A Citation-Based Analysis and Review of Significant Papers on Timing and Time Perception

Abstract

Time is an important dimension of brain function, but little is yet known about the underlying cognitive principles and neurobiological mechanisms. The field of timing and time perception has witnessed tremendous growth and multidisciplinary interest in the recent years with the advent of modern neuroimaging and neurophysiological approaches. In this article, I used a data mining approach to analyze the timing literature published by a select group of researchers (n = 202) during the period 2000–2015 and highlight important reviews as well as empirical articles that meet the criterion of a minimum of 100 citations. The qualifying articles (n = 150) are listed in a table along with key details such as number of citations, names of authors, year and journal of publication as well as a short summary of the findings of each study. The results of such a data-driven approach to literature review not only serve as a useful resource to any researcher interested in timing, but also provides a means to evaluate key papers that have significantly influenced the field and summarize recent progress and popular research trends in the field. Additionally, such analyses provides food for thought about future scientific directions and raises important questions about improving organizational structures to boost open science and progress in the field. I discuss exciting avenues for future research that have the potential to significantly advance our understanding of the neurobiology of timing, and propose the establishment of a new society, the Timing Research Forum, to promote open science and collaborative work within the highly diverse and multidisciplinary community of researchers in the field of timing and time perception.

Full text

MINI REVIEW
published: 15 July 2016
doi: 10.3389/fnins.2016.00330
Frontiers in Neuroscience | www.frontiersin.org 1July 2016 | Volume 10 | Article 330
Edited by:
Andrea Ravignani,
Vrije Universiteit Brussel, Belgium
Reviewed by:
Warren H. Meck,
Duke University, USA
Marshall Gilmer Hussain Shuler,
Johns Hopkins University, USA
*Correspondence:
Sundeep Teki
sundeep.teki@gmail.com
Specialty section:
This article was submitted to
Auditory Cognitive Neuroscience,
a section of the journal
Frontiers in Neuroscience
Received: 12 April 2016
Accepted: 30 June 2016
Published: 15 July 2016
Citation:
Teki S (2016) A Citation-Based
Analysis and Review of Significant
Papers on Timing and Time
Perception. Front. Neurosci. 10:330.
doi: 10.3389/fnins.2016.00330
A Citation-Based Analysis and
Review of Significant Papers on
Timing and Time Perception
Sundeep Teki *
Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, UK
Time is an important dimension of brain function, but little is yet known about the
underlying cognitive principles and neurobiological mechanisms. The field of timing
and time perception has witnessed tremendous growth and multidisciplinary interest
in the recent years with the advent of modern neuroimaging and neurophysiological
approaches. In this article, I used a data mining approach to analyze the timing literature
published by a select group of researchers (n=202) during the period 2000–2015
and highlight important reviews as well as empirical articles that meet the criterion of
a minimum of 100 citations. The qualifying articles (n=150) are listed in a table along
with key details such as number of citations, names of authors, year and journal of
publication as well as a short summary of the findings of each study. The results of
such a data-driven approach to literature review not only serve as a useful resource to
any researcher interested in timing, but also provides a means to evaluate key papers
that have significantly influenced the field and summarize recent progress and popular
research trends in the field. Additionally, such analyses provides food for thought about
future scientific directions and raises important questions about improving organizational
structures to boost open science and progress in the field. I discuss exciting avenues
for future research that have the potential to significantly advance our understanding of
the neurobiology of timing, and propose the establishment of a new society, the Timing
Research Forum, to promote open science and collaborative work within the highly
diverse and multidisciplinary community of researchers in the field of timing and time
perception.
Keywords: timing, time perception, rhythm perception, music perception, interval timing, temporal processing,
citations, bibliometrics
INTRODUCTION
Natural sounds have a rich temporal structure, in the form of sequences of sounds that rapidly
change over time and result in dynamic states of perceptual organization. Natural sound sequences
like speech and music form sequences of temporal intervals, often evoking the percept of a rhythm.
How the brain processes time intervals and rhythmic sound sequences is an unresolved and
challenging problem, given the absence of dedicated neural systems for encoding time.
William James was one of the first psychologists to recognize time as a “sensation,” and
heralded a longstanding interest and debate on the nature of time perception and its underlying
representation in the brain (James, 1890). William Gooddy, recognized the importance of motor
structures for timing from a neurological perspective and suggested that they act as “observers”

Teki A Citation-Based Review of Papers on Timing
of time (Gooddy, 1958). Braitenberg (1967) proposed the
cerebellum as an internal timekeeper and hypothesized that
parallel fibers act as delay lines and provide a means to represent
temporal patterns. In the 1970 and 1980s, electrophysiological
studies led by Llinas, Cohen and colleagues revealed the
specialization of the olivocerebellar circuits for temporal
representation (Llinas et al., 1974; Llinás and Yarom, 1981; Welsh
et al., 1995; see Yarom and Cohen, 2002 for a review). At the
same time, fundamental properties of timing behavior like scalar
property provided a theoretical foundation that formal models
of an internal clock must address (Church, 1984; Gibbon et al.,
1984). In the 1980s and 1990s, neuropsychological work in
patients with disorders of the cerebellum and basal ganglia (e.g.,
Ataxia, Parkinson’s) began to provide causal evidence for a role
of these brain regions in perceptual and motor timing (Ivry et al.,
1988; Ivry and Keele, 1989; Artieda et al., 1992; Pastor et al., 1992;
Ivry, 1993; Nichelli et al., 1996).
In the last two decades, however, scientific interest
and progress in understanding the neural codes and
mechanisms underlying temporal processing has advanced
rapidly, aided by technological developments in functional
neuroimaging techniques like magnetic resonance imaging
and magnetoencephalography; brain stimulation techniques
like transcranial magnetic stimulation and transcranial current
stimulation; as well as progress in neural recording methods with
the development of dense multi-electrode arrays, two-photon
calcium imaging, genetic and molecular biology tools including
the use of novel experimental animals models and optogenetic
targeting of specific cell-types for causal investigations amongst
others. Our understanding of the neural mechanisms and circuits
involved in temporal computations has significantly advanced
through the use of these new technologies and continues to shed
light on their underlying brain bases.
However, paralleling the recent advancements in the field is an
exponential growth in research output in terms of more research
articles, conference proceedings, and new journals. Therefore,
unlike in the previous decades, a synthesis of the research
advances in the field poses a significant challenge. Discovery of
knowledge represents an acute problem with a low “signal-to-
noise” threshold, and it is a veritable challenge for a new or
even a current investigator in the field to assimilate new ideas
and apply these concepts for designing innovative experimental
paradigms.
In order to make sense of the progress in the field of timing
and time perception in the last fifteen years, I have adopted
a data-mining approach to identify key review articles and
empirical papers, from a select group of authors that have
significantly impacted research on the cognitive and neural
principles of time perception. The process involved shortlisting
a group of established researchers in the field of timing, and
identifying articles published during the period 2000–2015 that
have received a minimum of 100 citations. Each qualifying article
(n=150) from this group of authors (n=202) is listed in Table 1
along with the number of citations, the rank of each article in
terms of number of citations as well as number of citations
normalized by time since publication, the names of the authors,
the name of the journal, the year of publication, whether the
article was an empirical study or a review, and a short summary
of each article.
KEY PAPERS ON TIMING AND TIME
PERCEPTION
To obtain a representative picture of the field, I examined
research articles by a select group of experts on timing and
time perception. These authors were selected on the basis
of their contribution to the recent special issue on “Interval
timing and skill learning: the multi sensory representation
of Time and Action” published in the Current Opinion
of Behavioral Sciences (Meck and Ivry, 2016; 75 authors)
as well as on the basis of membership of the recently
concluded European COST Action—Timely (http://www.timely-
cost.eu/?q=members_list; 127 authors). These 202 authors
represented research group all over the world (see Supplementary
material B for the complete list of authors), and covered
various aspects of timing research including psychophysics,
neuroimaging, modeling, and electrophysiology in both humans
and experimental animal models.
A number of metrics are commonly used to evaluate
the quality and impact of research articles including impact
factor, h-index, i-10 index amongst others. Although none of
these bibliometrics represent an unbiased estimate of research
impact nor are they accepted as standard across the scientific
community, the number of citations represents a useful metric
as it indicates the impact of a paper and how well the reported
findings are accepted and circulated in the field. It is not an
ideal measure, for the number of citations an article receives is
often skewed by the impact factor of the journal. In order to
draw reasonable conclusions about recent progress in the field,
articles that were published from 2000 to 2015 and indexed in
Google Scholar were considered eligible. Furthermore, to identify
the most impactful papers (ideas), a threshold of a minimum
of 100 citations was applied. As such a metric may be biased
toward older papers than more recent articles, a measure based
on the number of citations normalized by the number of years
since publication was also considered. Although it is possible to
design a more optimal multi-variate measure of research impact
(based on number of citations, impact factor of journal or novel
altmetrics including number of downloads, number of views and
circulation in social media amongst other variables), that is not
the motivation of the paper.
Using the above criteria, 150 papers were identified as
listed in Table 1 (references of these papers in Supplementary
material A; up-to-date as of April 10, 2016). These papers
covered topics related to perception of time, rhythm, music,
inter-sensory synchrony amongst others and used techniques
including psychophysics, neuroimaging, electrophysiology and
modeling. Out of the 150 papers, 52 papers were review articles
(34.7% of all articles; marked with an asterisk next to the number
of citations) that received an average of 271.7 citations (median:
183), i.e., one out of three prominent articles on timing in the
last ten years were review articles that either summarized the
current state of research or presented new hypotheses to drive
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Teki A Citation-Based Review of Papers on Timing
TABLE 1 | List of 150 papers on timing and time perception from 2000 to present sorted according to the number of citations (minimum of 100 citations)
in Google Scholar collated on 10 April, 2016 (see Section Key Papers on Timing and Time Perception for More Details).
Citation and rank Reference Year Journal Summary
1305*[1, 1] Patel 2008 Oxford Uni Press A book that analyses music cognition in relation to language from the
standpoint of cognitive neuroscience.
1192*, [2, 2] Buhusi and Meck 2005 Nat. Rev. Neurosci. Time is represented in a distributed manner through coincidental
activation of cortico-striatal neuronal populations.
1054, [3, 4] Boroditsky 2001 Cogn. Psychol. Native language shapes how we think about time.
1036, [4, 6] Boroditsky 2000 Cognition Time structure is shaped by metaphorical mapping from experiential
domains like space.
719, [5, 13] Rao et al. 2001 Nat. Neurosci. Cortical-subcortical network mediates different components of
temporal processing.
623, [6, 3] Casasanto and Boroditsky 2008 Cognition Spatial information affects judgments about duration but not vice versa.
622*, [7, 14] Lewis and Miall 2003 Curr. Opin. Neurobiol. Timing is measured by automatic (motor) system and cognitive
(prefrontal and parietal) systems.
587*, [8, 12] Mauk and Buonomano 2004 Ann. Rev. Neurosci. Temporal processing depends on state-dependent changes in network
dynamics.
569*, [9, 15] Matell and Meck 2004 Cogn. Brain. Res. Striatal beat frequency model proposes basal ganglia as coincidence
detector of cortical and thalamic input.
551*, [10, 16] Ivry and Spencer 2004 Curr. Opin. Neurobiol. Cerebellum mediates precise timing and basal ganglia mediates
decisions for longer intervals.
512, [11, 11] Wittmann et al. 2006 Chronobiol. Int. Social jetlag, i.e., the discrepancy between social and biological timing
affects wellbeing and stimulant consumption.
469, [12, 10] Grahn et al. 2007 J. Cogn. Neurosci. Basal ganglia and Supplementary Motor Areas mediate beat
perception, in addition to motor production.
450, [13, 23] Coull et al. 2004 Science Attention to time is mediated by a corticostriatal network.
410*, [14, 45] Matell and Meck 2000 Bioessays Coincidence detection of neural activity represents a fundamental
mechanism of timing.
379*, [15, 47] Grondin 2001 Psychol. Bull. Weber’s law provides a framework for psychological models of time.
364*, [16, 25] Ivry et al. 2006 Ann. N. Y. Acad. Sci. Cerebellum provides an explicit representation of time.
364, [17, 50] Coull et al. 2000 Neuropsychologia Temporal orienting depends on sensory events and top-down
expectations.
360*, [18, 8] Grondin 2010 Att. Percept. Psychophys. Review of recent behavioral and neuroscientific studies of timing.
346, [19, 41] Spencer et al. 2003 Science Cerebellar patients can produce continuous rhythmic movements but
not discontinuous movements.
338*, [20, 19] Ivry and Schlerf 2008 Trends Cogn. Sci. Dedicated models of timing are preferred over intrinsic models.
333, [21, 24] Karmarkar and Buonomano 2007 Neuron Cortical networks can read out time as a result of intrinsic network
dynamics.
332*, [22, 5] Coull et al. 2011 Neuropsychopharmacology Review of neuroimaging, neuropsychological and
psychopharmacological aspects of timing.
320, [23, 21] Chen et al. 2008 Cereb. Cortex Passively listening to rhythms recruits motor regions of the brain.
318*, [24, 28] Droit-Volet and Meck 2007 Trends Cogn. Sci. Review of how emotional arousal and valence modulates attentional
time-sharing and clock speed.
318, [25, 29] Shuler and Bear 2006 Science Primary sensory cortex, like V1, mediates reward-timing activity.
315*, [26, 62] Lewkowicz 2000 Psychol. Bull. Temporal relations emerge in a hierarchical and sequential fashion.
306, [27, 17] Patel et al. 2009 Curr. Biol. Snowball, a cuckatoo, can spontaneously synchronize its movements
to a musical beat.
296, [28, 39] Morrone et al. 2005 Nat. Neurosci. Short intervals of time between two successive perisaccadic visual
stimuli (but not auditory) are underestimated.
289, [29, 51] Lewis and Miall 2003 Neuropsychologia Distinct brain areas encode time in the sub- and supra-second range.
287*, [30, 26] Wittmann and Paulus 2008 Trends Cogn. Sci. Review of how impulsivity affects perception of time and decision
making.
283, [31, 77] Penney et al. 2000 J. Exp. Psychol. Hum.
Perc. Perf.
Attention modulates the internal clock at different rates for auditory and
visual signals.
268, [32, 22] Winkler et al. 2009 Proc. Natl. Acad. Sci.
U.S.A.
Newborn infants show beat perception.
267, [33, 9] MacDonald et al. 2011 Neuron Hippocampal time cells encode successive moments during a
sequence of events.
(Continued)
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Teki A Citation-Based Review of Papers on Timing
TABLE 1 | Continued
Citation and rank Reference Year Journal Summary
257*, [34, 18] Wiener et al. 2010 Neuroimage Meta analysis that suggests distinct for perceptual vs. motor timing;
SMA and right IFG are most commonly activated in various timing
tasks.
256*, [35, 71] Meck and Benson 2002 Brain Cogn. Frontostriatal circuits are involved in interval timing and shifting
attention between contexts.
241*, [36, 32] Meck et al. 2008 Curr. Opin. Neurobiol. Review that proposes striatum serves as a core timer, as part of a
distributed timing system.
241*, [37, 40] Nobre et al. 2007 Curr. Opin. Neurobiol. Review that describes how temporal expectations modulate perception
and action, and the underlying neural mechanisms.
241*, [38, 52] Meck 2005 Brain Cogn. Review of timing that suggests a distributed representation of time
across multiple neural systems.
240, [39, 70] Patel et al. 2003 Cognition Rhythms of French and English speech and music are different.
237*, [40, 35] Coull and Nobre 2008 Curr. Opin. Neurobiol. Review that suggests basal ganglia is key for explicit timing while
parietal and premotor areas mediate implicit timing.
235*, [41, 92] Nobre 2001 Neuropsychologia Optimization of behavior by temporal orienting is reflected in latency
and amplitude of ERPs.
234, [42, 99] Buonomano 2000 J. Neurosci. Neural circuits possess intrinsic synaptic mechanisms for timing.
231, [43, 83] Gentner et al. 2002 Lang. Cogn. Proc. Humans use spatial metaphors in temporal reasoning and language.
230, [44, 64] Vroomen et al. 2004 Cogn. Brain Res. Perception of temporal order is shaped by exposure to audio-visual
asynchronies.
222, [45, 89] Janata et al. 2002 Cogn. Aff. Behav. Neurosci. Attentive listening to music is mediated by domain-general areas.
220, [46, 38] Chen et al. 2008 J. Cogn. Neurosci. Musicians show greater prefrontal cortex activity vs. non-musicians
while tapping to complex auditory rhythms.
218, [47, 82] Matell et al. 2003 Behav. Neurosci. Striatal and cortical neurons encode time intervals in their firing rates.
213, [48, 109] Medina et al. 2000 J. Neurosci. Computer simulations show that cerebellum can learn adaptively timed
responses.
212*, [49, 42] Eagleman 2008 Curr. Opin. Neurobiol. Review summarizing illusions of time perception in humans.
208, [50, 65] Patel et al. 2005 Exp. Brain. Res. Beat perception and synchronization show modality specific benefits
for auditory vs. visual beat patterns.
207, [51, 36] Grahn and Rowe 2009 J. Neurosci. Putamen, SMA and premotor cortex are important for internal
generation of the beat and auditory motor coupling during beat
perception.
197, [52, 61] Meck 2006 Brain Res. Dopamine depleting lesions in different parts of the basal ganglia
shows dissociable effects on duration discrimination.
197, [53, 122] Cemgil et al. 2000 J. New Mus. Res. Kalman filter based approach can be used to track tempo.
187*, [54, 67] Lewis and Miall 2006 Trends Cogn. Sci. Dorsolateral prefrontal cortex mediates working memory as well as
timing.
186*, [55, 110] Buonomano and Karmarkar 2002 Neuroscientist Review that argues that time is coded by the population activity of a
large group of neurons.
185, [56, 43] Arvaniti 2009 Phonetica Review of work on rhythmic categorization which argues that timing is
distinct from rhythm.
185, [57, 112] Buhusi and Meck 2002 Behav. Neurosci. Dopamine modulates attentional components of interval timing.
184*, [58, 7] Merchant et al. 2013 Ann. Rev. Neurosci. Review that highlights the role of a core timing mechanism in the basal
ganglia and its interaction with context dependent areas.
183, [59, 56] Noesselt et al. 2007 J. Neurosci. Temporal correspondence between auditory and visual streams
modulates activity of multisensory STS as well as unisensory cortices.
182*, [60, 31] Kotz and Schwartze 2010 Trends Cogn. Sci. Review which suggests that temporal and speech processing is
processed by cortical and subcortical systems associated with motor
control.
182*, [61, 72] Patel 2006 Music Percept. Review that focuses on the evolutionary aspects of musical rhythm.
179*, [62, 34] Vroomen and Kreetels 2010 Att. Percept. Psychophys. Review that focuses on intersensory timing and mechanisms that
encode intersensory lags.
179, [63, 58] Burr et al. 2007 Nat. Neurosci. Short visual events are encoded by visual neural mechanisms with
localized receptive fields rather than by a centralized supramodal clock.
178, [64, 59] Wittmann et al. 2007 Exp. Brain Res. Posterior insula mediates delayed gratification of reward while striatum
encodes time delay.
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Teki A Citation-Based Review of Papers on Timing
TABLE 1 | Continued
Citation and rank Reference Year Journal Summary
178, [65, 74] McAuley et al. 2006 J. Exp. Psychol. General Event timing profiles for a battery of perceptual-motor timing tasks vary
across the life span (4–95 years old).
177, [66, 27] Boroditsky et al. 2011 Cognition English and Mandarin speakers think about time differently.
177*, [67, 46] Wittmann 2009 Phil. Trans. R. Soc. B Review that discusses different models of time perception with a
particular focus on the insula as a core timer.
177, [68, 76] Zelaznik et al. 2006 J. Exp. Psychol. Hum.
Perc. Perf.
Repetitive tapping and drawing movements highlight explicit vs. implicit
timing.
175, [69, 101] Harrington et al. 2004 Brain Motor vs. clock variability in time reproduction and perception tasks
does not support a role for cerebellum in timekeeping.
175, [70, 128] Yarrow et al. 2001 Nature Perceptual fill-in during saccadic suppression underlies the illusion of
chronostasis.
174*, [71, 37] Block et al. 2010 Acta Psychol. Meta analysis that focuses on the effects of cognitive load on
prospective and retrospective duration judgments.
174, [72, 80] Chen et al. 2006 Neuroimage Metrical structure of musical rhythms modulates functional connectivity
between auditory and dorsal premotor cortex.
174, [73, 102] Droit-Volet et al. 2004 Cogn. Emot. The duration of emotional faces is overestimated compared to neutral
ones.
174, [74, 108] Nenadic et al. 2003 Exp. Brain Res. fMRI during a time estimation task shows activation in right putamen.
172*, [75, 123] Ivry and Richardson 2002 Brain Cogn. A multiple timer model accounts for timing and coordination of
repetitive movements.
169*, [76, 20] Allman and Meck 2012 Brain Review that focuses on distortions of time perception and timed
performance in various neurological and psychiatric conditions.
167*, [77, 68] Taatgen et al. 2007 Psychol. Rev. A time perception model based on adaptive control of thought-rational
can explain effects of attention and learning during time estimation.
165, [78, 133] Burle and Casini 2001 J. Exp. Psychol. Hum.
Perc. Perf.
Activation and attention have independent effects on timing
performance.
163, [79, 118] McAuley and Jones 2003 J. Exp. Psychol. Hum.
Perc. Perf.
Timing performance is enhanced when intervals fall on vs. off the beat.
162, [80, 107] Lewis et al. 2004 Neuropsychologia Brain activity during over-learned tapping varies with temporal
complexity of the sequence.
159, [81, 111] Harrington et al. 2004 Cogn. Brain Res. Event-related fMRI reveals brain areas subserving different aspects of
timing.
158, [82, 60] O’Reilly et al. 2008 J. Neurosci. Posterior cerebellum provides a temporal signal to cortical networks for
spatial orienting.
158, [83, 103] Matlock et al. 2005 Cogn. Sci. Fictive motion influences temporal reasoning.
156, [84, 104] Doherty et al. 2005 J. Neurosci. Combined spatial and temporal attention lead to enhanced P1
response.
156, [85, 132] Droit-Volet and Wearden 2002 Q. J. Exp. Psychol. Visual flicker increases the internal clock speed in young children.
155, [86, 125] Rubia et al. 2003 J. Abn. Child Psychol. Motor timing is impaired in children with ADHD and hyperactivity.
154*, [87, 94] Correa et al. 2006 Brain Res. Review that focuses on how temporal attention modulates the
amplitude and latency of ERPs like N2 and P300 components.
154*, [88, 114] Rubia and Smith 2004 Acta Neurobiol. Motor timing and time estimation is mediated by common brain
networks.
153, [89, 30] Nozaradan et al. 2011 J. Neurosci. EEG frequency tagging reveals neural entrainment to beat and meter.
152*, [90, 53] Rubia et al. 2009 Phil. Trans. R. Soc. B Review that suggests that impulsivity in ADHD is related to
compromised timing functions and dopamine dysregulation.
151*, [91, 54] Droit-Volet and Gil 2009 Phil. Trans. R. Soc. B Review that addresses the role of emotional context on timing.
151, [92, 81] Pariyadath and Eagleman 2007 PLoS ONE Repetition suppression underlies duration distortion.
151*, [94, 117] Coull 2004 Cogn. Brain Res. Frontal operculum is key for mediating attentional aspects of time
estimation.
151, [93, 129] Desain and Honing 2003 Perception Musical metro primes the perception of rhythmic categories.
150, [95, 33] Teki et al. 2011 J. Neurosci. Perception of relative and absolute time is mediated by distinct
networks based in the basal ganglia and the cerebellum, respectively.
148, [96, 84] Noulhiane et al. 2007 Emotion Emotional stimuli are judged longer than neutral stimuli, when balanced
for the levels of arousal.
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Teki A Citation-Based Review of Papers on Timing
TABLE 1 | Continued
Citation and rank Reference Year Journal Summary
147, [97, 98] Kanai et al. 2006 J. Vis. Temporal frequency of a stimulus serves as the clock for perceived
duration.
145, [98, 55] Kotz et al. 2009 Cortex Review that focuses on the non-motor functions of basal ganglia with
particular emphasis on prediction in speech and language.
143, [99, 87] Styns et al. 2007 Hum. Mov. Sci. Walking speed is modulated by the tempo of musical and metronome
stimuli.
140, [100, 49] Fuhrman and Boroditsky 2010 Cogn. Sci. Temporal judgments in nonlinguistic tasks are influenced by culturally
specific spatial representations.
140*, [101, 115] Eagleman et al. 2005 J. Neurosci. Review of timing based on psychophysics, electrophysiology, imaging
and computational modeling.
139, [102, 105] Lewis and Miall 2006 Behav. Proc. Dorsolateral prefrontal cortex mediates working memory and posterior
parietal cortex and anterior cingulate attentional aspects of timing.
137, [103, 106] Rammsayer and Altenmuller 2006 Music Percept. Musicians perform better than non-musicians in temporal
discrimination but not temporal generalization tasks.
136, [104, 63] Grahn and Brett 2009 Cortex Parkinson’s patients show selective deficits in discrimination of
beat-based rhythms.
134, [105, 97] Keller et al. 2007 Consc. Cogn. Action simulation in ensemble musicians like pianists underlies
synchronization and self-recognition.
132*, [106, 66] Eagleman and Pariyadath 2009 Phil. Trans. R. Soc. B Energy expended in coding a stimulus represents its duration.
132, [107, 124] Navarra et al. 2005 Cogn. Brain Res. Temporal window for audiovisual integration is extended for
asynchronous speech and music.
131*, [108, 126] Lustig et al. 2005 Memory Striatum may detect oscillatory cortical firing in a coincident manner to
time brief intervals.
131*, [109, 145] Mauk et al. 2000 Curr. Biol. Cerebellum is key for movement through feedforward use of sensory
information via temporally specific learning.
130, [110, 113] Patel et al. 2006 J. Acoust. Soc. Am. Music reflects durational patterns in speech as well as patterns of
variability in pitch.
130, [111, 135] Hinton and Meck 2004 Cogn. Brain Res. fMRI activations show involvement of fronto-striatal circuits in interval
timing.
127, [112, 88] Ishihara et al. 2008 Cortex A mental time line exists from left to right along the horizontal axis in
space.
127, [113, 116] Matell et al. 2006 Psychopharm Methamphetamine produces a dose-dependent overestimation of time.
126, [114, 90] van Eijk et al. 2008 Att. Percept. Psychophys. Synchrony and temporal order judgment tasks produce different PSS
estimates.
126, [115, 91] Wassenhove et al. 2008 PLoS ONE Multisensory interactions influence perception of time: vision can
impact auditory temporal perception.
126, [116, 131] Correa et al. 2005 Psychon. Bull. Rev. Temporal orienting enhances perceptual processing.
125*, [117, 119] Ivry 2006 Ann. N. Y. Acad. Sci. Review that analyzes the role of the cerebellum as an internal clock.
124, [118, 75] Iversen et al. 2009 Ann. N. Y. Acad. Sci. Beta-band activity influences auditory rhythm perception.
124, [119, 93] Wearden et al. 2008 J. Exp. Psychol. Hum.
Perc. Perf.
Decreasing arousal affects performance on time perception tasks.
123*, [120, 95] Wearden and Lejeune 2008 Q. J. Exp. Psychol. A review of the conformity and violations of the scalar property in
human timing tasks.
123, [121, 138] Smith et al. 2003 Neuroimage Right dorsolateral prefrontal cortex is involved in time perception, and
may serve as an accumulator.
122, [122, 78] Grahn and McAuley 2009 Neuroimage Individual differences in beat perception exist and modulate activity in
auditory and motor areas.
122, [123, 79] Zarco et al. 2009 J. Neurophys. Performance of rhesus monkeys and humans is compared on a
number of sub-second interval reproduction tasks.
121, [124, 136] Matell et al. 2004 Behav. Neurosci. Intermittent but not continuous administration of cocaine increases the
speed of internal clock.
121*, [125, 139] Wearden 2003 Time and Mind II Book chapter that reviews timing in the light of scalar expectancy
theory.
120, [126, 57] Boroditsky and Gaby 2010 Psychol. Sci. Pormpuraaw, an Australian Aboriginal community represent time
according to cardinal directions.
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TABLE 1 | Continued
Citation and rank Reference Year Journal Summary
119, [127, 48] Simen et al. 2011 J. Neurosci. A temporal integration model yields a firing-rate based representation
of time.
118, [128, 137] Correa et al. 2004 Percept. Psychophys. Temporal orienting effects are larger when temporal expectancy is
varied between and not within blocks.
118, [129, 144] Griffin et al. 2002 Neuropsychologia Spatial and temporal orienting optimize behavior through distinct
attentional processes.
118, [130, 146] Droit-Volet and Wearden 2001 J. Exp. Child Psychol. 8 year old children show higher temporal sensitivity than 3 and 5 year
old children.
117*, [131, 100] Keller 2008 Emerg. Comm. Review that addresses cognitive processes underlying joint action in
music performance.
117, [132, 127] Vatakis and Spence 2006 Brain Res. Cross-modal temporal discrimination performance is better for
audiovisual stimuli of lower complexity.
115, [133, 130] Effron et al. 2006 Emotion Embodiment plays a role in the emotional modulation of time.
114, [134, 140] Muller-Gethmann et al. 2003 Psychophysiol Temporal preparation enhances the processing speed of early evoked
potentials.
114, [135, 148] Lustig and Meck 2001 Psychol. Sci. Age-related changes in attentional resources affects interval timing.
113*, [136, 85] Buhusi and Meck 2009 Phil. Trans. R. Soc. B Attentional and memory resources for timing are shared between timed
and intruder events.
112*, [137, 86] Balsam and Gallistel 2009 Trends Neurosci. Review which suggests that associative learning depends on temporal
contiguity.
112, [138, 120] Droit-Volet et al. 2007 Behav. Proc. 5- and 8-year old children underestimate the duration of visual vs.
auditory signals.
112, [139, 121] Stetson et al. 2007 PLoS ONE Slowing of time during threatening events is a function of episodic
recollection, not perception.
111, [140, 69] Casasanto et al. 2010 Cogn. Sci. Spatial information influences temporal judgments more than time
affects spatial judgments in children as well as adults.
110, [141, 143] Lange et al. 2003 Psychophysiol Stimuli presented at attended vs. unattended moments in time yield an
enhanced N1 response.
109, [142, 134] Jahanshahi et al. 2006 J. Neurosci. Basal ganglia and cerebellum are involved in reproduction of both short
and long intervals.
108*, [143, 147] Wing 2002 Brain Cogn. Review that presents an information processing perspective on human
voluntary timing.
107, [144, 73] Jahanshahi et al. 2010 Brain Dopamine increases connectivity between caudate nucleus and
prefrontal cortex during motor timing.
106, [145, 96] Cummins 2009 J. Phonetics Rhythm affords synchronization among two speakers.
104, [146, 44] Arvaniti 2012 J. Phonetics Rhythm metrics for classification and cross-linguistic comparisons
should be used with caution.
104, [147, 141] Repp and Keller 2004 Q. J. Exp. Psychol. Period correction depends on intention, attention and awareness of
tempo changes whilst phase correction depends on intention.
104, [148, 149] Volz et al. 2001 Neuroreport Schizophrenic patients show hypo-activation in putamen and prefrontal
cortex during time estimation.
103*, [149, 142] MacDonald and Meck 2004 Neurosci. Biobehav. Rev. A review that assesses the close correspondence between reaction
time and interval timing.
101*, [150, 150] Meck 2001 CRC Press A book that reviews functional and neural mechanisms of interval
timing in humans and animals.
Asterisks next to the number of citations denote review articles as opposed to empirical papers. The number of citations, name(s) of authors, year and journal of publication as well as
a brief summary is presented for each qualifying article. The authors’ names are hyperlinked to the corresponding article’s web page on Google Scholar. The numbers in the square
brackets next to the number of citations denote the rank of each article in terms of overall number of citations and the rank according to the number of citations normalized by years
since publication, respectively. References of all articles in this table are provided in supplementary information.
the field forward. The remaining empirical papers, 98 in all
(65.3% of all articles), received an average of 208 citations per
paper (median: 157). Normalizing the number of citations by
the number of years since publication to remove the bias due to
the “age” of each article revealed a similar trend—review articles
receive more citations (mean: 30.0; median: 21.8) than empirical
papers (mean: 20.7; median: 16.5). A brief one-sentence summary
of each study is also presented in the last column of Table 1, to
provide the reader an informed basis to select relevant papers for
more in-depth review.
There are several conclusions to be drawn from Table 1,
for instance—review articles tend to dominate the field in
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Teki A Citation-Based Review of Papers on Timing
terms of number of citations while only an average of six
significant empirical papers are published every year (also see
Supplementary material C, D, and E). Although many of these
reviews are now “classic” in the field, even the most recent article
in the table is a review (Merchant et al., 2013a; 184 citations).
Among other things, this suggests that either the field is still in an
embryonic stage where review articles by established researchers
are needed to set the precedent on certain topics, or that the field
of timing is too diverse, and represents the intersection of various
sub-fields including time perception, rhythm perception, music
perception, temporal coding, inter sensory asynchrony, motor
timing and coordination, that is reflected in the diversity of topics
covered by the review articles.
It is not clear whether a similar analysis of the most recent
and highly cited papers in other prominent fields like memory,
vision, or decision-making will yield similar trends, e.g., ratio of
reviews to empirical studies but one could make a null hypothesis
that such a ratio may be smaller than for the highly diverse
and multidisciplinary field of timing. Alternatively, compared to
research topics like vision and memory that have been intensely
studied for several decades, the field of timing is still in a nascent
stage and does not boast of a large research community as
evidenced by the number of specialist journals on timing, or
number of exclusive workshops and meetings dedicated to timing
research.
FUTURE DIRECTIONS—SCIENTIFIC
Apart from organizational considerations, there are several new
scientific directions that the field can and should embrace
to achieve a more comprehensive understanding of the
neurobiology of natural timing behavior. Animal models of
timing focused on core timing networks including the basal
ganglia, cerebellum, premotor and parietal cortex (Grahn, 2012;
Schneider and Ghose, 2012; Teki et al., 2012; Merchant et al.,
2013a; Allman et al., 2014; Hayashi et al., 2015) will be key to
understanding the encoding of time by neuronal ensembles. Such
a line of work has been recently pioneered by Merchant and
colleagues in rhesus macaques that combines timing behaviors
and the examination of the underlying neuronal code in the
basal ganglia (Merchant et al., 2011, 2013b; Bartolo et al., 2014;
Bartolo and Merchant, 2015). Recent work by Mello et al. (2015)
and Gouvêa et al. (2015) further demonstrated that a population
code for time exists in the striatum that scales with the interval
being timed and multiplexes information about action as well as
time. Optogenetic approaches in specific identified cells in animal
models will yield crucial insights into the causal role of such
mechanisms and their impact on timing behavior (Grosenick
et al., 2015). For instance, a recent study by Chen et al. (2014)
reported rapid modulation of striatal activity by the cerebellum
via a disynaptic pathway that has implications for the coordinated
processing of temporal information in these two core timing
areas.
The other dominant view of timing is that time is not
based on the computations in dedicated circuits but rather
represents the output of intrinsic neuronal dynamics (Karmarkar
and Buonomano, 2007). In this respect, the activity of sensory
areas including auditory, visual, and somatosensory cortices
merits further attention. Combining optogenetics and single-
unit recordings in primary visual cortex (V1), Hussain Shuler
and colleagues have recently provided novel insights into how
basal forebrain cholinergic input to V1 provides a teaching
signal to modulate the response dynamics of V1 so that cues
predictive of given delays to future reward produce responses
that express those learned delays (Chubykin et al., 2013; Liu
et al., 2015), that those responses reflect learned reward timing
(Shuler and Bear, 2006; Zold and Hussain Shuler, 2015) and
inform visually-cued timing (Namboodiri et al., 2015). Similar
work in other sensory domains such as audition will enable
us to decipher the multi-sensory representation of time and
action during adaptive behaviors such as speech and movement.
Further neurophysiological work using high channel-count
electrophysiology (n∼400–1000) based on new Silicon probes
based on CMOS technology (e.g., Berényi et al., 2014; Lopez et al.,
2016) or mesoscopic analysis of timing behavior across different
cortical layers and multiple brain areas using multi-plane calcium
imaging may further shed new light on the underlying circuit-
level cortical computations (Yang et al., 2016).
Apart from adopting the latest technological tools and genetic
probes, a fundamental understanding of timing can be obtained
by designing more naturalistic tasks that use ecological stimuli
that are meaningful to the experimental subject in the real
world. Naturalistic sequences with variable temporal structure
(Teki et al., 2011; Teki and Griffiths, 2014, 2016) that go
beyond the traditional use of single intervals may yield novel
insights into the encoding of time as well as associated motor
behaviors (Kornysheva and Diedrichsen, 2014). Table 1 and the
reviews therein highlight that timing is not mediated by a single
brain area but rather involves a distributed network (Meck,
2005) in cortical and subcortical areas including prefrontal,
parietal, premotor and sensory cortices, insula, basal ganglia,
cerebellum, inferior olive amongst others. To formulate a unified
theory of how timing is mediated by these structures, it is
also important to understand the core functions of these areas
and what particular aspect of timing they mediate, whether
it is related to perception, attention, or memory. The use of
comparative paradigms in healthy human volunteers as well as
clinical populations that show timing deficits such as patients
with Parkinson’s, Huntington’s, Schizophrenia amongst others
will provide a more uniform understanding of timing functions
and dysfunctions in health and disease (Allman and Meck, 2012).
An identical approach (and even the use of similar paradigms)
in animal models via use of control animals as well as lesion
or knock-out models will complement findings from the human
literature and provide a more generic understanding of the neural
computations and circuits that underlie timing.
FUTURE DIRECTIONS—ORGANIZATIONAL
In order to drive more impactful experimental work, the field of
timing needs to attract young researchers which would require
more concerted efforts from the entire timing community.
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Teki A Citation-Based Review of Papers on Timing
A recent positive step in this direction was marked by the
launch of a specialist journal for timing, Timing and Time
Perception (Meck et al., 2013) as well as its corresponding
review journal, Timing and Time Perception Reviews. Another
step forward would be the launch of an academic society
exclusively for researchers in timing that would promote
interdisciplinary exchange of ideas amongst researchers
with diverse interests in timing via annual conferences that
draw on a range of methods from purely behavioral to
neurophysiological and neuroanatomical measures; share
pertinent news and information like grant funding calls,
new papers, job opportunities for doctoral and postdoctoral
candidates, workshops and training opportunities; and promote
the career development of young researchers through grants for
short cross-disciplinary collaborations or exchange visits and
funding for attending conferences and mentoring support.
Although there already exist a few scientific societies and
communities relevant to timing like the Society for Music
Perception and Cognition (SPMC: http://www.musicperception.
org), Rhythm Perception and Production Workshop (RPPW:
http://rppw.org), European Society for Cognitive Sciences of
Music (ESCOM: http://escom2015.org), Society for Education,
Music and Psychology Research (SEMPRE: http://www.sempre.
org.uk), Deutsche Gesellschaft fur Musikpsychologie (DGM:
http://www.music-psychology.de), Asia-Pacific Society for
the Cognitive Sciences of Music, Fondazione Mariani (http://
fondazione-mariani.org/) that organizes the NeuroMusic
conferences, their scope is limited to music perception and
psychology, and do not cover all aspects of timing and time
perception. Society for Neuroscience (SfN) represents the
primary venue where timing researchers gather for structured
symposia on human and animal timing research but the
scientific discussions are limited given the busy nature of SfN
meetings. A recent example of such a successful academic
organization for a diverse topic of research is the Society for
the Neurobiology of Language (http://www.neurolang.org/)
funded by the National Institutes of Health, which since its
inception in 2009, attracts more than 400 researchers for its
annual conferences. To address the absence of an association of
researchers working on all aspects of timing, Argiro Vatakis and
I have established a new timing society to promote open science
and collaboration—the “Timing Research Forum” (http://
timingforum.org).
Irrespective of the present state of affairs, the field of timing
and time perception represents a promising and exciting field
of research that is growing every year in terms of number of
researchers and scientific output, and one where new students
and researchers may find a relatively unexplored topic of research
and make a significant impact on the field.
AUTHOR CONTRIBUTIONS
The author confirms being the sole contributor of this work and
approved it for publication.
FUNDING
ST is funded by the Wellcome Trust (WT106084/Z/14/Z; Sir
Henry Wellcome Postdoctoral Fellowship).
ACKNOWLEDGMENTS
I thank Anu Chowdhry for help with compiling the list of papers
in Table 1.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: http://journal.frontiersin.org/article/10.3389/fnins.
2016.00330
DATA
Metrics data presented in Table 1 are available to download as
a .mat file from Figshare:
Link : https://figshare.com/s/0fb93a59927786300644;
DOI : https://dx.doi.org/10.6084/m9.figshare.3153124.
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Conflict of Interest Statement: The author declares that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Copyright © 2016 Teki. This is an open-access article distributed under the terms
of the Creative Commons Attribution License (CC BY). The use, distribution or
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are credited and that the original publication in this journal is cited, in accordance
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