Psychology and Aging

© 2020 American Psychological Association 2020, Vol. 35, No. 8, 1184 –1200
ISSN: 0882-7974 http://dx.doi.org/10.1037/pag0000575

Rhythmic Timing in Aging Adults: On the Role of Cognitive Functioning

and Structural Brain Integrity

Annett Schirmer Rafael Romero-Garcia

The Chinese University of Hong Kong University of Cambridge

Man Hey Chiu Nicolas Escoffier

The Chinese University of Hong Kong Neurolandscape, Warsaw, Poland
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
This document is copyrighted by the American Psychological Association or one of its allied publishers.

Trevor B. Penney Benjamin Goh

The Chinese University of Hong Kong National University of Singapore

John Suckling Jasmine Tan

University of Cambridge Goldsmiths, University of London

Lei Feng
National University of Singapore

Here we asked whether impaired timing in older adults results from an aging clock or a more general brain
and cognitive decline. Healthy aging adults (N ⫽ 70, aged 62– 83 years) tapped to the beat of a periodic and
a syncopated rhythm. Analyses focused on performance differences between rhythms (periodic-syncopated),
which reduced the impact of timing unrelated processes. Apart from tapping, participants completed a
cognitive assessment and neuroimaging of gray matter volume (GMV) and fractional anisotropy (FA) globally
as well as regionally (cortical: auditory, premotor, paracentral; subcortical: putamen, caudate, cerebellum).
The rhythm difference showed no significant age effects for tapping asynchrony and an age-related decrease
for tapping consistency. Additionally, age reduced cognitive functioning, global GMV/FA, and, beyond this,
auditory GMV. Irrespective of age, the rhythm difference in tapping asynchrony was linked, not to GMV, but
to caudal, premotor, and paracentral FA after controlling for global FA. Tapping consistency was associated
with global rather than regional brain integrity. Additionally, age differences in tapping consistency were
mediated by a decline in global brain integrity as well as cognitive functioning. Together these results agree
with previous proposals differentiating between timing accuracy and reliability and suggest that aging largely
preserves the former but not the latter. Whereas timing accuracy may depend on an internal clock supported
by robust striatocortical circuitry, timing reliability may depend on global brain and cognitive functioning,
which show a pronounced age-related decline.

Keywords: relative timing, motor entrainment, striatum, human development

Supplemental materials: http://dx.doi.org/10.1037/pag0000575.supp

This article was published Online First October 1, 2020.
X Annett Schirmer, Department of Psychology and Brain and Mind
Institute, The Chinese University of Hong Kong; Rafael Romero-Garcia,
Department of Psychiatry, University of Cambridge; Man Hey Chiu,
Department of Psychology, The Chinese University of Hong Kong;
X Nicolas Escoffier, Neurolandscape, Warsaw, Poland; Trevor B. Penney,
Department of Psychology and Brain and Mind Institute, The Chinese
University of Hong Kong; Benjamin Goh, Department of Psychological
Medicine, Yong Loo Lin School of Medicine, National University of
Singapore; X John Suckling, Department of Psychiatry, University of
Cambridge; X Jasmine Tan, Department of Psychology, Goldsmiths, Uni-
versity of London; Lei Feng, Department of Psychological Medicine, Yong
Loo Lin School of Medicine, National University of Singapore.
The study, Choral Singing for the Prevention of Dementia: A Random-
ized Controlled Trial, was supported by the National Innovation Challenge
on Active and Confident Ageing Programme, Ministry of Health of Sin-
gapore (Award MOH/NIC/COG06/2017); the National Medical Research
Council of Singapore (Award NMRC/TA/0053/2016); the National Uni-
versity of Singapore Society Choir Dementia Research Fund. The work
associated with the data analysis and reporting of the present results was
supported by a grant awarded by the Hong Kong Research Grants Council
to Annett Schirmer (14612318). This research has not been presented in
any format previously.
Correspondence concerning this article should be addressed to Annett Schirmer,
Department of Psychology, The Chinese University of Hong Kong, 3rd Floor,
Sino Building, Shatin, N.T., Hong Kong. E-mail: schirmer@cuhk.edu.hk

1184
 NEUROCOGNITIVE STATUS AND TIMING IN THE ELDERLY
Most of our bodily processes are rhythmical. From the overall
cycle of birth and death down to short-timescale behavioral and
physiological patterns such as walking, breathing, or blinking,
regular temporal recurrence organizes our existence (Buhusi &
Meck, 2005; Merchant, Grahn, Trainor, Rohrmeier, & Fitch, 2015;
Schirmer, Meck, & Penney, 2016). Similarly, the world around us
is rhythmical and by adjusting internal to external rhythms, we can
optimize the outcomes of our actions. Here we explored how aging
changes such rhythmic processes by combining a paced tapping
task with assessments of cognitive functioning and brain morphol-
ogy in a group of seniors varying in age. Moreover, we asked
whether potential age effects on the ability to synchronize motor
output with an auditory rhythm are better explained by general
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cognitive and brain decline or by the deterioration of a dedicated
This document is copyrighted by the American Psychological Association or one of its allied publishers.
clock mechanism.
Much research has pursued the aging of mind and behavior.
Efforts directed specifically at timing showed that older adults
perform more poorly than younger adults (for a review see Tur-
geon, Lustig, & Meck, 2016). However, our ability to time com-
prises a heterogeneous set of functions and the aging of rhythmic
timing in particular has attracted limited attention to date (e.g.,
McAuley, Jones, Holub, Johnston, & Miller, 2006). Thus, it re-
mains debated what aspects of rhythmic timing might be compro-
mised in late adulthood and whether apparent deficits reflect the
deterioration of timing-specific or domain-general functions. In
what follows, we will shortly review relevant work on rhythmic
timing and introduce current accounts of the role of age in timing,
drawing on evidence from rhythmic and other timing functions.
Research on the role of age for rhythmic timing is grounded in
the literature on motor synchronization (Repp, 2005; Repp & Su,
2013) and relies on self-paced and continuation finger tapping
tasks. In a self-paced tapping task, participants are asked to tap
regularly without being exposed to a tapping stimulus. Hence, they
must find their own rhythm. In a continuation tapping task, par-
ticipants are given a rhythm and asked to continue its pace for
some time after the rhythm has stopped. Across both paradigms,
older age increases the variability of tap-to-tap intervals and de-
creases tapping speed (Baudouin, Vanneste, & Isingrini, 2004;
McAuley et al., 2006; Thompson, White-Schwoch, Tierney, &
Kraus, 2015; Turgeon & Wing, 2012; Turgeon, Wing, & Taylor,
2011). Moreover, these age effects are more pronounced for more
complex, anisochronous rhythms (Krampe, Engbert, & Kliegl,
2001, 2002; Krampe, Mayr, & Kliegl, 2005).
In addition to self-paced and continuation tapping some studies
explored paced tapping (Schirmer, Wijaya, Chiu, Maess, &
Gunter, 2020). Here participants are provided with a continuous
rhythm, which they are asked to follow. To date, studies adopting
this paradigm are very limited, and their results suggest that pacing
one’s own movement to a regular pacing signal remains well
preserved into older age (Turgeon et al., 2012; Turgeon et al.,
2011).
There is no consensus explanation of age effects on timing.
Some evidence suggests that timing deficits are a byproduct of
general functional decline. Supporting this possibility is research
exploring the relationship between timing and cognitive perfor-
mance. A study of 647 participants ranging in age from 18 to 67
years used a variety of timing tests that revealed a negative
correlation between timing performance and age (Bartholomew,
Meck, & Cirulli, 2015). Importantly, this correlation disappeared
1185
after the researchers controlled for cognitive performance. Studies
that directly manipulated the cognitive effort associated with a
timing or secondary task corroborated these results (Droit-Volet,
Lorandi, & Coull, 2019; Meijer & Krampe, 2018). Age differences
depended largely on an explicit instruction to time or on the
demands of a secondary task, thus suggesting that they reflect a
more general cognitive deficit and that timing itself may be a
fundamental primitive activity that remains fairly preserved later
in life (Droit-Volet et al., 2019).
Yet the absence of evidence for age effects on a timing-specific
mechanism is not evidence that such effects do not exist. More-
over, some findings do point to an internal clock that declines with
age. For example, an age-related decrease in spontaneous motor
tempo has been interpreted as a reduction in clock speed (Turgeon
et al., 2012). Changes in the temporal discrimination threshold
support this view (Ramos, Esquenazi, Villegas, Wu, & Hallett,
2016). In line with a slowing clock, for every additional year of
age, individuals required, on average, an additional 0.66 ms to
discriminate between two successive stimuli (Ramos et al., 2016).
In addition to speed, however, other clock mechanisms may be
implicated including, for example, the accuracy and reliability of
clock ticks (Turgeon et al., 2012) or the kind of information (e.g.,
previously learned vs. locally cued intervals) that biases temporal
decisions (Droit-Volet et al., 2019).
Behavioral evidence concerning an aging clock is comple-
mented by insights from neuroscience. Listening to an auditory
rhythm aligns and/or amplifies associated oscillations in neural
activity (Escoffier, Herrmann, & Schirmer, 2015; Schirmer et al.,
2020), and older age dampens this response (Sauvé, Bolt, Fleming,
& Zendel, 2019). Additionally, it appears that regions thought to
support timing show a pronounced age-related decline. Prominent
models of time perception consider a striatocortical network to be
central to our ability to perceive and represent temporal intervals
and rhythms (Buhusi et al., 2005; Leow & Grahn, 2014; Repp et
al., 2013). Moreover, age appears to compromise this network both
functionally and structurally (Wild-Wall, Willemssen, Falkenstein,
& Beste, 2008). Functional change entails, perhaps compensatory,
hyperactivity in a range of regions associated with higher-order
conceptual processing such as the middle/inferior frontal gyrus and
fusiform gyrus (Di, Rypma, & Biswal, 2014; Kleerekooper et al.,
2016). Structurally, gray matter volume (GMV) declines fastest in
sensorimotor regions in pre- and postcentral gyrus, inferior frontal
gyrus, and insula (Gorbach et al., 2017; Schippling et al., 2017;
Taki et al., 2013). Some studies, furthermore, highlight the caudate
(Bauer, Toepper, Gebhardt, Gallhofer, & Sammer, 2015; Di et al.,
2014; Taki et al., 2013), which forms part of the striatum. How-
ever, the locus within the caudate as well as the consistency with
which this structure is implicated vary.
To summarize, aging affects how we perceive, represent, and
interact with time. Yet we know little about the relation between
age and rhythmic timing and the mechanisms underlying age-
related timing deficits. It remains unclear whether and to what
extent such deficits result from a general decline in cognitive and
brain functioning or from emerging deficits in a dedicated clock
mechanism. Although the idea of an internal clock changing with
age is popular in neuroscience, there is still no evidence that
directly links age-related timing deficits to the brain system
thought to support timing.
 1186 SCHIRMER ET AL.
The present study was aimed at addressing this situation. Using
a paced tapping task thought to minimize cognitive demands
(Turgeon et al., 2016), we tested rhythmic synchronization in a
group of healthy older adults ranging in age from 62 to 83 years.
Participants were asked to tap regularly to the beats (not notes) of
one periodic and one more challenging syncopated auditory
rhythm. In the latter condition, only two of the four measure beats
were acoustically marked, which likely prompted internal and
more active temporal processes typically associated with self-
paced and continuation tapping. The comparison between the two
rhythms was used to isolate these processes while reducing a
contribution of timing-unspecific aspects of the task, including
auditory processing and motor preparation. We acknowledge that
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this two-rhythm manipulation probably entailed more general dif-
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ferences in task difficulty and consider this as a caveat in the
discussion.
Our goal was to expand on existing research in two ways. First,
published studies simply focused on the interta interval irrespec-
tive of how this interval aligned with the external rhythm (e.g.,
Bangert & Balota, 2012; McAuley et al., 2006; Tobin, Mador,
Guenther, Lodato, & Sackner, 1988; Turgeon et al., 2011; Van-
neste, Pouthas, & Wearden, 2001). Others also examined the
asynchrony between beats in the rhythm and the closest tap by
subtracting the former from the latter (Thompson et al., 2015).
Both approaches are problematic: the first because a person may
tap at a target rate but still be misaligned and this misalignment
would go unnoticed; the second because it makes the interpretation
of results challenging because ordinary averaging of subtraction
values may imply a convergence on the beat that is not actually
there. By adopting a circular statistics framework, the present
study circumvented these issues and elucidated two functional
properties of an alleged internal clock. The mean angle or asyn-
chrony between taps and the beat afforded insights into temporal
accuracy, whereas angular consistency from tap to tap afforded
insights into temporal reliability (Oprisan & Buhusi, 2013).
The second contribution of this study is the inclusion of both
cognitive and brain structural measures as to pin age effects to a
general functional and structural decline and/or a central clock
mechanisms supported by striatocortical loops (Buhusi et al.,
2005; Grahn & Brett, 2007; Merchant et al., 2015). Of primary
interest were changes in GMV, derived via structural magnetic
resonance imaging (MRI), and fractional anisotropy (FA), derived
via diffusion tensor imaging. GMV indexes the volume of neuro-
nal cell bodies present in the brain and, as discussed above, shows
a salient age-related reduction. FA indexes the directional anisot-
ropy of gray and white matter; that is, the degree to which there is
a preferred direction of water diffusion. As age changes the brain
by, for example, reducing neurite density (Cox et al., 2016) and
neurite orientation dispersion (Nazeri et al., 2015), age also
changes FA (Cox et al., 2016; Garcia-Lazaro, Becerra-Laparra,
Cortez-Conradis, & Roldan-Valadez, 2016; Nazeri et al., 2015;
Rathee, Rallabandi, & Roy, 2016).
Our hypotheses were as follows. In line with prior behavioral
work, we expected little or no age effects in tapping accuracy
and/or reliability for the periodic and strictly paced condition but
an age-related performance decline for the syncopated condition.
Thus, the performance difference between the periodic and the
syncopated rhythm was our main interest and was expected to
increase with age. Additionally, cognitive functioning, GMV, and
FA should show an age-related decline and explain the tapping
data. A mediation of age-related timing deficits via variation in
global cognitive functioning and brain structure would underline
the role of timing unspecific aging in the rhythmic tapping of older
adults. By contrast, an absence of such effects in the presence of a
mediation via striatocortical GMV/FA would support the idea that
such deficits engage aging of an internal clock.
Method
Participants
This experiment was part of a longitudinal study aimed at
investigating possible cognitive and health benefits of choral sing-
ing. All participants were interviewed in person by a trained nurse
prior to participation in this research and excluded if they self-
reported a hearing deficit or if such a deficit became apparent
during the interview. No standardized hearing assessment was
conducted. The project recruited 93 participants for a baseline
assessment and then assigned these individuals to an experimental
(choral singing) or a control (health education) group and assessed
them again after 1 year and 2 years. The data reported here were
collected during the baseline assessment. Specifically, a total of 71
participants performed the baseline tapping task and had artifact-
free baseline MRI recordings. Of those, one female participant
tapped less than 10 times in the two conditions and was excluded
from all analyses. The remaining participants had a mean age of
70.3 years (see Figure 1).
Of the final sample, 58 individuals were female and 12 were
male. Participants had a minimum of 0 and a maximum of 14 years
of education with a mean of 6 years. They reported having re-
ceived on average 1.6 years of formal musical training (vocal
and/or instrumental) with a range of 1–2.5 years. All participants
completed the Goldsmiths Musical Sophistication Index (Müllen-
siefen, Gingras, Musil, & Stewart, 2014). A performance histo-
gram of the summary score is illustrated in Figure 1. For analyses
detailing the relation between tapping and education/musical so-
phistication, please refer to the online supplementary materials.
Behavioral Procedure
This study was approved by the National University of Singa-
pore Institutional Review Board. All participants provided written
informed consent prior to study procedures commencing. An over-
view of the study paradigm is illustrated in Figure 2.
Participants performed a tapping task as part of their initial
study assessment. During the task, they sat in a quiet room on a
comfortable chair facing a laptop computer. The computer played
a simple periodic rhythm at a sound level that was clearly audible
and that could be adjusted if needed. The rhythm was presented by
a synthesized snare drum with a sound onset asynchrony of 750 ms
with four beats per measure for a total of 24 measures. Sound
intensity and duration, as measured with Praat (Boersma &
Weenink, 2013), were 0.18 Pa and 214 ms, respectively. The
sound had a rise time of 7 ms and a decay time of 185 ms. The total
duration of periodic tapping was 1.2 min. Participants were in-
structed to listen to the rhythm, and, when comfortable, to begin
tapping along to its perceived beat on the laptop’s space bar. They
were given 12 practice measures prior to the actual tapping task.
 NEUROCOGNITIVE STATUS AND TIMING IN THE ELDERLY
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Figure 1. Participant age and musicality. Illustrated on the left is the age distribution in the current sample, and
illustrated on the right is the musicality distribution as measured with the Goldsmiths Musical Sophistication
Index.
The Presentation software from Neurobehavioral Systems (https://
www.neurobs.com/) was used to present the rhythm and record the
timing of taps relative to the rhythm.
Following this simple tapping task, participants were presented
with a syncopated rhythm used previously (Escoffier et al., 2015;
Escoffier, Sheng, & Schirmer, 2010). This rhythm was played at
the same tempo as the isochronous rhythm. It comprised one
four-beat measure that was looped 24 times. Its first two beats
were regularly marked, its third beat was surrounded by a synco-
pation, and its fourth beat fell within a silent interval. Nevertheless,
all beats could be felt based on the rhythm’s overall structure. The
rhythm entailed a snare drum sound with 214.5 ms duration, 7 ms
rise time, 185 ms fall time and either 0.17 or 0.04 Pa. There was
also a bass sound with 224 ms duration, 9 ms rise time, 201 ms fall
time, and 0.17 Pa.
The reason for including this second tapping task was that it
required more sophisticated rhythmic processing and as such was
potentially more sensitive in the assessment of age and choir
training effects. Moreover, by comparing tapping to the beat (not
notes) of a syncopated and an isochronous rhythm, we sought to
isolate active temporal processes from more basic functions related
to auditory perception and motor programming. We tested the
syncopated rhythm after the isochronous rhythm because we an-
ticipated it being difficult and performance potentially too poor for
a circular analysis if participants had not already established the
beat for the simple rhythm.
Cognitive Assessment
On the first study visit, a trained nurse conducted a computer-
ized version of the Mini-Mental State Examination. Only two
participants had scores lower than 24, indicative of a mild cogni-
tive impairment. However, because their score fell just one point
below the cutoff, we decided to include these individuals in this
research.
On a separate day, a research assistant assessed each of the
participants again using paper-and-pen versions of the Digit Span
Test forward and backward, Block Design (from the Wechsler
Intelligence Scale; Wechsler, 1955), the Boston Naming Test
1187
(Kaplan, Goodglass, Weintraub, & Goodglass, 1983), the Color
Trail Test (Parts 1 and 2) (Maj et al., 1993), the Symbol Digit
Modality Test (Smith, 1973), and the Montreal Cognitive Assess-
ment (Nasreddine et al., 2005). All testing was done individually
in a quiet room.
Brain Imaging and Analysis
Brain imaging was conducted on a separate day at the National
University of Singapore Clinical Imaging Research Center using a
3-Tesla Siemens MRI machine. T1-weighted, magnetization-
prepared, gradient-echo images (MPRAGE) were acquired using
the following parameters: echo time ⫽ 2.03 ms, repetition time ⫽
2300 ms, flip angle ⫽ 9°, 1 mm3 isotropic voxel resolution, field
of view ⫽ 256 ⫻ 240 mm2 and 176 contiguous slices. Each
MPRAGE image was processed and segmented using FreeSurfer
version 6.0.0 (http://surfer.nmr.mgh.harvard.edu/).
An echo planar imaging sequence was used to acquire diffusion
weighted images (DWI) in 60 gradient directions with b values
ranging from 350 to 1600 mm/s, and one unweighted B0 image,
echo time ⫽ 96 ms, repetition time ⫽ 8,500 ms, 63 slices, field of
view ⫽ 192 mm, and 2 mm3 of voxel resolution. Diffusion images
were corrected for B0 field inhomogeneity, Gibbs artifacts, and
eddy-current distortions using MRtrix 3 and FSL 5.0 (http://fsl
.fmrib.ox.ac.uk). FA was computed by fitting a diffusion tensor to
DWI data using FSL FDT (https://fsl.fmrib.ox.ac.uk/fsl/fslwiki/
FDT). The B0 image was linearly coregistered to the MPRAGE,
and the inverse transformation was used to map gray matter and
white matter masks into DWI space. All scans were quality con-
trolled by an experienced researcher to reduce the impact of
motion artifacts. Two MPRAGE and three DWI scans were re-
moved because of motion artifacts. As mentioned above, affected
participants were excluded from the data analyses.
The analyses reported below were based on brain parcellations
following the method of Desikan and colleagues (Desikan et al.,
2006). For each parcellated region, we obtained mean GMV and
FA. To facilitate cross-measure comparison and to reduce the
number of statistical tests, no analyses were done on white matter
 1188 SCHIRMER ET AL.
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Figure 2. Stimuli and procedure. The upper panel illustrates the distribution of sounds for one measure in each
of the two stimulus rhythms. The colored bars mark the sound duration, and the black lines within each bar mark
the duration of the steady-state period. The magenta bar at 3,000 ms marks the first note of the next measure.
In the experimental blocks, measures were looped for 1.2 min. The lower panel illustrates the different study
phases. Initial screening interviews and cognitive testing were conducted on separate days prior to the actual
experiment. During the experiment, participants tapped along the tapping stimuli beginning with a short practice,
which was followed by two short experimental blocks comprised of 96 beats each. See the online article for the
color version of this figure.

FA. Instead we focused on gray matter FA, which was previously
shown to characterize brain development (Dudink et al., 2010;
Jonkman, Klaver, Fleysher, Inglese, & Geurts, 2016) and to have
a morphometric topological organization that resembles other
gold-standard connectivity approaches such as axonal tract tracing
(Seidlitz et al., 2018).
GMV and FA were analyzed as follows. For each measure, we
explored cortex and subcortical gray matter globally and for four
regions of interest (ROIs) including the caudate and putamen as
major components of the striatum as well as the lateral precentral
cortex (including supplemental and other motor-related areas) and
the auditory cortex as key cortical components of a striatocortical
system thought by some to support the rhythmic timing of auditory
events (Merchant et al., 2015; Teki, Grube, Kumar, & Griffiths,
2011). In addition to these ROIs, we explored a potential contri-
bution of a medial sensorimotor region (i.e., paracentral) and the
caudal anterior cingulate because of their role in conflict monitor-
ing (Jahn, Nee, Alexander, & Brown, 2016). We also examined the
cerebellum as another candidate region with potential relevance
for rhythmic timing (Ivry & Keele, 1989).
To control for general brain decline in our regional analyses, we
divided the GMV and FA of each cortical region by the GMV and
FA of all other cortex, excluding that region. The same was done
separately for subcortical regions such that measures were ex-
pressed as a ratio relative to other subcortical gray matter. We
separately controlled for cortical and subcortical global morphol-
ogy because they could be expected to show different aging
trajectories and, for FA, differed substantially, irrespective of age.
All global and globally controlled regional measures were then
separately normalized across participants to a mean of 0 and a
standard deviation of 1. This served to facilitate the detection of
outliers and the comparison of effects across regions. Participants
with scores deviating more than 3 SD from the mean were ex-
cluded from a given test.
 NEUROCOGNITIVE STATUS AND TIMING IN THE ELDERLY
Statistical Analysis
Statistical analyses were conducted in R (R Core Team, 2015)
and approached using a circular statistics framework in which time
is not a linear but a circular phenomenon (for an introduction see
Cremers & Klugkist, 2018). Such an approach is particularly
suited for data with regular temporal recurrence like, for example,
the recurrence of days, months, years, and, in this present case, a
beat. Specifically, the present stimuli were characterized by a
recurrent beat at 750 ms, which we mapped onto 360° with the
0/360° position coinciding with the beat.
To accomplish this, we centered our interbeat interval at each
beat to obtain a beat-locked analysis window extending from 375
ms before to 375 ms after each beat. For each participant and
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condition, we then aggregated taps falling within this window
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using the mean.circular function (to compute the mean angle
relative to the beat) and the rho.circular function (to compute the
mean resultant vector length from the individual angles, i.e., the
consistency of angles) of the circular package (Agostinelli & Lund,
2017). The first variable is referred to as tapping asynchrony and
the second variable as tapping consistency. Tapping asynchrony
reflects the extent to which tapping angles differ from 0/360°, the
beat position. Note that within a linear framework, taps falling
symmetrically below ⫺187 and above ⫹ 187 ms (i.e., 270° and
90°) would yield a misleading tapping average coinciding with the
beat position. By contrast, within a circular framework, they would
more appropriately produce a mean tapping angle of 180°, the
farthest point away from the beat. Moreover, taps falling directly
at ⫺187 and ⫹ 187 ms would fail to produce a central tendency
because their resultant vector length would be 0. The term tapping
consistency describes the resultant vector length. It marks the
degree to which tapping angles were the same from tap to tap.
Tapping asynchrony, a circular variable, was explored using a
circular-linear regression analysis implemented in the circular
package. Tapping consistency was explored using a linear-linear
regression analysis. In both cases, the tapping measure served as
the dependent variable.
The present study also explored global and regional GMV and
FA. Regional analyses entailed seven tests, one for each region
examined here, thus increasing type I error. Therefore, we cor-
rected the p value of regional analyses using the p.adjust function
from the stats package with the false discovery rate (FDR; Ben-
jamini & Hochberg, 1995) setting (R Core Team, 2015). Where
relevant, we provide 95% confidence intervals.
Results
Effects of Age on Tapping Performance
Tapping asynchrony. The relation between age and tapping
performance is illustrated in Figure 3. Because we opted for a
circular statistics approach, we first used a Rayleigh test (for
nonuniformity) with mu set to 0 to determine whether tapping
clustered unimodally around 0, the beat position. This was the case
for the periodic (R ⫽ .45, p ⬍ .0001, confidence interval [CI:
0.3060, 0.5989]) and, but to a lesser degree, in the syncopated
condition (R ⫽ .24, p ⫽ .002, CI [0.0795, 0.4068]). To test
condition differences, we computed the mean angle for each par-
ticipant and rhythm on a scale ranging from ⫺␲ to ␲, with 0 again
1189
as the beat position. We then subtracted mean angles of the
syncopated from the periodic condition. To ensure that the result
had the original range of ⫺␲ to ␲, we subtracted 2 ␲ if the angular
difference was greater than ␲ and added 2 ␲ if the angular
difference was smaller than ⫺␲. Last, we tested whether the
resulting values differed significantly from 0 using a bootstrap
approach with 5,000 repetitions (Canty & Ripley, 2017). This
indicated that the mean angle in the periodic condition differed
significantly from that in the syncopated condition (CI of angular
difference ⫽ ⫺1.72 to ⫺.75).
Regression analyses exploring age differences in tapping angles
revealed a significant effect for the periodic condition (ß ⫽ .01,
SE ⫽ .002, p ⬍ .0001). With increasing age, participants were less
likely to tap at an optimal prebeat position and more likely to tap
with delay at or after the beat. Also for the syncopated condition
did age predict tapping (ß ⫽ ⫺.01, SE ⫽ .004, p ⫽ .0003).
However, as illustrated in Figure 3, the mean tapping angles of
younger participants clustered shortly after the beat position,
whereas older participants tended to tap earlier with the oldest
individuals being almost half a period too early. Importantly, the
angular difference between the periodic and the syncopated con-
dition failed to differ as a function of age (ß ⫽ .0002, SE ⫽ .002,
p ⫽ .136).
Tapping consistency. We examined tapping consistency by
computing for each participant the mean resultant length of the
vector derived from tapping angles in the periodic and the synco-
pated condition and by subjecting both sets of scores to a paired t
test. Tapping consistency was greater in the periodic (0.625)
compared with the syncopated condition (0.238, difference CI
[.306, .468]; t[69] ⫽ 9.55, p ⬍ .0001).
The relationship between age and tapping consistency is illus-
trated in Figure 3. To examine this relationship, we conducted a
regression analysis with tapping consistency as the dependent
variable and age as the independent variable for each rhythm
condition and the condition difference. For the periodic condition,
we found a significantly negative relationship (ß ⫽ ⫺.014, SE ⫽
.007, p ⫽ .044), indicating that older age was associated with less
consistent tapping. For the syncopated condition, the effect sur-
prisingly reversed (ß ⫽ .01, SE ⫽ .005, p ⫽ .0423). Moreover, the
difference in tapping consistency derived by subtracting the syn-
copated from the periodic score correlated negatively with age
(ß ⫽ ⫺.02, SE ⫽ .007, p ⫽ .001). Thus, with increasing age,
participants were less likely to show a reduction in tapping con-
sistency from the periodic to the more difficult syncopated rhythm
condition.
Effects of Age on Cognition and Brain Morphology
Cognition. Cognitive test results and exploratory correlation
analyses (p uncorrected) with age and tapping are presented in
Table 1.
The nine test results were normalized to a mean of 0 and a
standard deviation of 1. The normalized values were subjected to
a principal component analysis. Tests for which a greater score
reflected better performance loaded positively and tests for which
a greater score reflected weaker performance loaded negatively on
the first principal component, which accounted for 50% of the total
variance (with other components accounting for 18.5% or less).
We then normalized the participants’ individual scores for this first
 1190 SCHIRMER ET AL.
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Figure 3. Age effects on rhythmic timing (top row). Distribution of taps around beats in a measure. The 0
position indicates the time of the beat. The time between beats is expressed in degrees. Mean participant tapping
angles are illustrated as rose petals using transparent colors. The larger the petal the more participants had a mean
tapping angle at this position. Participants were sorted by age and divided into three nonoverlapping age groups
of similar size. The groups are marked with different colors (middle row). Age is plotted as a function of tapping
asynchrony expressed as the mean tapping angle for each participant. In blue we show a polynomial regression
line with one quadratic term (lm[Age ⬃ poly(Angle,2)])—which facilitates the illustration of circular data if
angles are plotted on the x-axis (bottom row). Age is plotted as a function of tapping consistency. The tapping
consistency measure rho varies between 0 and 1, with larger values indicating greater consistency. A linear
regression line is shown in blue. See the online article for the color version of this figure.

component, confirmed the absence of outliers (more than 3 SD
away from the mean), and used the normalized scores for all
analyses reported below.
A simple linear regression of age against the summary cognitive
score indicated that older age was associated with weaker cogni-
tive performance (ß ⫽ ⫺2.47, SE ⫽ .56, p ⬍ .0001, ␩p2 ⫽ .22,
Figures 4 and 5).
Gray matter volume. To analyze the relation between age
and brain morphology, we conducted a series of univariate linear
regression analyses with a given brain measure as the dependent
variable and age as the independent variable. As mentioned above,
for each analysis we removed outliers for whom one or more
variables exceeded 3 SD from the mean. This concerned the
analysis of premotor cortex (N ⫽ 1), caudate (N ⫽ 2), and
cerebellum (N ⫽ 1).
An analysis of age effects on global GMV revealed a negative
relationship for both the cortex (ß ⫽ ⫺.06, SE ⫽ .02, p ⫽ .012, ␩p2 ⫽
.088) and subcortical matter (ß ⫽ ⫺.04, SE ⫽ .02, p ⫽ .046, ␩p2 ⫽
.057). An analysis of age effects on our ROIs revealed a negative
relationship for auditory cortex (ß ⫽ ⫺.06, SE ⫽ .02, pFDR ⫽ .036,
 NEUROCOGNITIVE STATUS AND TIMING IN THE ELDERLY 1191

Table 1
Cognitive Control Measures

Correlations with other variables

Tapping asynchrony Tapping consistency
Test M (range) Age PC1 Per Syn Dif Per Syn Dif
ⴱ
MMSE 28.2 (23–30) ⫺.15 .22 ⫺.06 .22 .17 .08 .01 .07
Digit span forward 10.44 (5–16) ⫺.29ⴱ .34 ⫺.06 ⫺.07 ⫺.06 .03 ⫺.01 .04
Digit span backward 5.9 (2–14) ⫺.29ⴱ .34 ⫺.06 ⫺.07 ⫺.06 .03 ⫺.01 .04
Block design 26.9 (3–45) ⫺.44ⴱⴱⴱ .35 ⫺.03 .29ⴱ .03 .11ⴱⴱ ⫺.007 .12ⴱⴱ
Boston naming 21.7 (10–30) ⫺.32ⴱⴱ .35 ⫺.02 ⫺.34ⴱ .22ⴱ .08ⴱ ⫺.02 .1ⴱ
Color trail test part 1 69 (33–184) .33ⴱⴱ ⫺.34 ⫺.07 ⫺.15 ⫺.1 ⫺.09ⴱ .004 ⫺.09ⴱ
Color trail test part 2 139 (63–270) .38ⴱⴱ ⫺.38 ⫺.01 ⫺.39ⴱⴱ .1 ⫺.09ⴱ ⫺.02 ⫺.06
Symbol digit modalities test 38.7 (9–63) ⫺.56ⴱⴱⴱⴱ .39 .01 .3ⴱ .2 .11ⴱⴱ ⫺.02 .13ⴱⴱⴱ
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Montreal cognitive assessment 85.4 (57–100) ⫺.13 .24 ⫺.11 ⫺.41ⴱ .22 .04 ⫺.02 .07
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Note. PC1 ⫽ first principal component of the principal component analysis done on the cognitive measures; Per ⫽ periodic rhythm condition; Syn ⫽
syncopated rhythm condition; Dif ⫽ syncopated minus periodic condition difference; MMSE ⫽ Mini-Mental State Examination.
ⴱ
p ⬍ .05. ⴱⴱ p ⬍ .01. ⴱⴱⴱ p ⬍ .001. ⴱⴱⴱⴱ p ⬍ .0001.

␩p2 ⫽ .11, other psFDR ⬎ .209), indicating that this region declined
above and beyond the rest of the brain. For the considered regions, we
observed a numerical age-related increase in caudal anterior cingulate
that did not reach conventional standards for significance (ß ⫽ .05,
SE ⫽ .02, pFDR ⫽ .082, ␩p2 ⫽ .073). Likely this region remained fairly
intact with age, thus tending to be proportionately larger for older
individuals in whom other brain regions had declined. Other explor-
atory analyses yielded nonsignificant results (psFDR ⬎ .35).
Fractional anisotropy. The relation between age and FA was
pursued as described for the relation between age and GMV. For two
participants no FA measures were available, reducing the sample to
68. Outliers were identified for auditory cortex (N ⫽ 1) and excluded
from analysis.
Age negatively predicted overall subcortical (ß ⫽ ⫺.05, SE ⫽ .02,
p ⫽ .037, ␩p2 ⫽ .064) but not cortical FA (ß ⫽ ⫺.04, SE ⫽ .02, p ⫽
.107, ␩p2 ⫽ .039), albeit both parameters showed a fairly similar
pattern. Older age was numerically positively associated with a
greater caudate FA, albeit the effect failed to reach significance (ß ⫽
.06, SE ⫽ .02, pFDR ⫽ .079, ␩p2 ⫽ .093). As overall subcortical FA
declined, caudal FA probably remained fairly intact. Effects were
nonsignificant for all other ROIs (psFDR ⬎ .588) and the exploratory
regions (psFDR ⬎ .588).

Figure 4. Age effects on cognitive functioning (first principal component), global brain GMV, and FA as well
as proportional region-specific GMV and FA. The y-axis shows the normalized score range. GMV ⫽ gray matter
volume; FA ⫽ fractional anisotropy; ROI ⫽ regions of interest; AC ⫽ anterior cingulate. See the online article
for the color version of this figure.
 1192 SCHIRMER ET AL.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
Age 1
Periodic Tapping Consistency 2
Per-Syn Tapping Consistency 3
Cognitive Score 4
Cortical GMV 5
Subcortical GMV 6
Auditory GMV 7
Premotor GMV 8
Paracentral GMV 9
Caudal AC GMV 10
Caudal GMV 11
Putamen GMV 12
Cerebellar GMV 13
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Cortical FA 14
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Subcortical FA 15
Auditory FA 16
Premotor FA 17
Paracentral FA 18
Caudal AC FA 19
Caudal FA 20
Putamen FA 21
Cerebellar FA 22
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22

Figure 5. Correlation matrix illustrating the relationship between age and the different linear variables
measured in this study. Numbers above the diagonal show the Pearson correlation coefficient and indicate the
significance of p values smaller than .001, .01, .05 and .1 with symbols ⴱⴱⴱ, ⴱⴱ, ⴱ, and ., respectively. Font size
and correlation coefficient size are proportionate. The diagonal shows the variable distribution. Below the
diagonal are dot plots with a robust locally weighted regression fit indicated in red. GMV ⫽ gray matter
volume; FA ⫽ fractional anisotropy; AC ⫽ anterior cingulate. See the online article for the color version
of this figure.

Mediation of Age Effects on Rhythmic Timing
We conducted a series of mediation analyses to explore the role
of cognitive functioning, GMV, and FA in explaining age-related
changes in tapping performance. For tapping asynchrony, a circu-
lar variable, we relied on the approach developed by Baron and
Kenny (1986) using an in-house– developed R function. For tap-
ping consistency, we used the mediate function from the mediation
package (Tingley, Yamamoto, Hirose, Keele, & Imai, 2014). Be-
cause our cognitive and brain measures were correlated (see Figure
5), we did not pursue them jointly but instead conducted separate
analyses.
For the analysis of brain measures, we first conducted a
principal component analysis to reduce data dimensionality and
the number of tests (two participants without FA scores were
excluded from this analysis). The global measures of cortical
and subcortical GMV and FA entered this analysis, resulting in
a total of four input variables. All variables loaded negatively
on the first principal component (cortexGMV ⫽ ⫺.51; subcor-
texGMV ⫽ ⫺.54, cortexFA ⫽ ⫺.39; subcortexFA ⫽ ⫺.53),
which accounted for 64% of the variance (other components
accounted for 22% or less). To facilitate its interpretation, we
switched the component sign and subjected the result to two
Pearson correlation analyses with age (r ⫽ ⫺.32, df ⫽ 66, p ⫽
.008) and cognitive functioning (r ⫽ .32, df ⫽ 66, p ⫽ .008,
respectively). The results indicated that the resigned component
scores predicted age and cognitive functioning in the expected
directions. We hence proceeded to use the resigned component
as a global brain measure in the following analyses. Addition-
ally, we probed auditory GMV as the only regional measure
significantly negatively related with age.
Periodic rhythm. Focusing on the periodic condition, we
observed an effect of age on both tapping asynchrony and consis-
tency and hence pursued both. Please see Figures 6 and 7 for an
illustration of the relation between tapping and the various indi-
vidual brain measures. For an illustration of the relation between
tapping and the cognitive summary score, please refer to the online
supplementary materials.
Age effects on tapping asynchrony approached significant me-
diation via cognitive functioning (rdiff ⫽ .074, CI [⫺.007, .22],
p ⫽ .062) but not via global brain morphology (p ⫽ .158) and
auditory GMV (p ⫽ .389).
Analysis of tapping consistency pointed to a mediation via the sum-
mary cognitive score (ß ⫽ ⫺.008, CI [⫺.018, ⫺.0002], p ⫽ .043) and
global brain morphology (ß ⫽ ⫺.005, CI [⫺.012, ⫺.0003], p ⫽ .038).
Effects were nonsignificant for auditory GMV (p ⫽ .88).
Periodic minus syncopated rhythm. Focusing on perfor-
mance differences between the periodic and the syncopated
rhythm, we observed nonsignificant age effects for tapping asyn-
chrony making a mediation analysis moot. However, tapping con-
sistency was affected by age and thus pursued.
The analysis with age as the independent variable, the cognitive
score as the mediator, and the condition difference in tapping
consistency as the dependent variable returned a small indirect
effect that, although nonsignificant (ß ⫽ ⫺.006, p ⫽ .078,
 NEUROCOGNITIVE STATUS AND TIMING IN THE ELDERLY 1193
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Figure 6. Cognitive functioning (first principal component) and brain morphology in relation to tapping
asynchrony. Lines represent a polynomial (quadratic) fit. GMV ⫽ gray matter volume; FA ⫽ fractional
anisotropy; AC ⫽ anterior cingulate; ROI ⫽ regions of interest. See the online article for the color version of
this figure.
 1194 SCHIRMER ET AL.
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Figure 7. Brain morphology and its relation to tapping consistency. Lines represent a linear fit. GMV ⫽ gray
matter volume; FA ⫽ fractional anisotropy; AC ⫽ anterior cingulate; ROI ⫽ regions of interest. See the online
article for the color version of this figure.
 NEUROCOGNITIVE STATUS AND TIMING IN THE ELDERLY
CI [⫺.015, .0007]), hinted that cognitive functioning may not be
irrelevant in explaining age deficits in tapping consistency. There
was also small and significant indirect effect via global brain
morphology (ß ⫽ ⫺.004, p ⫽ .041, CI [⫺.01, ⫺.0002]). Media-
tion via auditory GMV was nonsignificant (p ⫽ .322).
Exploring the Neural Underpinnings of Rhythmic
Tapping
Because tapping performance may have been shaped by age-
irrelevant differences in brain morphology, we subjected tapping
asynchrony and consistency to an additional set of analyses ad-
dressing their relation with measures of brain morphology. Our
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focus here was on explaining tapping differences between the
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syncopated and the periodic condition using a simple regression
approach with the tapping measure as the dependent variable and
the global or ratio-corrected regional GMV and FA as the inde-
pendent variable.
Analysis of the relation between tapping asynchrony and the
brain emphasized regional over global effects, especially for FA.
For GMV, we obtained nonsignificant effects for subcortical re-
gions (ß ⫽ .17, SE ⫽ .13, p ⫽ .098) and cortical regions globally
(p ⫽ .335). Among our ROIs, the putamen seemed most relevant,
albeit its effect was also nonsignificant (ß ⫽ ⫺.24, SE ⫽ .13,
pFDR ⫽ .092; other psFDR ⬎ .423). Similarly, among our explor-
atory regions, the cerebellum seemed most relevant but again
effects were nonsignificant (ß ⫽ .32, SE ⫽ .14, pFDR ⫽ .092; other
psFDR ⬎ .423). For FA, we found nonsignificant global effects
(ps ⬎ .409). Among our ROIs, premotor cortex (ß ⫽ ⫺.34, SE ⫽
.15, pFDR ⫽ .039) and caudate (ß ⫽ .33, SE ⫽ .13, pFDR ⫽ .039;
other psFDR ⬎ .224) were significant. Our exploratory analyses
revealed a significant effect in the paracentral region (ß ⫽ .29,
SE ⫽ .14, pFDR ⫽ .041) with no other effects (psFDR ⬎ .158).
Tapping consistency emphasized global over regional effects,
again especially for FA. For GMV, the global effect was signifi-
cant for subcortical (ß ⫽ .09, SE ⫽ .04, p ⫽ .021) but not cortical
matter (p ⫽ .165). No effect showed among our ROIs (psFDR ⬎
.481). Effects were also nonsignificant for our exploratory regions
(psFDR ⬎ .609). For FA, the global effect was significant for both
subcortical (ß ⫽ .11, SE ⫽ .04, p ⫽ .009) and cortical matter (ß ⫽
.09, SE ⫽ .04, p ⫽ .021). Again, all ROI and exploratory analyses
were nonsignificant (psFDR ⬎ .331).
Discussion
This study examined the aging timer by exploring temporal
performance in conjunction with more general cognitive function-
ing and brain morphology. In the following discussion, we first
describe how age predicted rhythmic tapping in the present sam-
ple. We then reflect on the association between age and cognitive
as well as brain structural measures and discuss the role of timing-
specific and general mental processes in explaining our ability to
time events in late adulthood.
Age Differences in Rhythmic Timing
We examined tapping performance in the present experiment
using a circular statistics approach. Thus, rather than looking
simply at the duration of tap-to-tap intervals, we considered the
1195
beats of our stimulus rhythm to fall on the 0 mark of a circle and
determined the angle between that mark and taps. In this manner,
we measured not only whether participants tapped at an interval
corresponding to the interbeat interval but also whether tapping
was beat aligned. Our summary statistics yielded, for each partic-
ipant, (a) a mean tapping angle reflecting tapping asynchrony or
the mean accuracy of finding the beat and (b) tapping consistency
reflecting tap-to-tap differences in angle and thus temporal reli-
ability.
Contrary to previous reports (Turgeon et al., 2012; Turgeon et
al., 2011), examination of tapping to a periodic rhythm revealed
age effects. Tapping to a consistently marked beat, a relatively
simple task, became harder with increasing age. Whereas our
youngest individuals were likely to tap shortly before the beat,
indicating that they could anticipate its occurrence (Leow et al.,
2014; Repp et al., 2013), this likelihood decreased in older partic-
ipants. Additionally, older participants tapped less consistently.
The difference between the present and previous findings for
paced tapping may be due to the advantages associated with
circular statistics.
We explored performance differences between the periodic and
syncopated rhythms as to probe the possibility of an internal clock
mechanism deteriorating with age. Compared with the periodic
rhythm, the syncopated rhythm engaged similar sensory and motor
processes but was temporally more challenging because the beat
was not consistently marked. In conflict with our predictions,
however, age effects for the condition difference were nonsignif-
icant for tapping asynchrony and opposite expectation for tapping
consistency.
Given these results we reason that the mean accuracy of rhyth-
mic tapping remains fairly preserved in older age and that its
underlying temporal function might well be a psychological prim-
itive (Droit-Volet et al., 2019). Indeed, age differences in the
periodic condition are a likely index of processes secondary to
timing that will be discussed in more detail below. By contrast, age
does not seem to spare the reliability of rhythmic tapping. When
tapping to an easy rhythm, the interval between taps increasingly
varied in older relative to younger participants. When tapping to
the more difficult rhythm, for some older participants, consistency
could not decrease further because of a floor effect. For others,
difficulty may not have mattered because of impoverished auditory
representations, reducing distraction from off-beat acoustic ele-
ments. Thus, with increasing age, the difference between periodic
and syncopated tapping consistency decreased.
Age Difference in Cognition and Brain Morphology
Apart from examining tapping, we assessed participants on a
range of cognitive measures and used a principal component
approach to identify shared variance representative of an individ-
ual’s overall cognitive status. Additionally, we quantified the
participants’ brain integrity as reflected by GMV and FA for the
whole brain and for four regions with potential relevance for an
internal clock. As expected, age and cognitive status were strongly
negatively related. Additionally, age negatively predicted GMV
and FA globally—albeit effects were relatively weak. Both brain
measures indexed a fairly broad decline and the only regional
measure surpassing this was auditory GMV.
 1196 SCHIRMER ET AL.
The observed age effects on auditory GMV corroborate existing
work highlighting that sensory processing declines with age (Jaya-
kody, Friedland, Martins, & Sohrabi, 2018; Lalwani et al., 2019).
However, that striatal decline failed to exceed that of other brain
regions with respect to GMV and FA seems at odds with previous
evidence (Bauer et al., 2015; Di et al., 2014; Taki et al., 2013). For
caudal FA in particular, we observed a numerically positive age
effect that, although nonsignificant, may index caudal integrity in
older age. A potential explanation is that the present approach
presents a more stringent test of regional decline relative to what
has been done before. Our sample was substantially larger than the
samples of most earlier studies and we used a continuous measure
rather than an extreme group design (e.g., Bauer et al., 2015; for a
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meta-analysis see Di et al., 2014). We also tested whether ROIs
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declined above and beyond the decline seen elsewhere in the brain.
Thus, the present results are perhaps more robust and informative
as concerns an accelerated striatal deterioration. Yet we acknowl-
edge that such a conclusion must remain tentative until probed
with a wider age range, including middle-aged adults (Taki et al.,
2013).
Mechanisms Underpinning Age Effects on Rhythmic
Timing
The present study identified age effects on measures of asyn-
chrony and consistency in the periodic tapping condition and on
measures of consistency for the condition difference. In an effort
to explore a potential role of cognitive and brain changes in
explaining these effects, we conducted a series of mediation anal-
yses.
Analysis of tapping asynchrony revealed that age effects in the
periodic condition were clearly unrelated to global GMV and only
weakly explained by general cognitive functioning and global FA
with effects failing to meet the traditional threshold of signifi-
cance. Moreover, results were nonsignificant for auditory cortex—
the only region that deteriorated above and beyond the deteriora-
tion seen globally. Unlike for the periodic condition, age had a
nonsignificant effect on the asynchrony difference between the
periodic and the syncopated condition. Thus, no mediation was
pursued.
We speculate that changes in tapping to a periodic and synco-
pated rhythm with increasing age reflect a fairly circumscribed
motor slowing as reported previously (Falkenstein, Yordanova, &
Kolev, 2006). Indeed, early work has differentiated motor from
cognitive timing processes and raised the possibility that the for-
mer could be affected without the latter (Ivry & Hazeltine, 1995).
The absence of age effects for the condition difference converges
with evidence that this difference is unrelated to more general
cognitive functioning (online supplementary materials). It suggests
that the accuracy of rhythmic timing, thought to be highlighted by
the condition difference, remains fairly unaffected by ongoing
cognitive and brain structural decline.
Our mediation results for tapping consistency were fairly com-
parable for the periodic condition and the condition difference. The
first principal components derived from combining the different
cognitive measures and from combining the different brain mea-
sures, respectively, statistically accounted for the age-related in-
crease in tapping variation in the periodic condition and the age-
related reduction in the difference in tapping variation between the
periodic and the syncopated condition. Please note, however, that,
although consistent, these effects were small and hovered above
and below the traditional significance threshold of p ⫽ .05. Au-
ditory GMV was again statistically irrelevant.
On this backdrop, we conclude that global changes in mental
functioning and their brain basis underpin age-related changes in
tapping consistency. As discussed farther below, this could entail
a decline in the reliability of an internal clock. Additionally,
tapping consistency may be affected by changes in not strictly
temporal processes including, for example, sensorimotor represen-
tations, which may have been more demanding in the syncopated
than the periodic condition.
Insights into the Brain Substrate of Rhythmic Timing
Different opinions exist as to how temporal processing is im-
plemented in the human mind and brain. According to one popular
perspective (Gibbon, Church, & Meck, 1984; Treisman, Faulkner,
Naish, & Brogan, 1990), humans possess a specialized timing
module that, in its simplest form, consists of a pacemaker emitting
pulses, which are then accumulated in memory and form the basis
for temporal decisions. An attentional switch connecting pace-
maker and accumulator may be in a closed or opened state, thus
determining whether pulses are successfully stored (Lejeune,
1998). Within this framework, timing depends on timing specific
processes but interfaces with more general cognitive functions
such as attention and memory.
Another popular perspective sees time as an emergent property
of more general mental functioning (for a review see Coull, Cheng,
& Meck, 2011). Object specific mental operations simply have
time as an additional dimension. Thus, for example, auditory
processing engenders the temporal representation of sounds (Jant-
zen, Steinberg, & Kelso, 2004, 2005). Whereas the first perspec-
tive allows for age to alter temporal performance in a multimodal
manner, potentially preserving a core timer, the second perspective
accommodates modality-specific deficits but holds that associated
performance deficits are pervasive in that they affect both timing
accuracy and reliability.
To address these possibilities, we explored the relation between
rhythmic tapping and brain morphology both as a function of age
as reported above and independently of age. The latter was based
on the rational that there may be age-unrelated individual variation
in brain morphology that could help us further specify the neural
underpinnings of rhythmic timing. Examination of asynchrony
differences between the periodic and the syncopated rhythm re-
vealed a nonsignificant global effect for both GMV and FA.
However, when controlling for global brain measures, premotor,
caudal, and paracentral FA emerged as relevant with small effects
for GMV in the putamen and cerebellum that did not cross signif-
icance. By contrast, examination of consistency differences be-
tween the periodic and the syncopated rhythm revealed significant
global effects for GMV and, more robustly, for FA. Regional
effects, however, were nonsignificant.
Together these results converge with the age effects reported
above and disagree with the notion of a distributed and function-
ally embedded timing system supporting object-specific temporal
representations. Indeed, the auditory cortex, which would have
supported rhythm perception here, showed pronounced changes
with age but failed to predict rhythmic tapping. Instead, our
 NEUROCOGNITIVE STATUS AND TIMING IN THE ELDERLY
findings corroborate the existence of a dedicated central timer that
interfaces with other mental processes (Gibbon et al., 1984; Tre-
isman et al., 1990). As suggested elsewhere and supported by the
present data, such a timer might depend on striatocortical circuitry
(Leow et al., 2014) and the striatal integration of cortical processes
as proposed by the striatal beat frequency model (Buhusi et al.,
2005; Matell & Meck, 2004; Oprisan & Buhusi, 2011, 2013;
Petter, Lusk, Hesslow, & Meck, 2016). This latter model offers a
physiologically plausible framework for how a central timer might
be implemented in the brain. It assumes a role for dopaminergic
neurons in the ventral tegmental area to synchronize cortical
activity. Medium spiny neurons within the striatum are believed to
monitor cortical synchronization and the ensuing relaxation of
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phase coherence. As such, these neurons are believed to integrate
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temporal information and to register the passage of time.
Based on the present results and in line with current perspec-
tives, different processes may underpin the accuracy and the reli-
ability of rhythmic timing. We speculate that timing accuracy
depends largely on the integrity of striatal mechanisms and their
interaction with the cortex. However, given that we also identified
timing accuracy effects in the paracentral area and, but nonsignifi-
cantly, in the cerebellum, a striatocortical system likely interacts
with both timing-specific and -unspecific processes in other parts
of the brain. The reliability of rhythmic timing may be a function
of noise present globally in both cortical and subcortical oscilla-
tory patterns (Oprisan & Buhusi, 2011, 2013). Thus, aging, which
emphasizes global over localized striatal decline, may be less
detrimental to the mean accuracy than to the reliability of internal
time.
Caveats and Future Directions
Before closing, we want to highlight a few caveats associated
with the present study that limit our conclusions. First, this work
would have benefited from an assessment of sensory and motor
functions. Apart from timing-specific and -unspecific cognition,
tapping performance also depended on the participants’ hearing as
well as motion planning and execution. Because both domains
decline with age, they create additional performance challenges
that could have impacted the present results. Please note, however,
that their impact would have been more severe for the periodic
tapping results than the tapping difference between the periodic
and the syncopated condition because the latter would reduce
impact from timing unspecific processes.
A second shortcoming concerns our comparison of tapping with
a periodic with tapping to a syncopated rhythm. Although this
comparison offered a range of advantages as detailed in the intro-
duction, we cannot exclude the possibility that it also captured
nontemporal processes. For example, some of the difficulty asso-
ciated with the syncopated rhythm may have been due to a natural
bias to tap at a sounding rather than a silent moment. For the
syncopated rhythm, such a bias would have created a response
conflict (Praamstra, Turgeon, Hesse, Wing, & Perryer, 2003) that
participants would have needed to suppress on some but not other
points in a measure. Although we cannot rule out this possibility,
the following observations make it unlikely. For one, impairments
in tapping accuracy and reliability for the syncopated relative to
the periodic condition failed to increase with age. Yet such an
increase should have materialized if a response conflict contrib-
1197
uted to the condition difference. This is because it is well estab-
lished that older age makes the suppression of unwanted responses
harder (Bialystok, Craik, Klein, & Viswanathan, 2004; Juncos-
Rabadán, Pereiro, & Facal, 2008). Additionally, we explored a role
of conflict-monitoring regions (i.e., paracentral, caudal anterior
cingulate) in the association between age and the performance
differences between the periodic and syncopated rhythm obtaining
nonsignificant results. We observed only a paracentral FA effect
on tapping accuracy, irrespective of age. Moreover, both paracen-
tral area and cingulate played no special role in accounting for
tapping consistency, which instead showed a robust dependency
on global brain integrity. Nevertheless, future research should use
a continuation tapping task, which rules out the possibility of a
response conflict contributing to task performance.
Third, it is important to acknowledge shortcomings associated
with the between-subjects design implemented here. For one, age
was nonuniformly distributed, with fewer participants in the higher
age range, thus potentially compromising power. Additionally,
results may have been affected by other variables that vary within
our sample such as education or musical sophistication. This can
be addressed with a cohort design that follows up the same group
of individuals for a number of years. Apart from being challenging
to set up, however, such an approach has other issues including
study dropouts.
Lastly, we want to highlight that the present study focused on
only one of possibly two different timing modes. Apart from the
rhythmic timing examined here, studies have explored the timing
of intervals by, for example, asking participants to judge or repro-
duce a stimulus duration (Lui, Penney, & Schirmer, 2011; Penney,
Gibbon, & Meck, 2000; Schirmer, Ng, Escoffier, & Penney, 2016).
At present, opinions divide as to whether rhythmic and interval
timing can and should be theoretically differentiated. There are
proposals of both being separate functions supported by segregated
brain circuitry (Grahn & Brett, 2009; Grube, Cooper, Chinnery, &
Griffiths, 2010; Teki, Grube, & Griffiths, 2012; Teki et al., 2011).
However, other proposals, like the striatal beat frequency model,
consider them in an integrated manner, assuming that rhythms
depend on the representation of intervals, thus making it impossi-
ble to meaningfully separate the two (Buhusi et al., 2005;
Schirmer, Meck, et al., 2016; Turgeon et al., 2016). On this
backdrop, future research is needed to determine whether the
present findings characterize rhythmic timing specifically or speak
to timing more broadly.
Conclusions
Here we explored whether and how cognitive and brain struc-
tural measures explain rhythmic tapping in a group of aging adults.
Focusing on the difference between a periodic and a syncopated
rhythm, we found the mean timing accuracy to remain fairly intact
with older age. Additionally, timing accuracy dissociated from not
strictly temporal cognition and, irrespective of age, showed a
number of regional effects including correlations with caudal,
premotor, and paracentral FA. By contrast, timing reliability sig-
nificantly differed by age, and this difference was weakly statis-
tically explained by a global reduction in cognitive functioning and
brain integrity rather than by regional effects. Together these
results suggest that age largely preserves the workings of a central
timer supported by the striatum but increases noise in timing
 1198 SCHIRMER ET AL.
relevant information represented throughout the brain in sensory,
cognitive, and motor systems.
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Received January 2, 2020
Revision received July 20, 2020
Accepted July 28, 2020 䡲