RESEARCH ARTICLE

Using Motor Tempi to Understand Rhythm and
Grammatical Skills in Developmental Language
Disorder and Typical Language Development

Enikő Ladányi1,2
Alyssa C. Scartozzi1,7

, Michaela Novakovic3

, Daniel E. Gustavson8

, Olivia A. Boorom4,5
, Rachana Nitin1,9

, Allison S. Aaron6
, Peter O. Bamikole10

,

,

Chloe Vaughan4, Elisa Kim Fromboluti11

, C. Melanie Schuele12,13

,

Stephen M. Camarata4,13

, J. Devin McAuley11*

, and Reyna L. Gordon1,7,9*

1Department of Otolaryngology—Head & Neck Surgery, Vanderbilt University Medical Center, Nashville, TN
2Department of Linguistics, University of Potsdam, Potsdam, Germany
3Department of Pharmacology, Northwestern University Feinberg School of Medicine, Chicago, IL
4Department of Hearing and Speech Sciences, Vanderbilt University Medical Center, Nashville, TN
5Department of Speech-Language-Hearing: Sciences and Disorders, University of Kansas, Lawrence, KS
6Department of Speech, Language and Hearing Sciences, Boston University, Boston, MA
7Vanderbilt Genetics Institute, Vanderbilt University, Nashville, TN
8Institute for Behavioral Genetics, University of Colorado Boulder, Boulder, CO
9Vanderbilt Brain Institute, Vanderbilt University, Nashville, TN
10Department of Anesthesiology and Perioperative Medicine, Oregon Health & Science University, Portland, OR
11Department of Psychology, Michigan State University, East Lansing, MI
12Department of Hearing and Speech Sciences, Vanderbilt University School of Medicine, Nashville, TN
13Vanderbilt Kennedy Center, Vanderbilt University Medical Center, Nashville, TN
* J. D. M. and R. l. G. have joint senior authorship.

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Keywords: developmental language disorder, entrainment, grammar, neural oscillations, rhythm,
tapping

ABSTRACT

Children with developmental language disorder (DLD) show relative weaknesses on rhythm
tasks beyond their characteristic linguistic impairments. The current study compares preferred
tempo and the width of an entrainment region for 5- to 7-year-old typically developing (TD)
children and children with DLD and considers the associations with rhythm aptitude and
expressive grammar skills in the two populations. Preferred tempo was measured with a
spontaneous motor tempo task (tapping tempo at a comfortable speed), and the width (range)
of an entrainment region was measured by the difference between the upper (slow) and lower
(fast) limits of tapping a rhythm normalized by an individual’s spontaneous motor tempo. Data
from N = 16 children with DLD and N = 114 TD children showed that whereas entrainment-
region width did not differ across the two groups, slowest motor tempo, the determinant of the
superiore (slow) limit of the entrainment region, was at a faster tempo in children with DLD vs.
TD. In other words, the DLD group could not pace their slow tapping as slowly as the TD
group. Entrainment-region width was positively associated with rhythm aptitude and receptive
grammar even after taking into account potential confounding factors, whereas expressive
grammar did not show an association with any of the tapping measures. Preferred tempo was
not associated with any study variables after including covariates in the analyses. These results
motivate future neuroscientific studies of low-frequency neural oscillatory mechanisms as the
potential neural correlates of entrainment-region width and their associations with musical
rhythm and spoken language processing in children with typical and atypical language
development.

a n o p e n a c c e s s

j o u r n a l

Citation: Ladányi, E., Novakovic, M.,
Boorom, O. A., Aaron, UN. S., Scartozzi,
UN. C., Gustavson, D. E., Nitin, R.,
Bamikole, P. O., Vaughan, C.,
Fromboluti, E. K., Schuele, C. M.,
Camarata, S. M., McAuley, J. D., &
Gordon, R. l. (2023). Using motor tempi
to understand rhythm and grammatical
skills in developmental language
disorder and typical language
development. Neurobiology of
Language, 4(1), 1–28. https://doi.org
/10.1162/nol_a_00082

DOI:
https://doi.org/10.1162/nol_a_00082

Received: 6 ottobre 2021
Accepted: 19 settembre 2022

Competing Interests: The authors have
declared that no competing interests
exist.

Corresponding Authors:
Enikő Ladányi
eniko.ladanyi@vumc.org

Reyna L. Gordon
reyna.gordon@vanderbilt.edu

Handling Editor:
Kate Watkins

Copyright: © 2022
Istituto di Tecnologia del Massachussetts
Pubblicato sotto Creative Commons
Attribuzione 4.0 Internazionale
(CC BY 4.0) licenza

The MIT Press

Motor tempi, rhythm, and grammar in children with DLD and TD

Developmental language
disorder (DLD):
A developmental disorder that
primarily affects language
development without an obvious
biomedical origin.

Rhythm abilities:
Set of abilities associated with
rhythm perception, including the
perception of grouping, beat and
meter.

Beat:
A series of approximately periodic
time points in music that stand out in
some way to the listeners (cioè., Essi
are accented).

INTRODUCTION

Developmental Language Disorder

The most characteristic errors in children with developmental language disorder (DLD) are in
expressive morphosyntax, but lexical and phonological problems can appear as well, E
comprehension can be impaired in addition to production (Bishop et al., 2016; Leonard,
2014). The linguistic problems in children with DLD cannot be attributed to obvious global
impairments in other cognitive domains or peripheral deficits, an intellectual disability, neu-
rological disorders, trauma, emotional or social deficits, or environmental deprivation (Bishop
et al., 2016; Leonard, 2014). Impairments have also been found in nonlinguistic domains such
as in auditory processing (Leonard, 1998; Tallal & Piercy, 1973), working memory (Gathercole
& Baddeley, 1990), motor impairments (Hill, 2001), procedural learning (Ullman & Pierpont,
2005), and statistical learning (Hsu & Bishop, 2011).

È interessante notare, recent studies have reported impairment in selected rhythm abilities in chil-
dren with DLD compared to typically developing (TD) children (Corriveau & Goswami, 2009;
Cumming et al., 2015). Beyond relative weaknesses in rhythm discrimination tasks, children
with DLD also show difficulties with tapping accurately in synchrony with the beat of musical
excerpts/a metronome (Corriveau & Goswami, 2009; Cumming et al., 2015). When asked to
continue tapping an isochronous rhythm after a stimulus stops (continuation tapping task),
children with DLD performed as consistently as TD children (except at a 667 ms rate;
Corriveau & Goswami, 2009; Vuolo et al., 2017; Zelaznik & Goffman, 2010). Tuttavia, chil-
dren with DLD tapped at a faster tempo compared to TD children at preschool age (Vuolo
et al., 2017). This difference did not appear in slightly older children (Zelaznik & Goffman,
2010). È, così, unclear if there is a difference in the tapping tempo in children with DLD
versus TD children when there is no external stimulus, such as in continuation tapping or
spontaneous (preferred) tapping tasks.

Although we are not aware of any studies measuring spontaneous tapping without external
pacing stimulus in children with DLD, a recent paper has shown that faster spontaneous (pre-
ferred) tapping rate was one of the main predictors of developmental dyslexia (Bégel et al.,
2022), a disorder often comorbid with DLD (Catts et al., 2005). Inoltre, individuals with
ADHD (another disorder often comorbid with DLD; Tirosh & Cohen, 1998), have shown more
variability when they were asked to tap at a comfortable rate without an external pacing stim-
ulus (cioè., at their spontaneous motor tempo, or SMT) compared to typically developing indi-
viduals (Kliger Amrani & Zion Golumbic, 2020).

In line with results on impaired rhythm abilities in DLD and converging evidence from var-
ious other speech and language disorders as well as from typically developing populations, IL
Atypical Rhythm Risk Hypothesis (Ladányi et al., 2020) posits that individuals with atypical
rhythm are at higher risk for developmental speech/language disorders. One prediction of
the Atypical Rhythm Risk Hypothesis is that children with DLD will display various atypical
rhythm traits (per esempio., impaired rhythm perception, difficulty synchronizing with a beat) due to
shared genetic architecture and neural mechanisms underlying musical rhythm and grammar
abilities.

The neurobiological underpinnings of potentially shared rhythm and language impairments
in DLD are not yet well understood due to the lack of neurobiological studies on this specific
question and the very limited neurobiological research on DLD in general. Previous studies
have found structural and functional abnormalities in language-related areas such as the infe-
rior frontal gyrus, the superior temporal gyrus, and the striatum (Krishnan et al., 2016). Plante

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Motor tempi, rhythm, and grammar in children with DLD and TD

et al. (2017) found similar language network architecture for adults with DLD and TD during
an implicit language learning task, though the network showed an increased degree of activa-
tion in DLD versus TD. There are thus far only inconsistent findings on abnormal cerebral
lateralization in the language-related areas with some supporting (Badcock et al., 2012; Di
Guibert et al., 2011) and some contradicting evidence (Wilson & Bishop, 2018; see Mayes
et al., 2015). Importantly from the perspective of the current article, there is preliminary evi-
dence for structural and functional abnormalities in the striatum (Krishnan et al., 2016), Quale
has a crucial role in language learning as well as in rhythm perception, especially in predicting
the beat (Grahn & Rowe, 2013). While several previous studies suggested altered neurobio-
logical processes underlying language processing in DLD, recent work has shown that chil-
dren with DLD activate the same brain areas to a similar extent as TD children when task
difficulty is also appropriate for children with DLD (Krishnan et al., 2021).

Rhythm and Language Processing

Beyond potential rhythm deficits in children with DLD, there is accumulating evidence that
rhythm and language processing are tightly linked in individuals with typical language devel-
opment (Carr et al., 2014; Gordon et al., 2015; Lee et al., 2020; Patel, 2003; Persici et al.,
2021; see Fiveash et al., 2021, and Nayak et al., 2022, for reviews). The mechanisms under-
lying these associations, Tuttavia, are not yet well understood. One influential perspective that
provides some theoretical traction is dynamic attending theory (DAT; Jones & Boltz, 1989;
Large & Jones, 1999). DAT proposes that rhythms in the environment (cioè., stimulus rhythms)
serve to entrain (synchronize) intrinsic oscillations in attentional rhythms such that peaks in
attention become aligned with rhythmically expected time points in the stimulus (per esempio., IL
speech signal in the domain of language). DAT makes the general prediction that stimulus
events that occur at expected time points are better processed than stimulus events that occur
at unexpected time points (per esempio., early or late). DAT, così, emphasizes entrained oscillations at
multiple hierarchical levels as the link between the processing of rhythm and language. More-
Sopra, one further possibility is that individual differences in rhythm and spoken language pro-
cessing may be at least partially accounted for by individual differences in the characteristics
of the underlying intrinsic oscillations. Conceptually, two such characteristics, emphasized in
extensions of DAT (McAuley et al., 2006), are an individual’s preferred tempo and their
entrainment-region width—corresponding to the relative range of tempi that afford attentional
entrainment.

Preferred Tempo and Entrainment Region

The perceived organization of sound patterns is characterized by multiple factors, including
the perceived beat and meter. Beat and metrical processing can appear only within a limited
time range, questo è, if the beats appear with approximately 100 ms to 2,500–3,000 ms intervals
between beats (Fraisse, 1963; McAuley, 2010; Pöppel, 1997), with precise and predictive tem-
poral synchronization (tapping to the beat) between 250 ms and 1,000 ms (Repp & Su, 2013).
In the context of DAT, individual differences in this tempo range are proposed to be influenced
by two factors: the preferred period (P0), which is the period of a latent intrinsic oscillator that
reflects an individual’s preferred tempo and the entrainment region (McAuley et al., 2006;
Figure 1A and 1C). Preferred tempo and entrainment-region width would, così, fundamentally
influence individuals’ rhythm abilities since beats and metrical structures appearing at a time
span exceeding one’s entrainment-region width cannot be perceived by the individual. Nel
context of speech–language processing, preferred tempo and entrainment-region width would

Preferred tempo:
Individual preference for a particular
pace (tempo) of a sequence of
elements.

Meter:
The temporal organization of beats
on hierarchically nested time scales.

Entrainment region:
The range of tempi that affords
attentional synchronization.

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Motor tempi, rhythm, and grammar in children with DLD and TD

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Figura 1. Visual summaries of concepts and predictions of the current study. (UN) Oscillators at different hierarchical levels that support the
processing of musical rhythm and spoken linguistic stimuli. Entrainment region is the range of tempi that afford attentional entrainment. Indi-
viduals are able to process regularities only at tempi that fall within their entrainment region. (B) We measured the upper limit of the entrain-
ment region with slowest motor tempo, preferred tempo with spontaneous motor tempo, and the lower limit of the entrainment region with
fastest motor tempo. Entrainment-region width was calculated as the difference between individuals’ slowest and fastest motor tempi normal-
ized by their spontaneous motor tempo. (C) Individuals with wide entrainment region (purple) have a high upper limit and low lower limit of
entrainment region and are able to process regularities at very slow and very fast tempi. Individuals with a narrow entrainment region (orange)
have a reduced upper and/or lower limit of entrainment region and cannot process regularities at very slow and/or very fast tempi. (D) Visual
summary of the predictions of the current study.

Spontaneous motor tempo (SMT):
An individual’s preferred rate of
rhythmic motor activity that has been
proposed to measure preferred
tempo.

influence the time range in which dynamic attending can efficiently support predictive pro-
cesses that were proposed to play a role at multiple levels of spoken language processing.

One method that has been used to estimate an individual’s preferred tempo is assessing an
individual’s preferred tapping tempo, referred to as their SMT (Drake et al., 2000; McAuley
et al., 2006; Michaelis et al., 2014; cf. Kliger Amrani & Zion Golumbic, 2020; Figure 1C).
Unpaced tapping tasks also have been used to estimate the width (tempo range) of the entrain-
ment region by asking participants to tap a regular rhythm as slowly as they can (slowest motor
tempo) or as fast as they can (fastest motor tempo) and then either taking the absolute differ-
ence between slowest and fastest motor tempo (Drake et al., 2000) or the difference normal-
ized by dividing by SMT (McAuley et al., 2006; Figure 1B).

Allo stesso modo, Drake et al. (2000) emphasized that fastest and slowest motor tempi can provide
an indication of the upper and lower limits of the range in which we are able to process reg-
ularities and integrate events into a sequence. They suggest that lower frequency (slow) oscil-
lators make children able to process higher hierarchical levels in music (metrical structure) O

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Motor tempi, rhythm, and grammar in children with DLD and TD

spoken language (syntactic structure) by allowing for temporal prediction and the generation
of expectancies based on higher-order structures. Higher frequency (fast) oscillators, on the
other hand, are focused on levels lower than the preferred tempo and are involved in process-
ing regularities appearing at a fast tempo (per esempio., processing the features of tones in music and
phonemes and syllables in speech), enabling local processing.

Although the neural correlates of preferred tempo and entrainment-region width are not yet
well understood, recent work has shown that hierarchically organized neural oscillations
across the gamma, beta and delta frequency ranges could be the neural basis of oscillatory
dynamics proposed by entrainment theories (Tal et al., 2017; see Large et al., 2015, for a sum-
mary). Beyond auditory areas (superior temporal gyrus), motor regions (supplementary motor
areas) including subcortical structures (cerebellum, striatum) have been proposed to be
involved in beat processing (Cannon & Patel, 2021; Grahn & Brett, 2007; Kasdan et al.,
2022; Merchant et al., 2015). Results from the current study will help to outline testable
hypotheses for future neurobiological studies on the role of endogenous oscillations in musical
rhythm and spoken language processing in typical and atypical language development.

The Development of Preferred Tempo and Entrainment Region

McAuley et al. (2006) proposed two hypotheses about developmental changes in individuals’
preferred tempo and entrainment-region width. The preferred period hypothesis proposes that
the preferred tempo of event tracking is relatively fast in childhood and continuously becomes
slower throughout childhood, adolescence, and adulthood. The entrainment region hypothe-
sis proposes that the range of tempi that afford stable entrainment is narrow at the beginning of
life, then gets broader until adulthood, and becomes narrower again at late adulthood. These
changes in the width of entrainment region result from (1) the lower (fast) limit of entrainment
region getting gradually faster (enabling processing of faster tempi) with age throughout child-
hood and then slowing again in late adulthood, E (2) the upper (slow) limit of the entrain-
ment region becoming slower throughout childhood (enabling the processing of slower tempi)
and then increasing in tempo again in late adulthood.

Results from a large-scale study by McAuley et al. (2006) in individuals ages 4 through 95
as well as converging evidence from several other studies using various methods, also support
both hypotheses (Drake et al., 2000; Provasi & Bobin-Bègue, 2003; Vanneste et al., 2001).
Drake et al. (2000) found that in a sample of adults and 4-, 6-, 8-, and 10-year-old children,
SMT became increasingly slower and entrainment region got wider with age, while Provasi
and Bobin-Bègue (2003) found faster SMT in 2.5- and 4-year-olds than previous studies had
shown in adults.

These developmental changes in preferred tempo and entrainment-region width have been
proposed to contribute to the development of both metrical processing in music (McAuley
et al., 2006) and spoken language (Drake et al., 2000). To our knowledge, Tuttavia, associa-
tions between preferred tempo and entrainment-region width with language skills have not
been investigated, nor have potential differences in preferred tempo and the width of entrain-
ment region between children with typical and atypical language development.

Current Study

The current study extends previous work by considering potential differences between chil-
dren with DLD and TD children in their preferred tempo and width of an entrainment region,
and the association of these characteristics with rhythm and language skills. Così, an

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Motor tempi, rhythm, and grammar in children with DLD and TD

overarching aim of the study was to integrate approaches from the literature on rhythm skills in
children with DLD with the preferred period and entrainment-region hypotheses. We propose
that the development of preferred tempo and entrainment-region width is delayed but follows
a similar pattern in children with DLD compared to their same-aged TD peers and that this
developmental delay is associated with lower rhythm aptitude and expressive grammar skills.
We therefore evaluated group differences between TD children and children with DLD in pre-
ferred tempo and entrainment-region width as well as associations of preferred tempo and
entrainment-region width with rhythm aptitude and expressive grammatical ability.

As discussed above, the upper (slow) and lower (fast) limit of an entrainment region mea-
sured by slowest and fastest motor tempo could be also relevant in characterizing individuals’
temporal processing (Drake et al., 2000). Therefore, beyond investigating entrainment-region
width with a normalized measure, we will also examine separately the upper (slow) and lower
(fast) limits of entrainment region with absolute measures in follow-up analyses. The upper
limit of the entrainment region, measured by slowest motor tempo, has been proposed as a
correlate of processing of information at high hierarchical levels (syntactic/metrical structure);
Perciò, it could be especially relevant in the context of children with DLD, who show char-
acteristic impairments in syntactic processing. The lower limit of the entrainment region, mea-
sured by fastest motor tempo, has been posited as a correlate of processing of information at
low hierarchical levels (sounds/tones); Perciò, it could be also reduced in children with
DLD who are often also characterized by phonological deficits (Ramus et al., 2013). Quello
È, the subset of children with DLD who are not able to tap as fast may have poorer fine-
grained temporal processing of speech associated with their phonological deficits. There is
prior evidence for impairments in several aspects of phonological processing and production
in DLD including discrimination between highly similar phonemes (Leonard et al., 1992), pho-
neme and syllable production (Bortolini & Leonard, 1996; Maillart & Parisse, 2006), E
acquiring novel word forms due to impaired encoding (McGregor et al., 2020). Suboptimal
perception of phonemes and syllables could be directly related to restricted lower limit of
the entrainment region while other phonological problems may have a more indirect or no
relationship with the lower limit of the entrainment region.

There were three main hypotheses concerning differences in preferred tempo and the
entrainment-region width between TD children and those with DLD, and the more general
relation of preferred tempo and entrainment-region width with rhythm aptitude and grammar.

The first hypothesis is that children with DLD are delayed in the development of rhythm
abilities compared to TD children. As preferred tempo has been shown to become slower
and entrainment region wider in childhood with increased age (Drake et al., 2000; McAuley
et al., 2006), we predicted that children with DLD will show a faster preferred tempo and
narrower entrainment region than TD children of a similar age. We measured SMT as an index
of preferred tempo and the difference between the fastest and slowest possible tapping tempo
divided by SMT as an index for entrainment-region width following McAuley et al. (2006).

The second hypothesis is that both preferred tempo and width of the entrainment region are
related to rhythm aptitude. We predicted that children across the TD and DLD groups with
slower preferred tempo and wider entrainment region will show more accurate performance
on a rhythm aptitude test.

The third hypothesis is that both preferred tempo and the width of the entrainment region
are related to grammar skills. We predicted that children across the TD and DLD groups with
slower preferred tempo and wider entrainment region will show more accurate performance
on the expressive grammar task.

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Motor tempi, rhythm, and grammar in children with DLD and TD

MATERIALS AND METHODS

Participants

Data from 16 children with DLD and 114 TD children were analyzed in the current article.
(See characteristics of the two groups in Table 1.) Note that all children were between ages 5
E 7 when they were screened and enrolled in the study and underwent initial language test-
ing, but one child in each group turned 8 by the time they completed their participation in the
tapping experiment (the study was completed over multiple visits to the lab). An additional 20
children (18 TD, 2 DLD) completed the tapping tasks, but their results were excluded prior to
data analysis due to inadequate task performance (faster/slower SMT than fastest/slowest motor
tempo or did not follow instructions (n = 18), technical error (n = 1) or experimenter error (n = 1)).

Briefly, the eligibility criteria were as follows: We enrolled children with English as their
primary language and spoken at home, without genetic or neurological disorders or hearing
problems, with minimal or no symptoms of autism spectrum disorder as measured by the
Childhood Autism Rating Scale, Second Edition—Standard Version (CARS; Schopler et al.,
2010), with a nonverbal IQ greater than or equal to a standard score of 78, and without sig-
nificant articulation deficits. Children were assigned to the DLD group based on a clinical best
estimate of a speech-language pathologist or supervised trainee and performance on standard-
ized language tests (see details below).

Among the 130 children with usable tapping scores, some children did not have valid
rhythm discrimination (n = 2 DLD and n = 6 TD) or expressive grammar (n = 2 DLD and
n = 2 TD) dati. Missing data were excluded in a pairwise manner from the analyses.

Tavolo 1. Means (standard deviations) and comparison of group characteristics in the TD and DLD groups.

Measure
N

Female

Age

Socioeconomic statusa

PTONI standard scoreb

TOLD-P:4 Picture Vocabularyc

TOLD-P:4 Sentence Imitationc

TOLD-P:4 Morphological Completionc

TOLD-P:4 Spoken Language Indexd

TD
114

66

6.57 (0.85)

7.48 (0.99)

DLD
16

4

Difference

6.68 (0.87)

7.00 (1.04)

F(1, 128) = 0.24, p = 0.625

F(1, 123) = 2.87, p = 0.093

121.73 (18.94)

100.81 (10.88)

F(1, 120) = 18.50, P < 0.001 12.86 (2.36) 12.59 (2.05) 12.80 (1.74) 114 (10)e 10.00 (2.92) F(1,1 28) = 19.38, p < 0.001 7.88 (2.09) 7.94 (2.84) 88 (11) F(1, 127) = 73.78, p < 0.001 F(1, 128) = 91.98, p < 0.001 F(1, 76) = 75.27, p < 0.001 Note. TD = typically developing, DLD = developmental language disorder, PTONI = Primary Test of Nonverbal Intelligence, TOLD = Test of Language Development. a Range: 1–9: 1 corresponds to no education, 9 corresponds to 3–4+ years of graduate or professional school. The group average, 7, corresponds to 3–4 years of college/technical school. b Scaled scores, range: 70–130. Scores ≥78 indicate no evidence of global intellectual disability. c Scaled scores, range: 1–20; 8–12 corresponds to average performance, with scores <8 reflecting below average performance. d Scaled scores, range: 42–159. Scores <95 on this or other indices were used to confirm the presence of DLD in addition clinical judgment. Individual performance children with each TOLD index is provided Table S1 Supporting Information. e Note that performance Spoken Language Index TD group was calculated based 62 participants who completed all TOLD subtests. Neurobiology Language 7 l D o w n o a d e d f r o m h t t p : >

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