How the brain entrains to musical rhythms.

‘How the brain entrains to musical rhythms’ was asked by our guest lecturer, Anna Katharina Bauer. To figure this out, we must first explore the concept of oscillation. Anna defined an oscillation as: ‘any system which uses periodic fluctuations between two states’ (see, Pikovsky et al., 2003). It could be like a pendulum of a clock, or a spring, or rockers at a concert jumping up and down. An oscillation has 3 key parameters, which are:

  • Amplitude (A): referring to the magnitude of the oscillation.
  • Frequency (f): referring to the number of cycles per unit of time (most of the time it’s in seconds).
  • Phase (Φ): referring to any point on this trajectory can described a phase.

Then, ‘What is a neural oscillation?’ Neural oscillation is very similar to an oscillation which is defined by amplitude, frequency and the phase. That is, ‘neural oscillations reflect periodic fluctuations in neural activity between high and low excitability states (Buzsaki & Draguhn, 2004).’

How do neural oscillations synchronize to external rhythms?

In 1665, a Dutch physicist, Huygens, observed two clocks which were very close together. After a while, he noticed that the pendulums started swinging in synchrony. After moving the clocks apart, they did not synchronize, as they had no natural influences. This explains how the neural oscillations synchronize to external rhythms – entrainment. Three requirements of this effect include:

  • Involvement of a self-sustained oscillator
  • Rhythmic stimulation
  • Synchronization

1

Source: brilliant.org

Entrainment has been observed through many biological systems such as the dancing of the fireflies, and the synchronized chirping of crickets. In humans, we have different kinds of entrainment. According to Dr. Bauer, body entrainment such as dancing with the music, synchronize to our breathing, and the most remarkable one is that our brain can also synchronize. Interestingly, it can be modulated through attentional mechanisms or temporal expectations – this will be explored further later.

How can we measure entrainment?

Once Anna established what entrainment was, she explored the concept of neural entrainment. During her PhD, Anna conducted two experiments which investigated the synchronization of neural oscillations to an external rhythmic stimulation by a phase alignment – neural entrainment. The first focused on temporal dynamics – where the evolution of neural entrainment was characterized through behavioral modulation and recorded EEG. Here, the auditory stimulations were long and short continuous tones, each with a slight gap (10-20ms) inserted at certain phases (see Henry and Obleser, 2012). The first image below indicates the behavior of individual participants as they were required to press a button when they heard the gap.

2

Source: Baeur et al. (2018)

As you can see, the participants were relatively accurate as their button-pressing closely followed the stimulation in a sinusoidal pattern. Interestingly, the participants were more accurate in the long condition – indicating that the more time they had to entrain, the greater the entrainment effects were. The image below indicates the neural activity in the frequency domain as evidence for neural entrainment.

3

Source: Bauer et al. (2018)

Evidently, there are spectral peaks in amplitude at 3Hz (stimulation frequency) and 6Hz (harmonic). This is further supported in the EEG topography images where we can see a frontocentral activation which is most likely projected from the auditory cortex. This indicates a solid measure of neural activity as evidence for neural entrainment. Inter-trial phase coherence within the time-frequency domain also evidences neural entrainment.

The second measure is called phase consistency, which is simply a measure of how consistent neural oscillations are along with the stimulation the brain has been entrained to. Using the same experimental paradigm Anna measured in phase in values between 0 (random phase) and 1 (perfect phase synchronization). She found that, within one second of stimulation, phase synchronization occurs. In other words, it only takes up to a second for the brain to entrain to a tone oscillation.

The underlying idea of synchronization is highly related to the anticipation mechanism. Once the subject has learned a rhythm, it is because they are able to anticipate the moment they have to press the button, that synchronization with the tone’s gap happens.

Again, the same as happened with accuracy in the long condition, the phase of the subjects’ neural oscillations would align faster with the phase of the tone in the long condition.

Her second experiment focused on cross-modal entrainment – where two types of stimuli used in entrainment both individually and combined. These two stimuli were auditory and visual, and this model was aimed to answer the following question:

Does visual rhythmic stimulation enhance auditory cortex activity and behavioural performance?

Here Anna focused on cross-modal entrainment using a similar experimental paradigm as in the first study but using magnetoencephalography (MEG) in addition. Participants were just required to detect the gaps inserted in different phases of a 3 Hz pulsating circle (visual-only condition), a 3 Hz frequency-modulated tone (auditory-only condition) and a cross-modal entrainment visual-auditory condition.

Accuracy in synchronizing under the visual-auditory condition was significantly higher than in the auditory-only condition. Both EEG and MEG at 3Hz (stimulation frequency) and 6Hz (harmonic) consistently showed auditory cortex activations during auditory-only condition and occipital activations during the visual-only condition. Most interestingly, MEG showed 3 Hz neural activation in auditory cortices during visual stimulation even in the absence of auditory stimuli (Figure 3). Taken together, these results provide clear evidence of neural entrainment in both visual and auditory modalities and that a cross-modal auditory-visual entrainment occurs at both behavioral and neural level.

Fig. 3

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Source: Bauer et al. (2018)

What does all this mean?

The interest in the fascinating and universal phenomenon of entrainment has increased among researchers. Interestingly, entrainment appears to pave the way to prediction which is of great adaptive value because successes or failures in prediction are associated with significant psychological and physiological consequences (Clark, 2013; Merker, 2015). Particularly interesting is that auditory entrainment appears to be fundamental in language development (Pammer, 2014) and rhythmic entrainment constitutes the most distinctive musical behavior which is very rare in other species (Merker, 2015; Patel, 2014). Several clinical implications of rhythm entrainment also arise for clinical contexts as a relevant working ingredient of music therapy in the context of dyslexia, gait rehabilitation of stroke patients and other motor problems such as those found in Parkinson’s disease, autism, etc. (Pammer, 2014; Thaut et al., 2015).

The research presented by Ana proposes a novel and exciting approach to music psychology. We look forward to hearing her new discoveries in her post-doc studies.

Stella Sun, Kirsty Hawkins, Beatriz Matt Martin and Paulo Andrade.

References

Bauer, A. R., Bleichner, M. G.., Jaeger, M., Thorne, J. D., & Debener, S. (2018). Dynamic phase alignment of ongoing auditory cortex oscillations. Neuroimage, 167, 396-407

Calderone, D. J., Lakatos, P., Butler, P. D., & Castellanos, F. X. (2014). Entrainment of neural oscillations as a modifiable substrate of attention. Trends in cognitive sciences, 18(6), 300-309.

Clark, A. (2013). Whatever next? Predictive brains, situated agents, and the future of cognitive science. Behavioral and Brain Sciences, 36(03), 181-204.

Clocks image: https://brilliant.org/practice/huygens-clock-puzzle/?chapter=intro Retrieved on 24th December 2018.

Henry, M. J., & Obleser, J. (2012). Frequency modulation entrains slow neural oscillations and optimizes human listening behavior. PNAS, 109(49), 20095-20100.

Merker, B., Morley, I., & Zuidema, W. (2015). Five fundamental constraints on theories of the origins of music. Philosophical Transactions of the Royal Society B: Biological Sciences370(1664), 20140095.

Pammer, K. (2014). Temporal sampling in vision and the implications for dyslexia. Frontiers in human neuroscience, 7, 933.

Pikovsky, A., Rosenblum, M., & Kurths, J. (2003). Synchronization: A Universal Concept in Non-linear Sciences. Cambridge University Press, United Kingdom.

Thaut, M. H., McIntosh, G. C., & Hoemberg, V. (2015). Neurobiological foundations of neurologic music therapy: rhythmic entrainment and the motor system. Frontiers in psychology, 5, 1185.

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