based on how much electric field was getting where. We determined that, unsurprisingly, maximizing electric field to the target brain region, but perhaps surprisingly, simultaneously minimizing the amount of electric field that reaches non-target regions, explained how well tACS worked to modulate an individual's behavior. These breakthroughs are critical going forward for understanding how to maximize the effects of noninvasive brain stimulation in humans.

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