ArticlePDF Available

Observations on recent progress in the field of timing and time perception

Abstract

Time is an important dimension of brain function, but little is still known about the underlying cognitive principles and neurobiological mechanisms. The field of timing and time perception has witnessed rapid growth and multidisciplinary interest in the recent years with the advent of modern neuroimaging, neurophysiological and optogenetic tools. In this article, I review the literature from the last ten years (2005-2015) using a data mining approach and highlight the most significant empirical as well as review articles based on the number of citations (a minimum of 100 citations). Such analysis provides a unique perspective on the current state-of-the-art in the field and highlights subtopics in the field that have received considerable attention, and those that have not. The objective of the article is to present an objective summary of the current progress in the field of timing and time perception and provide a valuable and accessible resource summarizing the most cited articles for new as well current investigators in the field.
Observations on recent progress in the field of timing and time perception !
1
!
!
Sundeep Teki!
!
Auditory Neuroscience Group, Department of Physiology, Anatomy & Genetics,
University of Oxford, South Parks Road, Oxford OX1 3QX, UK.
sundeep.teki@dpag.ox.ac.uk
!
Abstract
Time is an important dimension of brain function, but little is still known about the
underlying cognitive principles and neurobiological mechanisms. The field of timing and
time perception has witnessed rapid growth and multidisciplinary interest in the recent years
with the advent of modern neuroimaging, neurophysiological and optogenetic tools. In this
article, I review the literature from the last ten years (2005-2015) using a data mining
approach and highlight the most significant empirical as well as review articles based on the
number of citations (a minimum of 100 citations). Such analysis provides a unique
perspective on the current state-of-the-art in the field and highlights subtopics in the field
that have received considerable attention, and those that have not. The objective of the article
is to present an objective summary of the current progress in the field of timing and time
perception and provide a valuable and accessible resource summarizing the most cited
articles for new as well current investigators in the field.
!
Page of 123
This article was originally written for an invited review on Auditory perception and Timing for a special issue of
1
Current Opinion in Behavioural Sciences on ‘Interval Timing and Skill Learning: The Multisensory Representation of
Time and Action’ guest edited by Warren Meck and Richard Ivry. The article was rejected as it did not conform to the
specific journal guidelines and is reproduced here in its original form.
I. Introduction!
!
This is not an editorial piece. For that, please read the editorial article for this special issue on
Interval Timing and Skill Learning: The Multisensory Representation of Time and Action’, by
Richard Ivry and Warren Meck, who are in the best position to comment on the various review
articles and provide a succinct summary of the field. My objective is to present my personal
observations on the current state of research on timing and time perception, specifically from
the point of view of a postdoctoral researcher interested in building an independent research
program focused on timing.!
!
My advisor, Tim Griffiths and I were invited by the editor, Warren Meck to contribute a review
focused on ‘Auditory perception and timing’. As per the guidelines circulated to all invited
authors, the review should focus on, and highlight recent articles of note, especially those
published in the last couple of years. My own contribution to the field, during my doctoral
research with Tim Griffiths, is represented by two empirical papers (Teki et al., 2011, Teki and
Griffiths, 2014) and a review article (Teki et al., 2012) in a special issue on timing, that was also
edited by Warren Meck. More recently, Tim and I collaborated with Warren Meck and Melissa
Allman on a review elaborating the subjective principles of time perception (Allman et al., 2014). !
!
The guide for authors provided by the Current Opinion in Behavioral Sciences (COBS) clearly
stipulates that - the aim of the manuscript is to review recent articles, with particular emphasis
on those articles published in the past two years. As the guide encourages the authors to
describe recent trends and provide subjective opinions of the topics discussed, I decided to take
the liberty to do exactly as instructed, and provide my subjective opinions of recent progress in
the field.!
Page of 223
A review article is meant to highlight and discuss recent trends and results on a particular topic.
Invariably, there is a tendency on the part of most authors to emphasize one’s own work at the
expense of not adequately discussing results from other research groups. At the outset, I also
outlined a possible structure for the review based on my work on duration-based and beat-
based timing (Teki et al., 2011, 2012). However, this work does not comply with the publication
timeline suggested by the journal. Thus, I decided to not discuss this work which was discussed
in a recent review article (Allman et al., 2014). Even if the restricted timeline of two years were
to be relaxed, Tim and I struggled to find ten recent articles of note on the particular topic and
published in the last two years to emphasize and highlight in our review. After further
discussions, we decided to focus on ‘Disorders of sequence and interval timing’ based on
recent neuropsychological work from Tim’s group that examined perceptual timing abilities of
patients with striatal and cerebellar degeneration in the form of Huntington’s disease, Multiple
Systems Atrophy and Parkinson’s disease (Cope et al., 2014a, b). !
!
This new topic was more exciting, for the list of authors and topics provided by COBS did not
include any clinically oriented articles. Although timing abilities are known to be impaired in a
range of neuropsychological and neurological disorders (Allman and Meck, 2012) including
Parkinson’s disease, Huntington’s disease, Multiple Systems Atrophy and Schizophrenia
amongst others, the extent to which their timing performance is affected and related to the
primary neurological deficits is not fully known. However, even though this field is gaining
traction and represents a highly fruitful area of translational research, a review of the recent
literature on this topic, again, yielded few promising articles to form the basis of a constructive
review that would be beneficial to the field.!
!
Page of 323
At this juncture, it appeared that the two topics of specialization investigated in Tim’s lab could
not be covered in a detailed and topical review for COBS. At this point, I wondered whether the
lack of recent significant breakthroughs is true of the field of timing and time perception as a
whole, or is it just a representation of the specific topics we focused on? !
!
!
II. Key papers on timing and time perception!
!
!
To obtain a representative picture of the field, I decided to examine recent papers by the authors
invited to contribute to this special issue (75 authors). As the list of invited authors was a fairly
small sample, I extended the list by considering all members of the recently concluded
European COST Action - Timely which included members from all over the world. This list
provided another 129 authors who were not already invited to contribute to the COBS special
issue, thus resulting in a reasonable sample size of 204 authors.!
!
A number of metrics are used to evaluate the quality and impact of research articles including
impact factor, h-index, i-10 index amongst others. Although none of these metrics are accepted
as standard across the scientific community, I decided on the number of citations as a metric as
it indicates the impact of a paper and how well the idea is accepted and circulated in the field by
other researchers. It is not a perfect measure, for the number of citations an articles receives is
often skewed by the impact factor of the journal where it is published but good ideas tend to
circulate well no matter where the ideas are published. Furthermore, to draw reasonable
conclusions about progress in the timing field, I focused on a period of 10 years and considered
all articles that were indexed in Google Scholar and published by the above set of authors from
2005 onward. In order to restrict my sample of publications and consider only the most impactful
papers (ideas), I used a threshold of a minimum of 100 citations. This timeframe is also not
Page of 423
ideal, for it is biased towards older papers than more recent articles which have not had the
same time to accumulate as many citations. !
!
Using these search criteria, 66 papers (an average of 1 article per every 3 authors) were found
as described in Table 1. These papers covered research on topics related to perception of time,
rhythm, music, inter-sensory synchrony amongst others and used techniques including
psychophysics, neuroimaging, electrophysiology and modeling. Out of these 66 papers, 24
papers were review articles (marked with an asterisk next to the number of citations) that
received an average of 223.5 citations (Z-score ranged from - 0.65 to 4.44), i.e. one of out three
prominent articles on timing in the last ten years were review articles that discussed the current
state of research. The remaining empirical papers, 42 in all, received an average of 181.6
citations per paper (Z-score ranged from - 0.82 to 3.70). !
!
There are several conclusions to be drawn from Table 1, for instance that review articles tend to
dominate the overall citations in the field while only an average of four significant empirical
papers are published a year. 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., 2013). 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, at an intersection of various 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. Although not evident from the
list, there has been a recent proliferation of review articles given the rise of specialist open
access journals like Frontiers that encourage researchers (repeatedly and frequently) to
commission special issues covering empirical work as well as reviews. It is not known whether a
similar analysis of the most recent and highly cited papers in other fields like memory, vision, or
Page of 523
decision-making will yield the same ratio of reviews to empirical studies but one could make a
reasonable null hypothesis that this ratio may be smaller than for the field of timing.
Alternatively, compared to fields like vision and memory that have been intense topics of
investigation for several decades the field of timing is more nascent and does not boast a large
research community as evident by the number of participants at specialist meetings in such
fields, for instance, the annual Vision Science Society conferences. !
!
In order to drive more experimental work, it is clear that the field of timing needs to attract more
young researchers and ensure a a bright future for the field, and this would need concerted
efforts from the entire timing community. A recent positive step in this direction is represented by
the launch of a specialist journal for timing, Timing and Time Perception 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, and from neurostimulation and
neuropsychological approaches to animal work and computational models; share pertinent
news and information like grant funding calls, new papers, job opportunities for doctoral and
postdoctoral candidates, workshops and training opportunities; and promote career
development of young researchers through grants for short cross-disciplinary collaborations or
exchange visits, funding for attending conferences and general 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
Page of 623
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 the interests of the entire field of timing and time perception. Society for Neuroscience
(SfN) represents the primary venue where researchers gather together for structured mini- or
nano-symposia on human and animal timing research but the scientific interaction and
discussions are limited given the hectic nature of SfN meetings. A recent example of such a
successful academic organization 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 that are held alternatively
in the USA (as a satellite meeting of SfN) and Europe.!
!
!
III. Future directions!
!
Organizational considerations apart, there are several new scientific directions that the field can
and should embrace to achieve a more comprehensive understanding of the neurobiology of
timing in natural environments. Animal models of timing focused on core timing networks
including the basal ganglia, cerebellum, premotor and parietal cortex (Grahn 2012; Teki et al.,
2012; Schneider and Ghose, 2012; Merchant et al., 2013; 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 Hugo Merchant colleagues in rhesus macaques that
combines timing behaviors and the examination of the underlying neuronal code in the basal
ganglia (Merchant et al., 2011, 2013; Bartolo et al., 2014; Bartolo and Merchant, 2015). Recent
work by Mello 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
Page of 723
well as time. Optogenetic approaches in specific target cells in animal models will yield further
crucial insights into the causal role of such mechanisms and their impact on timing behaviors
(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 which has implications
for the coordinated processing of temporal information in the two core timing areas.!
!
The other dominant view of timing is that it is not a computation of specific dedicated circuits but
rather the output of intrinsic neuronal dynamics (Karmarkar and Buonomano, 2007; Ivry and
Schlerf, 2008). 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
beautiful insights into how V1 responses predict and drive the timing of future actions
(Namboodiri et al., 2015) and recruit basal forebrain and cholinergic input within V1 to encode
the timing of visually cued behaviors (Liu et al., 2015). !
!
In order to obtain a fundamental understanding of timing, it is also imperative to use stimuli and
paradigms that mimic timing behaviors in the natural world. Such naturalistic sequences that go
beyond the use of single intervals that have been traditionally used will offer additional insights
on 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 form a clear picture 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 attention, memory or perception.
Page of 823
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. 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 fundamental
mechanisms of timing.!
!
Irrespective of the present state of affairs, the field of timing and time perception represents a
promising and highly active field of research that is growing every year in terms of number of
researchers and scientific output and one where new students and researchers can find a niche
topic and leave a significant mark on the field. !
!
!
!
!
!
!
!
!
!
!
!
!
!
!
!
!
!
!
!
!
!
!
!
!
!
!
Page of 923
Table List of 66 papers on timing, rhythm and music perception from 2005 to present sorted
according to the number of citations (minimum of 100 citations) in Google Scholar collated
during the period from August 30 to September 16, 2015 (see section II for more details).
Asterisks next to the number of citations denote review articles.!
!
No. of
citations
Reference
Year
Journal
1068*
Buhusi & Meck
2005
Nat Rev Neurosci
550
Casasanto & Boroditsky
2008
Cognition!
442
Wittmann et al.
2006
Chronobiol Int
417
Grahn et al.
2007
J Cogn Neurosci
310*
Grondin
2010
Att Percept
Psychophys
305
Karmarkar & Buonomano
2007
Neuron
294*
Ivry & Schlerf
2008
Trends Cogn Sci
292
Shuler & Bear
2006
Science
289*
Coull et al
2011
Neuropsychophar
macology
276
Morrone et al.
2005
Nat Neurosci
Page of 10 23
274
Chen et al.
2008
Cereb Cortex
265*
Droit-Volet & Meck
2007
Trends Cogn Sci
261
Patel et al.
2009
Curr Biol
253*
Wittman & Paulus
2008
Trends Cogn Sci
237
Winkler et al.
2009
Proc Natl Acad Sci
228
MacDonald et al.
2011
Neuron
222*
Meck
2005
Brain & Cognition!
220*
Meck et al.
2008
Curr Opin
Neurobiol
219*
Wiener et al.
2010
NeuroImage!
212*
Coull & Nobre
2008
Curr Opin
Neurobiol
210*
Nobre et al.
2007
Curr Opin
Neurobiol
193
Patel et al.
2005
Brain Res
No. of
citations
Reference
Year
Journal
Page of 11 23
192
Chen et al.
2008
J Cogn Neurosci
177
Grahn & Rowe
2009
J Neurosci
177*
Lewis & Miall
2006
Trends Cogn Sci
175
Meck
2006
Brain Res
173
Noesselt et al.
2007
J Neurosci
170
Arvaniti
2009
Phonetica
168
Wittmann et al.
2007
Exp Brain Res
165*
Kotz & Schwartze
2010
Trends Cogn Sci
162
Burr et al.
2007
Nat Neurosci
159*
Vroomen & Kreetels
2010
Att Percept
Psychophys
155*
Wittmann
2009
Phil Trans R Soc B
No. of
citations
Reference
Year
Journal
Page of 12 23
153
McAuley et al.
2006
J Exp Psychol:
General
152
Chen et al.
2006
NeuroImage!
151
Boroditsky et al.
2011
Cognition!
150*
Ta at g en et al .
2007
Psychol Rev
150*
Correa et al.
2006
Brain Res
144
Matlock et al.
2005
Cogn Sci
136*
Allman & Meck
2012
Brain!
135*
Block et al.
2010
Acta Psychol
135
Kotz et al.
2009
Cortex
134
Teki et al.
2011
J Neurosci
134
Lewis & Miall
2006
Behav Proc
No. of
citations
Reference
Year
Journal
Page of 13 23
130*
Rubia et al.
2009
Phil Trans R Soc B
130
Styns et al.
2007
Hum Mov Sci
128
Kanai et al.
2006
J Vis
125
Noulhiane et al.
2007
Emotion
124
Fuhrman & Boroditsky
2010
Cogn Sci
122
Grahn & Brett
2009
Cortex
122*
Eagleman et al.
2005
J Neurosci
120
Keller et al.
2007
Consc & Cogn
120
Correa et al.
2005
Psychon Bull &
Rev
118 *
Merchant et al.
2013
Ann Rev Neurosci
113
Grahn & McAuley
2009
NeuroImage!
110
Zarco et al.
2009
J Neurophys
No. of
citations
Reference
Year
Journal
Page of 14 23
!
!
!
!
!
!
!
!
!
!
!
!
109
Wearden et al.
2008
Q J Exp Psychol
108
Vatakis & Spence
2006
Brain Res
107
Nozaradan et al.
2011
J Neurosci
107
Wassenhove et al.
2008
PLoS One
107
Ishihara et al.
2008
Cortex
105*
Keller
2008
Emerg Comm
102
Casasanto et al.
2010
Cogn Sci
101
Iversen et al.
2009
Ann NY Acad Sci
100*
Droit-Volet & Gil
2009
Phil Trans R Soc B
100
Jahanshahi et al.
2006
J Neurosci
No. of
citations
Reference
Year
Journal
Page of 15 23
References!
!
1.!Allman MJ, Meck WH: Pathophysiological distortions in time perception and
timed performance. Brain 2012, 135:656–677.!
2.!Arvaniti A: Rhythm, timing and the timing of rhythm. Phonetica 2009, 66:46–63.!
3.!Bartolo R, Merchant H: β oscillations are linked to the initiation of sensory-cued
movement sequences and the internal guidance of regular tapping in the
monkey. J. Neurosci. 2015, 35:4635–4640.!
4.!Bartolo R, Prado L, Merchant H: Information processing in the primate basal
ganglia during sensory-guided and internally driven rhythmic tapping. J.
Neurosci. 2014, 34:3910–3923.!
5.!Block RA, Hancock PA, Zakay D: How cognitive load affects duration judgments:
A meta-analytic review. Acta Psychol. 2010, 134: 330-343.!
6.!Boroditsky L, Fuhrman O, McCormick K: Do English and Mandarin speakers
think about time differently? Cognition 2011, 118:123–129.!
7.!Buhusi CV, Meck WH: What makes us tick? Functional and neural mechanisms
of interval timing. Nat. Rev. Neurosci. 2005, 6:755–765.!
8.!Burr D, Tozzi A, Morrone MC: Neural mechanisms for timing visual events are
spatially selective in real-world coordinates. Nat. Neurosci. 2007, 10:423–425.!
9.!Casasanto D, Boroditsky L: Time in the mind: Using space to think about time.
Cognition 2008, 106:579–593.!
10.!Casasanto D, Fotakopoulou O, Boroditsky L: Space and Time in the Child’s
Mind: Evidence for a Cross-Dimensional Asymmetry. Cognitive Science 2010,
34:387–405.!
Page of 16 23
11.!Chen CH, Fremont R, Arteaga-Bracho EE, Khodakhah K: Short latency
cerebellar modulation of the basal ganglia. Nat. Neurosci. 2014, 17:1767–1775.!
12.!Chen JL, Penhune VB, Zatorre RJ: Listening to musical rhythms recruits motor
regions of the brain. Cereb. Cortex 2008, 18:2844–2854.!
13.!Chen JL, Penhune VB, Zatorre RJ: Moving on time: brain network for auditory-
motor synchronization is modulated by rhythm complexity and musical training. J
Cogn Neurosci 2008, 20:226–239.!
14.!Chen JL, Zatorre RJ, Penhune VB: Interactions between auditory and dorsal
premotor cortex during synchronization to musical rhythms. Neuroimage 2006,
32:1771–1781.!
15.!Correa Á, Lupiáñez J, Madrid E, Tudela P: Temporal attention enhances early
visual processing: A review and new evidence from event-related potentials.
Brain research 2006, 1076:116–128.!
16.!Correa Á, Lupiáñez J, Tudela P: Attentional preparation based on temporal
expectancy modulates processing at the perceptual level. Psychonomic Bulletin
& Review 2005, 12:328–334.!
17.!Coull J, Nobre A: Dissociating explicit timing from temporal expectation with
fMRI. Curr. Opin. Neurobiol. 2008, 18:137–144.!
18.!Coull JT, Cheng R-K, Meck WH: Neuroanatomical and neurochemical substrates
of timing. Neuropsychopharmacology 2011, 36:3–25.!
19.!Droit-Volet S, Meck WH: How emotions colour our perception of time. Trends
Cogn. Sci. (Regul. Ed.) 2007, 11:504–513.!
20.!Eagleman DM, Tse PU, Buonomano D, Janssen P, Nobre AC, Holcombe AO:
Time and the brain: how subjective time relates to neural time. J. Neurosci. 2005,
25:10369–10371.!
Page of 17 23
21.!Fuhrman O, Boroditsky L: Cross-cultural differences in mental representations of
time: evidence from an implicit nonlinguistic task. Cogn Sci 2010, 34:1430–1451.!
22.!Grahn JA, Brett M: Impairment of beat-based rhythm discrimination in
Parkinson’s disease. Cortex 2009, 45:54–61.!
23.!Grahn JA, Brett M: Rhythm and beat perception in motor areas of the brain. J
Cogn Neurosci 2007, 19:893–906.!
24.!Grahn JA, Rowe JB: Feeling the beat: premotor and striatal interactions in
musicians and nonmusicians during beat perception. J. Neurosci. 2009,
29:7540–7548.!
25.!Grahn JA: Neural mechanisms of rhythm perception: current findings and future
perspectives. Top Cogn Sci 2012, 4:585–606.!
26.!Grondin S: Timing and time perception: a review of recent behavioral and
neuroscience findings and theoretical directions. Atten Percept Psychophys
2010, 72:561–582.!
27.!Grosenick L, Marshel JH, Deisseroth K: Closed-loop and activity-guided
optogenetic control. Neuron 2015, 86:106–139.!
28.!Hayashi MJ, Ditye T, Harada T, Hashiguchi M, Sadato N, Carlson S, Walsh V,
Kanai R: Time Adaptation Shows Duration Selectivity in the Human Parietal
Cortex. PLoS Biol. 2015, 13:e1002262.!
29.!Ishihara M, Keller PE, Rossetti Y, Prinz W: Horizontal spatial representations of
time: evidence for the STEARC effect. Cortex 2008, 44:454–461.!
30.!Iversen JR, Repp BH, Patel AD: Top-down control of rhythm perception
modulates early auditory responses. Ann. N. Y. Acad. Sci. 2009, 1169:58–73.!
31.!Ivry RB, Schlerf JE: Dedicated and intrinsic models of time perception. Trends
Cogn. Sci. (Regul. Ed.) 2008, 12:273–280.!
Page of 18 23
32.!Jahanshahi M, Jones CR, Dirnberger G, Frith CD: The substantia nigra pars
compacta and temporal processing. The Journal of neuroscience 2006,
26:12266–12273.!
33.!Kanai R, Paffen CLE, Hogendoorn H, Verstraten FAJ: Time dilation in dynamic
visual display. J Vis 2006, 6:1421–1430.!
34.!Karmarkar UR, Buonomano DV: Timing in the absence of clocks: encoding time
in neural network states. Neuron 2007, 53:427–438.!
35.!Keller PE, Knoblich G, Repp BH: Pianists duet better when they play with
themselves: on the possible role of action simulation in synchronization.
Conscious Cogn 2007, 16:102–111.!
36.!Keller PE: Joint Action in Music Performance. Emerging Communication: Studies
in New Technologies and Practices in Communication 2008, 14: 205-221. IOS
Press Ebooks Volume 10: Enacting Intersubjectivity!
37.!Kornysheva K, Diedrichsen J: Human premotor areas parse sequences into their
spatial and temporal features. Elife 2014, 3:e03043.!
38.!Kotz SA, Schwartze M, Schmidt-Kassow M: Non-motor basal ganglia functions: a
review and proposal for a model of sensory predictability in auditory language
perception. Cortex 2009, 45:982–990.!
39.!Kotz SA, Schwartze M: Cortical speech processing unplugged: A timely
subcortico-cortical framework. Trends in Cognitive Science 2010, 14:392–399.!
40.!Lewis PA, Miall RC: A right hemispheric prefrontal system for cognitive time
measurement. Behavioural Processes 2006, 71:226–234.!
41.!Lewis PA, Miall RC: Remembering the time: a continuous clock. Trends in
cognitive sciences 2006, 10:401–406.!
Page of 19 23
42.!Liu C-H, Coleman JE, Davoudi H, Zhang K, Hussain Shuler MG: Selective
activation of a putative reinforcement signal conditions cued interval timing in
primary visual cortex. Curr. Biol. 2015, 25:1551–1561.!
43.!MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H: Hippocampal “time cells”
bridge the gap in memory for discontiguous events. Neuron 2011, 71:737–749.!
44.!Matlock T, Ramscar M, Boroditsky L: On the experiential link between spatial and
temporal language. Cognitive science 2005, 29:655–664.!
45.!McAuley JD, Jones MR, Holub S, Johnston HM, Miller NS: The time of our lives:
life span development of timing and event tracking. Journal of Experimental
Psychology: General 2006, 135:348.!
46.!Meck WH, Penney TB, Pouthas V: Cortico-striatal representation of time in
animals and humans. Curr. Opin. Neurobiol. 2008, 18:145–152.!
47.!Meck WH: Neuroanatomical localization of an internal clock: a functional link
between mesolimbic, nigrostriatal, and mesocortical dopaminergic systems.
Brain Res. 2006, 1109:93–107.!
48.!Meck WH: Neuropsychology of timing and time perception. Brain Cogn 2005,
58:1–8.!
49.!Mello GBM, Soares S, Paton JJ: A scalable population code for time in the
striatum. Curr. Biol. 2015, 25:1113–1122.!
50.!Merchant H, Harrington DL, Meck WH: Neural basis of the perception and
estimation of time. Annu. Rev. Neurosci. 2013, 36:313–336.!
51.!Merchant H, Pérez O, Zarco W, Gámez J: Interval tuning in the primate medial
premotor cortex as a general timing mechanism. J. Neurosci. 2013, 33:9082–
9096.!
Page of 20 23
52.!Merchant H, Zarco W, Pérez O, Prado L, Bartolo R: Measuring time with different
neural chronometers during a synchronization-continuation task. Proc. Natl.
Acad. Sci. U.S.A. 2011, 108:19784–19789.!
53.!Morrone MC, Ross J, Burr D: Saccadic eye movements cause compression of
time as well as space. Nat. Neurosci. 2005, 8:950–954.!
54.!Namboodiri VMK, Huertas MA, Monk KJ, Shouval HZ, Hussain Shuler MG:
Visually cued action timing in the primary visual cortex. Neuron 2015, 86:319–
330.!
55.!Nobre AC, Correa A, Coull JT: The hazards of time. Current opinion in
neurobiology 2007, 17:465–470.!
56.!Noesselt T, Rieger JW, Schoenfeld MA, Kanowski M, Hinrichs H, Heinze H-J,
Driver J: Audiovisual temporal correspondence modulates human multisensory
superior temporal sulcus plus primary sensory cortices. J. Neurosci. 2007,
27:11431–11441.!
57.!Noulhiane M, Mella N, Samson S, Ragot R, Pouthas V: How emotional auditory
stimuli modulate time perception. Emotion 2007, 7:697–704.!
58.!Nozaradan S, Peretz I, Missal M, Mouraux A: Tagging the neuronal entrainment
to beat and meter. J. Neurosci. 2011, 31:10234–10240.!
59.!Patel AD, Iversen JR, Bregman MR, Schulz I: Experimental evidence for
synchronization to a musical beat in a nonhuman animal. Curr. Biol. 2009,
19:827–830.!
60.!Patel AD, Iversen JR, Chen Y, Repp BH: The influence of metricality and modality
on synchronization with a beat. Exp Brain Res 2005, 163:226–238.!
61.!Rubia K, Halari R, Christakou A, Taylor E: Impulsiveness as a timing disturbance:
neurocognitive abnormalities in attention-deficit hyperactivity disorder during
Page of 21 23
temporal processes and normalization with methylphenidate. Philos. Trans. R.
Soc. Lond., B, Biol. Sci. 2009, 364:1919–1931.!
62.!Schneider BA, Ghose GM: Temporal production signals in parietal cortex. PLoS
Biol. 2012, 10:e1001413.!
63.!Shuler MG, Bear MF: Reward timing in the primary visual cortex. Science 2006,
311:1606–1609.!
64.!Styns F, van Noorden L, Moelants D, Leman M: Walking on music. Hum Mov Sci
2007, 26:769–785.!
65.!Taatgen NA, van Rijn H, Anderson J: An integrated theory of prospective time
interval estimation: the role of cognition, attention, and learning. Psychol Rev
2007, 114:577–598.!
66.!Teki S, Grube M, Griffiths TD: A unified model of time perception accounts for
duration-based and beat-based timing mechanisms. Front Integr Neurosci 2011,
5:90.!
67.!Teki S, Grube M, Kumar S, Griffiths TD: Distinct neural substrates of duration-
based and beat-based auditory timing. J. Neurosci. 2011, 31:3805–3812.!
68.!Vatakis A, Spence C: Audiovisual synchrony perception for music, speech, and
object actions. Brain Res. 2006, 1111:134–142.!
69.!Vroomen J, Keetels M: Perception of intersensory synchrony: a tutorial review.
Attention, Perception, & Psychophysics 2010, 72:871–884.!
70.!Wearden JH, Norton R, Martin S, Montford-Bebb O: Internal clock processes and
the filled-duration illusion. Journal of Experimental Psychology: Human
Perception and Performance 2007, 33:716.!
71.!Wiener M, Turkeltaub P, Coslett HB: The image of time: a voxel-wise meta-
analysis. Neuroimage 2010, 49:1728–1740.!
Page of 22 23
72.!Winkler I, Háden GP, Ladinig O, Sziller I, Honing H: Newborn infants detect the
beat in music. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2468–2471.!
73.!Wittmann M, Dinich J, Merrow M, Roenneberg T: Social jetlag: misalignment of
biological and social time. Chronobiol. Int. 2006, 23:497–509.!
74.!Wittmann M, Leland DS, Paulus MP: Time and decision making: differential
contribution of the posterior insular cortex and the striatum during a delay
discounting task. Exp Brain Res 2007, 179:643–653.!
75.!Wittmann M, Paulus MP: Decision making, impulsivity and time perception.
Trends Cogn. Sci. (Regul. Ed.) 2008, 12:7–12.!
76.!Wittmann M: The inner experience of time. Philos. Trans. R. Soc. Lond., B, Biol.
Sci. 2009, 364:1955–1967.!
77.!Zarco W, Merchant H, Prado L, Mendez JC: Subsecond timing in primates:
comparison of interval production between human subjects and rhesus monkeys.
J. Neurophysiol. 2009, 102:3191–3202.!
!
!
Page of 23 23
... Teki [30] recently posted his views on ways in which the field can further nurture and support young investigators, indicating that an academic society designed exclusively for timing researchers would help to promote interdisciplinary exchange and provide various types of support for career development. ...
... Teki [31] recently posted his views on ways in which the field can further nurture and support young investigators, indicating that an academic society designed exclusively for timing researchers would help to promote interdisciplinary exchange and provide various types of support for career development. ...
... Teki [32] recently posted his views on ways in which the field can further nurture and support young investigators, indicating that an academic society designed exclusively for timing researchers would help to promote interdisciplinary exchange and provide various types of support for career development. ...
Article
Full-text available
Skilled performance is characterized by precise and flexible control of movement sequences in space and time. Recent theories suggest that integrated spatio-temporal trajectories are generated by intrinsic dynamics of motor and premotor networks. This contrasts with behavioural advantages that emerge when a trained spatial or temporal feature of sequences is transferred to a new spatio-temporal combination arguing for independent neural representations of these sequence features. We used a new fMRI pattern classification approach to identify brain regions with independent vs integrated representations. A distinct regional dissociation within motor areas was revealed: whereas only the contralateral primary motor cortex exhibited unique patterns for each spatio-temporal sequence combination, bilateral premotor areas represented spatial and temporal features independently of each other. These findings advocate a unique function of higher motor areas for flexible recombination and efficient encoding of complex motor behaviours.
Article
Full-text available
Author Summary The human brain has the ability to estimate the passage of time, which allows us to perform complex cognitive tasks such as playing music, dancing, and understanding speech. Scientists have just begun to understand which brain areas become active when we estimate time. However, it still remains a mystery how exactly the information about time is represented in the brain. In this study, we hypothesized that time might be represented by neurons that are specifically tuned to a specific duration, as has been known for simple visual features such as the orientation and the motion direction in the visual cortex. To test this idea, we performed multiple functional magnetic resonance imaging (fMRI) adaptation experiments in which we sought evidence of neuronal adaptation, that is, a reduction in the responsiveness of neurons to repeated presentations of similar durations. Our experiments revealed that the level of brain activity in the right inferior parietal lobule (IPL) was strongly reduced when a stimulus of the same duration was repeatedly presented. This finding was reproduced for a range of subsecond durations. Our results indicate that neurons in the human IPL are tuned to specific preferred durations.
Article
Full-text available
As a consequence of conditioning visual cues with delayed reward, cue-evoked neural activity that predicts the time of expected future reward emerges in the primary visual cortex (V1). We hypothesized that this reward-timing activity is engendered by a reinforcement signal conveying reward acquisition to V1. In lieu of behavioral conditioning, we assessed in vivo whether selective activation of either basal forebrain (BF) or cholinergic innervation is sufficient to condition cued interval-timing activity. Substituting for actual reward, optogenetic activation of BF or cholinergic input within V1 at fixed delays following visual stimulation entrains neural responses that mimic behaviorally conditioned reward-timing activity. Optogenetically conditioned neural responses express cue-evoked temporal intervals that correspond to the conditioning intervals, are bidirectionally modifiable, display experience-dependent refinement, and exhibit a scale invariance to the encoded delay. Our results demonstrate that the activation of BF or cholinergic input within V1 is sufficient to encode cued interval-timing activity and indicate that V1 itself is a substrate for associative learning that may inform the timing of visually cued behaviors. Copyright © 2015 Elsevier Ltd. All rights reserved.
Article
Full-text available
β oscillations in the basal ganglia have been associated with interval timing. We recorded the putaminal local field potentials (LFPs) from monkeys performing a synchronization-continuation task (SCT) and a serial reaction-time task (RTT), where the animals produced regularly and irregularly paced tapping sequences, respectively. We compared the activation profile of β oscillations between tasks and found transient bursts of β activity in both the RTT and SCT. During the RTT, β power was higher at the beginning of the task, especially when LFPs were aligned to the stimuli. During the SCT, β was higher during the internally driven continuation phase, especially for tap-aligned LFPs. Interestingly, a set of LFPs showed an initial burst of β at the beginning of the SCT, similar to the RTT, followed by a decrease in β oscillations during the synchronization phase, to finally rebound during the continuation phase. The rebound during the continuation phase of the SCT suggests that the corticostriatal circuit is involved in the control of internally driven motor sequences. In turn, the transient bursts of β activity at the beginning of both tasks suggest that the basal ganglia produce a general initiation signal that engages the motor system in different sequential behaviors. Copyright © 2015 the authors 0270-6474/15/354635-06$15.00/0.
Article
Full-text available
The graceful, purposeful motion of our body is an engineering feat that remains unparalleled in robotic devices using advanced artificial intelligence. Much of the information required for complex movements is generated by the cerebellum and the basal ganglia in conjunction with the cortex. Cerebellum and basal ganglia have been thought to communicate with each other only through slow, multi-synaptic cortical loops, begging the question as to how they coordinate their outputs in real time. We found that the cerebellum rapidly modulates the activity of the striatum via a disynaptic pathway in mice. Under physiological conditions, this short latency pathway was capable of facilitating optimal motor control by allowing the basal ganglia to incorporate time-sensitive cerebellar information and by guiding the sign of cortico-striatal plasticity. Conversely, under pathological condition, this pathway relayed aberrant cerebellar activity to the basal ganglia to cause dystonia.
Article
How does the brain estimate time? This old question has led to many biological and psychological models of time perception (R. A. Block, 1989; P. Fraisse, 1963; J. Gibbon, 1977; D. L. I. Zakay, 1989). Because time cannot be directly measured at a given moment, it has been proposed that the brain estimates time based on the number of changes in an event (S. W. Brown, 1995; P. Fraisse, 1963; W. D. Poynter, 1989). Consistent with this idea, dynamic visual stimuli are known to lengthen perceived time (J. F. Brown, 1931; S. Goldstone & W. T. Lhamon, 1974; W. T. Lhamon & S. Goldstone, 1974, C. O. Z. Roelofs & W. P. C. Zeeman, 1951). However, the kind of information that constitutes the basis for time perception remains unresolved. Here, we show that the temporal frequency of a stimulus serves as the "clock" for perceived duration. Other aspects of changes, such as speed or coherence, were found to be inconsequential. Time dilation saturated at a temporal frequency of 4-8 Hz. These results suggest that the clock governing perceived time has its basis at early processing stages. The possible links between models of time perception and neurophysiological functions of early visual areas are discussed.
Article
To guide behavior and learn from its consequences, the brain must represent time over many scales. Yet, the neural signals used to encode time in the seconds-to-minute range are not known. The striatum is a major input area of the basal ganglia associated with learning and motor function. Previous studies have also shown that the striatum is necessary for normal timing behavior. To address how striatal signals might be involved in timing, we recorded from striatal neurons in rats performing an interval timing task. We found that neurons fired at delays spanning tens of seconds and that this pattern of responding reflected the interaction between time and the animals' ongoing sensorimotor state. Surprisingly, cells rescaled responses in time when intervals changed, indicating that striatal populations encoded relative time. Moreover, time estimates decoded from activity predicted timing behavior as animals adjusted to new intervals, and disrupting striatal function led to a decrease in timing performance. These results suggest that striatal activity forms a scalable population code for time, providing timing signals that animals use to guide their actions. Copyright © 2015 Elsevier Ltd. All rights reserved.
Article
Advances in optical manipulation and observation of neural activity have set the stage for widespread implementation of closed-loop and activity-guided optical control of neural circuit dynamics. Closing the loop optogenetically (i.e., basing optogenetic stimulation on simultaneously observed dynamics in a principled way) is a powerful strategy for causal investigation of neural circuitry. In particular, observing and feeding back the effects of circuit interventions on physiologically relevant timescales is valuable for directly testing whether inferred models of dynamics, connectivity, and causation are accurate in vivo. Here we highlight technical and theoretical foundations as well as recent advances and opportunities in this area, and we review in detail the known caveats and limitations of optogenetic experimentation in the context of addressing these challenges with closed-loop optogenetic control in behaving animals. Copyright © 2015 Elsevier Inc. All rights reserved.
Article
Most behaviors are generated in three steps: sensing the external world, processing that information to instruct decision-making, and producing a motor action. Sensory areas, especially primary sensory cortices, have long been held to be involved only in the first step of this sequence. Here, we develop a visually cued interval timing task that requires rats to decide when to perform an action following a brief visual stimulus. Using single-unit recordings and optogenetics in this task, we show that activity generated by the primary visual cortex (V1) embodies the target interval and may instruct the decision to time the action on a trial-by-trial basis. A spiking neuronal model of local recurrent connections in V1 produces neural responses that predict and drive the timing of future actions, rationalizing our observations. Our data demonstrate that the primary visual cortex may contribute to the instruction of visually cued timed actions. Copyright © 2015 Elsevier Inc. All rights reserved.
Article
Two fundamental cognitive functions, selective attention and processing of time, have been simultaneously explored in recent studies of temporal orienting of attention. A temporal-orienting procedure may consist of a temporal analogue to the Posner's paradigm, such that symbolic cues indicate the most probable moment for target arrival. Behavioral measures suggest that performance is improved for events appearing at expected vs. unexpected moments. However, there is no agreement on the locus of stimulus processing at which temporal attention operates. Thus, it remains unclear whether early perceptual or just late motor processes can be modulated. This article reviews current ERP research on temporal orienting, with an emphasis on factors that might determine the modulation of temporal orienting at early stages of processing. We conclude that: First, late components (N2 and P300) are consistently modulated by temporal orienting, which suggests attentional preparation of decision and/or motor processes. Second, early components (e.g., N1) seem to be modulated only when the task is highly demanding in perceptual processing. Hence, we conducted an ERP experiment which aimed to observe a modulation of early visual processing by using a perceptually demanding task, such as letter discrimination. The results show, for the first time, that targets appearing at attended moments elicited a larger P1 component than unattended targets. Moreover, temporal attention modulated the amplitude and latency of N2 and P300 components. This suggests that temporal orienting of attention not only modulates late motor processing, but also early visual processing when perceptually demanding tasks are used.