# Editorial: Entrainment and responses to rhythmic stimulation during development

Stefanie Peykarjou, Stefanie Hoehl, Arnaud Leleu, Aliette Lochy, Viola Macchi Cassia

<figure><img src="image_1.png" /></figure>

## To cite this version:

Stefanie Peykarjou, Stefanie Hoehl, Arnaud Leleu, Aliette Lochy, Viola Macchi Cassia. Editorial: Entrainment and responses to rhythmic stimulation during development. Frontiers in Psychology, 2023, 14, pp.1189054. 10.3389/fpsyg.2023.1189054. hal-04101296

HAL Id: hal-04101296

https://hal.inrae.fr/hal-04101296

Submitted on 19 May 2023

HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d'enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

<figure><img src="image_2.png" /></figure>
<figure><img src="image_3.png" /></figure>

Check for updates

## OPEN ACCESS

EDITED AND REVIEWED BY
Peter Klaver,
Interkantonale Hochschule für Heilpädagogik
(HfH), Switzerland

*CORRESPONDENCE
Stefanie Peykarjou
✉ stefanie.peykarjou@
psychologie.uni-heidelberg.de

RECEIVED 18 March 2023

ACCEPTED 10 April 2023

PUBLISHED 28 April 2023

## CITATION

Peykarjou S, Hoehl S, Leleu A, Lochy A and Macchi Cassia V (2023) Editorial: Entrainment and responses to rhythmic stimulation during development. *Front. Psychol.* 14:1189054.
doi: 10.3389/fpsyg.2023.1189054

## COPYRIGHT

© 2023 Peykarjou, Hoehl, Leleu, Lochy and Macchi Cassia. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Editorial: Entrainment and responses to rhythmic stimulation during development

Stefanie Peykarjou<fnref n="1" />*, Stefanie Hoehl², Arnaud Leleu<fnref n="3" />, Aliette Lochy⁴ and Viola Macchi Cassia⁵,<fnref n="6" />

## KEYWORDS

FPVS, frequency tagging, oscillations, SSVEPs, synchronization, development

### Editorial on the Research Topic

### Entrainment and responses to rhythmic stimulation during development

Rhythms are omnipresent in physiological processes, sensory inputs and social interactions. Humans respond to external rhythms with synchronization, which can be observed across multiple levels (e.g., behavior, brain, and physiology). Given their ubiquitous nature, utilizing rhythmic stimulation to characterize development is beneficial in many domains, including cognition, perception, and motor functioning.

This Research Topic brings together current research on behavioral and brain responses to rhythmic stimulation in development across these domains. This ultimately helps to broaden our understanding of neural entrainment (e.g., Bánki et al.), of the links between rhythms and cognitive or behavioral development (e.g., Frischen et al.; Yu et al.), and of the methods employing rhythmic stimulation to investigate early development (e.g., Peykarjou). Since rhythmic responses can be conceived as entrainment of endogenous oscillators to external rhythms (e.g., Notbohm et al., 2016), or periodic evoked responses (Capilla et al., 2011), “entrainment” is broadly defined here as responses elicited by a corresponding external driving rhythm.

Several contributions in this Research Topic focus on theoretical advancements regarding relevant concepts and relations of rhythms with development (Bánki et al.; Bowsher-Murray et al.; Frischen et al.). Bánki et al. provide a discussion of neural entrainment in contrast to stimulus tracking and argue that evidence in favor of entrainment is accumulating. However, this evidence largely comes from research with adults, and establishing the presence of neural entrainment in early development requires adapting current methods. The authors call for studies aligning the stimulation frequency to individual internal oscillations of participants and investigating how external rhythms modulate behavioral performance.

The relation between rhythm processing, cognitive and motor abilities is analyzed by Frischen et al. who discuss predictive processing (Friston, 2005) as the mechanism that might link these functions. Studies showing substantial correlations between rhythm processing and language ability, motor skills and executive functions are summarized. Predictive

<footnote n="1">¹Department of Psychology, Heidelberg University, Heidelberg, Germany, ²Department of Developmental and Educational Psychology, Faculty of Psychology, University of Vienna, Vienna, Austria,</footnote>

<footnote n="3">³Development of Olfactory Communication and Cognition Laboratory, Centre des Sciences du Goût et de l'Alimentation, Université de Bourgogne, CNRS, INRAe, Institut Agro, Dijon, France, ⁴Institute of Cognitive Science and Assessment (COSA), Department of Behavioral and Cognitive Sciences (DBCS), Faculty of Humanities, Social and Educational Sciences (FHSE), University of Luxembourg,</footnote>

<footnote>Esch-sur-Alzette, Luxembourg, ⁵Department of Psychology, University of Milano-Bicocca, Milan, Italy,</footnote>

<footnote n="6">⁶NeuroMI, Milan Center for Neuroscience, Milan, Italy</footnote>
processing in beat perception, anticipating temporally ordered
sound events, is suggested to stimulate prediction in other domains,
providing a link explaining commonalities in development.

Lau et al. provide support for the view that early links between
language (i.e. vocalizations) and cognition may be subserved
by infants' perceptual sensitivity to rhythmic elements. Drawing
on evidence from four-month-olds showing that language may
facilitate categorization (Ferry et al., 2013), the authors employ
supervised machine learning to show that rhythm-related features
of acoustic stimuli and temporal envelope components may be vital
for supporting cognition.

In their contribution, Bowsher-Murray et al. approach the role
of rhythm in development by focusing on interpersonal synchrony,
i.e., the “tendency for social partners to temporally coordinate
their behavior when interacting”. They provide an overview of
components underpinning successful non-verbal interpersonal
synchrony, including social orienting, action prediction and motor
behavior, monitoring and error detection, pointing out that more
work on the potentially bidirectional nature of behavioral and
neural entrainment is required. Indeed, spanning these levels of
analysis was accomplished across contributions in this Research
Topic but should be tackled within studies in the future.

Behavioral entrainment is addressed in three studies
investigating the development of rattle-shaking and drumming
(Laudanska et al.; Rocha and Addyman; Yu et al.). The ability
to coordinate drumming movements to match external rhythms
was investigated in toddlers between 18 and 30 months of age
(Rocha and Addyman; Yu et al.). The beginnings of rhythmic
behavior are explored by Laudanska et al., who investigate coupling
between infants' arm movements longitudinally from four to
twelve months. They document infants' motivation for rhythmic
behavior from early on, as participants similarly attempt rattle-
shaking across all ages. With age, left and right arm movements
become more coupled during rattle-shaking independent of age,
demonstrating how synchronization diffuses throughout the body.
Yu et al. demonstrate that by 24 months, children begin to slow
down their spontaneous motor tempo toward the rhythm provided
by a drumming partner, but successful synchronization is only
achieved by 30 months. Rocha and Addyman employ a novel
tool, deep learning-based OpenPose, to automatically estimate
drumming behavior from home-recorded videos. Both studies
show that toddlers between 24 and 30 months of age are strongly
motivated to engage in synchronous movement, as they adapt their
drumming tempo away from their intrinsic rate of movement to
match either a social interaction partner, a robot (Yu et al.), or the
video of a drumming hand (Rocha and Addyman).

The research by Frey et al. applies rhythmic stimulation as a
tool for facilitating development. In a training study with preschool
children, they demonstrate correlations between children's
rhythmic and literacy skills and between rhythm synchronization
and pen pressure. Training provided in their study effectively
improves rhythmic abilities, however these improvements do not
transfer to literacy or graphomotor development. Further research
is needed to evaluate whether rhythmic training may causally
support development in other domains.

Other studies assembled in this Research Topic employ
responses to rhythmic stimulation coupled with neural measures
to examine auditory and visual processing (Attaheri et al.;

Bertels et al.; Cantiani et al.; Pescuma et al.; Peykarjou; Poncet
et al.). In these studies, rhythmic stimulation is mainly employed as
a tool for exploring perceptual and cognitive development without
necessitating a behavioral response.

Auditory processing is investigated by Cantiani et al. who employ frequency tagging with complex music and speech stimuli. The authors report similar neural entrainment to auditory stimuli, particularly music, in eight-month-old infants and adults. They infer that neural synchronization and tempo flexibility develop before synchronization abilities become apparent in behavior. Attaheri et al. also compare neural synchronization to speech stimuli between adults and infants (four to eleven months) and find commonalities across development. Participants track sung speech in delta and theta bands, but specific peak-frequencies differ between the two populations. Together, these studies suggest that infant and adult brains utilize similar cortical mechanisms to track linguistic inputs, but the interplay between these mechanisms varies with age and language experience.

Four studies employ the Fast Periodic Visual Stimulation (FPVS) oddball paradigm (Liu-Shuang et al., 2014) with visual stimuli. Infants' developing ability to discriminate facial expressions from 3.5 to 7 months is investigated by Poncet et al. Significant expression discrimination is observed from 3.5 months, with partly diverging topographies across facial expressions and age. Responses for emotional faces among neutral ones are recorded at right occipito-temporal sites, similar to adults (Poncet et al., 2019), suggesting that the discrimination of neutral vs. expressive faces is subserved by similar networks across development.

Bertels et al. investigate characteristics of a potentially
inborn mechanism to detect snakes, a species posing an
evolutionarily important threat to humans. EEG responses in six-
to-eleven-month-olds reveal that they detect snakes among other
animals, and this effect is not influenced by color. However,
responses increase with infant age, which is interpreted as a
specific visual development for evolutionary-relevant shapes in
complex backgrounds.

Peykarjou presents a systematic literature review on frequency tagging EEG employing the FPVS oddball paradigm and examines the effects of analysis decisions in a large sample of infants. Based on the assembled evidence, recommendations regarding duration, number of conditions, sequence- and participant-retention are made. Overall, evidence indicates that analysis decisions should be tailored to the age-group.

Pescuma et al. use frequency tagging to investigate a developing cultural skill, morpheme identification. They adapt an established paradigm (Lochy et al., 2016a,b) to MEG and demonstrate morpheme identification in developing readers that is overall similar to adults. Neural responses are primarily present for word stems in children and word suffixes in adults, suggesting an influence of accumulated reading experience.

This Research Topic assembles a variety of findings
demonstrating the importance of rhythms for development,
and their usefulness for elucidating cognitive, visual, auditory, and
motor functions. Moreover, it provides readers with an overview of
methodological advancements for infant studies, such as wearable
motion trackers (Laudanska et al.), an online version of a measure
for drumming synchrony (Rocha and Addyman), or guidelines
for frequency tagging EEG categorization tasks (Peykarjou). By
integrating findings across the different contributions, several
conclusions can be drawn. First, rhythms provide both a window
into development across different domains and a linking concept
for understanding the interplay of development and environmental
influences. Second, across developmental domains and levels of
analysis, rhythms play an important role that we only begin to
understand. Third, at both conceptual and empirical levels, further
work is required to leverage the potential of rhythmic stimulation
and entrainment for developing a more comprehensive picture of
how behavior and brain processing develop across domains.

Author contributions

SP wrote the initial draft. All authors listed have made a
substantial, direct, and intellectual contribution to the work and
approved it for publication.

Funding

This work was supported by a grant from the German Research
Foundation (DFG, grant number: PE 3125/1-1) to SP, two FWF

grants (grant numbers: P 33853 and I 4332) awarded to SH, the
French National Research Agency (grant number: ANR-19-CE28-
0009) awarded to ALe, and the Luxembourg National Research
Fund (FNR grant number: C21/SC/16241557) to ALo.

Conflict of interest

The authors declare that the research was conducted
in the absence of any commercial or financial relationships
that could be construed as a potential conflict
of interest.

Publisher's note

All claims expressed in this article are solely those
of the authors and do not necessarily represent those of
their affiliated organizations, or those of the publisher,
the editors and the reviewers. Any product that may be
evaluated in this article, or claim that may be made by
its manufacturer, is not guaranteed or endorsed by the
publisher.

References

Capilla, A., Pazo-Alvarez, P., Darriba, A., Campo, P., and Gross, J. (2011). Steady-state visual evoked potentials can be explained by temporal superposition of transient event-related responses. *PLoS ONE* 6, e14543. doi: 10.1371/journal.pone.0014543

Ferry, A. L., Hespos, S. J., and Waxman, S. R. (2013). Nonhuman primate vocalizations support categorization in very young human infants. *Proc. Nat. Acad. Sci.* 110, 15231–15235. doi: 10.1073/pnas.1221166110

Friston, K. (2005). A theory of cortical responses. *Philosoph. Transact. Royal Soc. B Biol. Sci.* **360**, 815–836. doi: 10.1098/rstb.2005.1622

Liu-Shuang, J., Norcia, A. M., and Rossion, B. (2014). An objective index of individual face discrimination in the right occipito-temporal cortex by means of fast periodic oddball stimulation. *Neuropsychologia* 52, 57–72. doi: 10.1016/j.neuropsychologia.10022

Lochy, A., Van Belle, G., and Rossion, B. (2016a). A robust index of lexical representation in the left occipito-temporal cortex as evidenced by

EEG responses to fast periodic visual stimulation. *Neuropsychologia* 66, 18–31.
doi: 10.1016/j.neuropsychologia.11007

Lochy, A., Van Reybroeck, M., and Rossion, B. (2016b). Left cortical specialization for visual letter strings predicts rudimentary knowledge of letter-sound association in preschoolers. *Proc. Nat. Acad. Sci.* 113, 8544–8549. doi: 10.1073/pnas.15203 66113

Notbohm, A., Kurths, J., and Herrmann, C. S. (2016). Modification of brain oscillations via rhythmic light stimulation provides evidence for entrainment but not for superposition of event-related responses. *Front. Hum. Neurosci.* 3, 10. doi: 10.3389/fnhum.2016.00010

Poncet, F., Baudouin, J.-Y., Dzhelyova, M. P., Rossion, B., and Leleu, A. (2019). Rapid and automatic discrimination between facial expressions in the human brain. *Neuropsychologia* 129, 47–55. doi: 10.1016/j.neuropsychologia.2019. 03.006