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Beta drives brain beats

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OPINION ARTICLE
published: 27 August 2014
doi: 10.3389/fnsys.2014.00155
Beta drives brain beats
Sundeep Teki1,2*
1Auditory Cognition Group, Wellcome Trust Centre for Neuroimaging, University College London, London, UK
2Institute of Neuroscience, Newcastle University, Newcastle-upon-Tyne, UK
*Correspondence: sundeep.teki@gmail.com
Edited by:
Federico Bermudez-Rattoni, Universidad Nacional Autónoma de México, Mexico
Reviewed by:
Sacha Jennifer Van Albada, Research Center Jülich, Germany
Sidney A. Simon, Duke University, USA
Keywords: interval timing, beta oscillations, timing and time perception, sensorimotor integration, beat perception, beat-based timing, interval tuning
Beta-band oscillations in basal ganglia-
corticalloopshavebeenshowntobe
linked to motor function in both healthy
and pathological states (Brown, 2007;
Engel and Fries, 2010). As well as coordi-
nating motor activity, for instance when
we synchronize our movements to a beat,
the basal ganglia including the putamen
and the caudate are said to contain spe-
cialized timekeeping mechanisms for per-
ceptual timing (Buhusi and Meck, 2005).
However, the exact neurophysiological role
of beta-band oscillatory activity in the
striatum in interval timing is not yet
known.
In a recent study published in The
Journal of Neuroscience,Bartolo et al.
(2014) examined the role of beta oscilla-
tions in interval timing by directly record-
ing from the putamen in macaques during
a rhythmic synchronization task. In this
paradigm, a metronome is used to estab-
lish an isochronous beat (synchronization
phase) and the variability in the subse-
quent taps produced by the subject after
the metronome is turned off (continuation
phase) is evaluated as an index of inter-
nal timing behavior. Single-unit as well as
local field potential (LFP) activity in the
putamen in the beta and gamma range was
analyzed to determine the neural corre-
lates of interval timing.
They found that LFPs in the beta band
exhibit interval tuning and showed a pref-
erence for intervals with duration around
800 ms, similar to the preferred duration
observed in medial premotor cortex neu-
rons (Merchant et al., 2013). They also
reported tuning for serial order (or the
task phases): LFPs in the beta band showed
preferential tuning for the continuation
phase that relies on internal timing whilst
gamma band LFPs showed a bias toward
the synchronization phase that depends
on precise sensory coding. Another sig-
nificant result suggests that beta oscil-
lations are coherent at large electrode
distances within the putamen that may
reflect functional coordination across sev-
eral areas of the putamen, and possibly the
wider sensorimotor network for tempo-
ral processing. On the other hand, gamma
oscillations showed small coherence asso-
ciated most likely with local stimulus
processing.
The present study and previous work
from this group (Merchant et al., 2011,
2013)arebasedonanarduousmethod-
ological approach where macaques are
trained to perform complex tapping tasks
based on sequences of intervals rather
than single isolated intervals and disam-
biguating stimulus-related neural activity
from movement-related responses (Perez
et al., 2013). Natural acoustic signals con-
sist of sequences of time intervals, and it
is important not only to encode the dura-
tion of individual sounds but also the serial
order in which they are presented. The cur-
rent study is the first to show evidence of
both interval and serial order tuning in
such sequences in the beta-band responses
in the putamen.
The present study only addresses inter-
nal timing in regular sequences and it is
not yet known how temporal jitter would
affect the putaminal beta-band activity.
In irregular sequences, beta-band modula-
tion may remain the same or change as a
function of the amount of jitter. As natural
sounds are rarely presented in a tempo-
rally regular context, future work needs to
address how the brain perceives time in
irregular sequences. Related to this ques-
tion, Fujioka et al. (2012) used magne-
toencephalography to examine the nature
of beta-band responses in the auditory
cortex during passive listening to regular
and random sequences. They found that
the beta desynchronization after stimu-
lus onset did not vary with the regularity
of the stimulus, but the subsequent beta
rebound peaked just before the next sound
onset only for the regular stimuli.
Temporal processing in irregular
sequences has been shown to be prefer-
entially mediated by a network based in
the cerebellum whilst timing in regular
sequences is carried out by a striato-
frontal network (Teki et al., 2011). The
cerebellum is another key node of the
temporal processing network (Ivry and
Spencer, 2004) and recent theoretical
models emphasize the involvement of both
the cerebellum and the basal ganglia that
are inter-connected with each other and
the cortex through multiple synaptic path-
ways (Teki et al., 2012; Allman et al., 2014).
Fujioka et al. (2012) demonstrated beta-
band coherence between auditory and
motor-related areas including the cere-
bellum but it remains to be investigated
whether such functional coupling during
interval timing is driven by the cerebellum,
the basal ganglia, or by a different brain
area that influences activity in both these
core timing areas.
Bartolo et al. (2014) only briefly men-
tion predictive coding mechanisms in
bottom-up (synchronization phase) and
top-down (continuation phase) process-
ing. Bastos et al. (2012) recently proposed
a canonical microcircuit for predictive
Frontiers in Systems Neuroscience www.frontiersin.org August 2014 | Volume 8 | Article 155 |1
SYSTEMS NEUROSCIENC
E
Teki Beta drives brain beats
coding based on iterative message pass-
ing between bottom-up stimulus-driven
processing (in the gamma range) by
superficial cortical neurons and top-
down coding of predictive signals by
deep cortical cells (in the beta range).
A predictive model can be invoked in
the context of the present rhythmic syn-
chronization task where tapping to the
metronome during the synchronization
phase helps establish an internal model of
the timing between successive metronome
pulses and subsequent taps following the
removal of the metronome may be driven
by predictive signals. The findings of pref-
erential gamma modulation during the
synchronization phase and beta modula-
tion during the continuation phase ties in
with such a predictive coding framework.
A hierarchical model for predictive coding
may be anatomically realizable even locally
within the striatum where there is evidence
of prediction error coding by the caudate
nucleus and ventral striatum whilst the
putamen encodes the prediction (Haruno
and Kawato, 2006). This hypothesis is sup-
ported by functional magnetic resonance
imaging data showing that the putamen
is specifically involved in internal predic-
tion of beats rather than detection of beats
(Grahn and Rowe, 2013).
In summary, this stimulating work on
the role of putamen during internally
driven timing behavior significantly adds
to previous work by Merchant and col-
leagues based on recordings from medial
premotor cortex (Merchant et al., 2011,
2013). It emphasizes the role of endoge-
nous beta oscillations in the basal ganglia
as a principal feature of interval timing in
a regular, beat-based context. The study
underlines the importance of local electro-
physiological recordings in key areas of the
animal brain to inform models of inter-
val timing and rhythmic synchronization
in humans (Teki et al., 2012)aswell
as non-human primates (Merchant and
Honing, 2014).
ACKNOWLEDGMENT
Sundeep Teki is supported by the
Wellcome Trust, UK.
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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.
Received: 12 June 2014; accepted: 08 August 2014;
published online: 27 August 2014.
Citation: Teki S (2014) Beta drives brain beats. Front.
Syst. Neurosci. 8:155. doi: 10.3389/fnsys.2014.00155
This article was submitted to the journal Frontiers in
Systems Neuroscience.
Copyright © 2014 Teki. This is an open-access article
distributed under the terms of the Creative Commons
Attribution License (CC BY). The use, distribution or
reproduction in other forums is permitted, provided the
original author(s) or licensor are credited and that the
original publication in this journal is cited, in accor-
dance with accepted academic practice. No use, distribu-
tion or reproduction is permitted which does not comply
with these terms.
Frontiers in Systems Neuroscience www.frontiersin.org August 2014 | Volume 8 | Article 155 |2
... The supplementary motor area and basal ganglia for 22 instance have been repeatedly reported to be more engaged in beat-based timing [14], 23 and that with further sub-specialization in finding vs. keeping the beat for instance [15]. 24 However, findings are not entirely consistent in terms of the specificity of criticalness 25 (e.g. [16,17]), in part probably due to differences in lesions or tasks. ...
... [20]). More specifically, the timing 31 system has been promoted to feature the entrainment of neural oscillations in the beta 32 range (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) with the periodicity of the beat in musical rhythms [21]. 33 In attempts to get to the bottom of the structural and functional neural correlates 34 that underlie our entrainment with and "feeling of the beat", previous MEG and EEG 35 work both demonstrated clear effects in oscillatory activity. ...
... These activity patterns were extracted as the result of an anatomically guided 41 analysis and appeared most prominently in the auditory cortex of the temporal lobe. 42 Further support for the beta band "driving the brain on beats" came from related EEG 43 work ( [23], Chang / Tillmann ?) with converging conclusions [24]. 44 We here present an alternative, customised, and open-source machine-learning 45 analysis pipeline that enables us to extract in a data-driven way the maximally relevant 46 brain activity in source space. ...
Fourier SPoC: A customised machine-learning analysis pipeline for auditory beat-based entrainment in the MEG
Preprint
Full-text available
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We propose here (the informed use) of a customised, data-driven machine-learning pipeline to analyse magnetoencephalography (MEG) in a theoretical source space, with respect to the processing of a regular beat. This hypothesis- and data-driven analysis pipeline allows us to extract the maximally relevant components in MEG source-space, with respect to the oscillatory power in the frequency band of interest and, most importantly, the beat-related modulation of that power. Our pipeline combines Spatio-Spectral Decomposition as a first step to seek activity in the frequency band of interest (SSD, [1]) with a Source Power Co-modulation analysis (SPoC; [2]), which extracts those components that maximally entrain their activity with the given target function, that is here with the periodicity of the beat in the frequency domain (hence, f-SPoC). MEG data (102 magnetometers) from 28 participants passively listening to a 5-min long regular tone sequence with a 400 ms beat period (the “target function” for SPoC) were segmented into epochs of two beat periods each to guarantee a sufficiently long time window. As a comparison pipeline to SSD and f-SpoC, we carried out a state-of-the-art cluster-based permutation analysis (CBPA, [3]). The time-frequency analysis (TFA) of the extracted activity showed clear regular patterns of periodically occurring peaks and troughs across the alpha and beta band (8-20 Hz) in the f-SPoC but not in the CBPA results, and both the depth and the specificity of modulation to the beat frequency yielded a significant advantage. Future applications of this pipeline will address target the relevance to behaviour and inform analogous analyses in the EEG, in order to finally work toward addressing dysfunctions in beat-based timing and their consequences. Author summary When listening to a regular beat, oscillations in the brain have been shown to synchronise with the frequency of that given beat. This phenomenon is called entrainment and has in previous brain-imaging studies been shown in the form of one peak and trough per beat cycle in a range of frequency bands within 15-25 Hz (beta band). Using machine-learning techniques, we designed an analysis pipeline based on Source-Power Co-Modulation (SPoC) that enables us to extract spatial components in MEG recordings that show these synchronisation effects very clearly especially across 8-20 Hz. This approach requires no anatomical knowledge of the individual or even the average brain, it is purely data driven and can be applied in a hypothesis-driven fashion with respect to the “function” that we expect the brain to entrain with and the frequency band within which we expect to see this entrainment. We here apply our customised pipeline using “f-SPoC” to MEG recordings from 28 participants passively listening to a 5-min long tone sequence with a regular 2.5 Hz beat. In comparison to a cluster-based permutation analysis (CBPA) which finds sensors that show statistically significant power modulations across participants, our individually extracted f-SPoC components find a much stronger and clearer pattern of peaks and troughs within one beat cycle. In future work, this pipeline can be implemented to tackle more complex “target functions” like speech and music, and might pave the way toward rhythm-based rehabilitation strategies.
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... Actually, the non-DBS patients showed a beta oscillatory activity increase externally to the double support and a lack of beta suppression during contralateral foot lift, which is in keeping with the detrimental beta oscillatory activity along the basal ganglia-thalamo-cortical circuitry in patients with PD (23,50,60,71,72,(85)(86)(87)(88)(89)(90). This condition reflects the restriction of patients with PD into timing function-based motor tasks and the hastening phenomenon (i.e., the involuntarily acceleration of motion instead of precisely synchronizing with rhythmic external cues) (24,(91)(92)(93). ...
... All the above mentioned issues suggest that the oscillatory effects we observed are likely to depend on the improvement of the basal ganglia-thalamo-cortical circuitry induced by the synergy between RAS plus physiotherapy and DBS. The former activates gait-related sensorimotor and auditory-motor coordination network at cortical level (through basal gangliathalamo-cortical circuitry that plays a critical role in modulating beta band activity during synchronization tasks (i.e., RAS treadmill) (42,43,93,97,98,101,102). The association between audiomotor synchronization and the amount of sensorimotor information related to gait execution, together with DBS stimulation, may modulate beta oscillations within basal ganglia-thalamo-cortical circuits that contribute to long-term potentiation(LTP)-like and spike-timing dependent plasticity mechanisms at the cortical level (maybe through GABAergic and cholinergic neural transmission) (103)(104)(105)(106)(107)(108)(109)(110)(111). ...
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Deep brain stimulation (DBS) is indicated when motor disturbances in patients with idiopathic Parkinson's disease (PD) are refractory to current treatment options and significantly impair quality of life. However, post–DBS rehabilitation is essential, with particular regard to gait. Rhythmic auditory stimulation (RAS)-assisted treadmill gait rehabilitation within conventional physiotherapy program plays a major role in gait recovery. We explored the effects of a monthly RAS–assisted treadmill training within a conventional physiotherapy program on gait performance and gait-related EEG dynamics (while walking on the RAS–aided treadmill) in PD patients with (n = 10) and without DBS (n = 10). Patients with DBS achieved superior results than those without DBS concerning gait velocity, overall motor performance, and the timed velocity and self-confidence in balance, sit-to-stand (and vice versa) and walking, whereas both groups improved in dynamic and static balance, overall cognitive performance, and the fear of falling. The difference in motor outcomes between the two groups was paralleled by a stronger remodulation of gait cycle–related beta oscillations in patients with DBS as compared to those without DBS. Our work suggests that RAS-assisted gait training plus conventional physiotherapy is a useful strategy to improve gait performance in PD patients with and without DBS. Interestingly, patients with DBS may benefit more from this approach owing to a more focused and dynamic re–configuration of sensorimotor network beta oscillations related to gait secondary to the association between RAS-treadmill, conventional physiotherapy, and DBS. Actually, the coupling of these approaches may help restoring a residually altered beta–band response profile despite DBS intervention, thus better tailoring the gait rehabilitation of these PD patients.
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... The ability to predict the timing of natural sounds is essential for accurate comprehension of speech and music (Allman et al., 2014). Rhythmic activity in the beta range (12-30 Hz) is crucial for encoding the temporal structure of regular sound sequences (Fujioka et al., 2009(Fujioka et al., , 2012Bartolo et al., 2014;Teki, 2014;Bartolo and Merchant, 2015). Specifically, the power of induced beta oscillations in the auditory cortex is dynamically modulated according to the temporal pattern of beats (Fujioka et al., 2012), such that beat-related induced beta power decreases after the beat and then increases preceding the next beat as depicted in Figure 1A. ...
... Specifically, desynchronization of induced beta power may reflect memory formation (Hanslmayr and Staudigl, 2014) or an active change in sensorimotor processing (Pfurtscheller and Lopes da Silva, 1999). During rhythm perception, where encoding the beat in memory is critical (Teki andGriffiths, 2014, 2016) the structure of the metrical accents and salient events may be represented by the depth of beta desynchronization. Therefore, the largest beta desynchronization may be expected to occur after the downbeat ( Figure 1C). ...
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The ability to predict the timing of natural sounds is essential for accurate comprehension of speech and music (Allman et al., 2014). Rhythmic activity in the beta range (12–30 Hz) is crucial for encoding the temporal structure of regular sound sequences (Fujioka et al., 2009, 2012; Bartolo et al., 2014; Teki, 2014; Bartolo and Merchant, 2015). Specifically, the power of induced beta oscillations in the auditory cortex is dynamically modulated according to the temporal pattern of beats (Fujioka et al., 2012), such that beat-related induced beta power decreases after the beat and then increases preceding the next beat as depicted in Figure Figure1A.1A. However, it is not known whether beta oscillations encode the beat positions in metrical sequences with physically or subjectively accented beats (i.e., “upbeat” and “downbeat”) and whether this is accomplished in a predictive manner or not.
View
... Power increases in the beta fre Li et al. Journal of Neurolinguistics xxx (2018) xxx-xxx quency band have been found to be related to top-down control process, such as maintaining the current cognitive/neural set or neural preparation for temporally expected stimuli (e.g., Fujioka et al., 2012;Gulberti et al., 2015;Kilavik, Zaepffel, Brovelli, MacKay, & Riehle, 2013;Lewis et al., 2015;Merchant, Grahn, Trainor, Rohrmeier, & Fitch, 2015;Patel & Iversen, 2014;Teki, 2014;de Lange et al., 2013). Given the reasons mentioned above, beta power increases observed here suggest that the human brain might have been entrained to the rhythmic temporal structure of the sentence context, and is maintaining the current cognitive process (e.g., segmenting the speech stream in a two-syllable by two-syllable manner) to be better prepared for the processing of upcoming speech input. ...
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... The reduced motor entrainment raises also questions regarding the contribution of the basal ganglia-motor system in attentional control. Motor circuits and the basal ganglia play an important role in internal rhythm generation and the formation of temporal predictions (Bartolo, Prado, & Merchant, 2014;Grahn & Rowe, 2009Teki, 2014), and it has been suggested that these temporal predictions are coded in beta oscillatory activity (Arnal, 2012;Bartolo et al., 2014;Gulberti et al., 2015). Studies have shown that these temporal predictions are being sent back to sensory areas, and can alter the processing of sensory stimuli (Morillon, Schroeder, & Wyart, 2014. ...
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... Modulation of auditory cortical activity in the beta band has been shown to track the clicks of a metronome, while gamma oscillations appear to encode anticipated stimulus timing as evidenced by a peak in gamma activity even in the absence of a click ( Fujioka et al., 2009). Beta oscillations have also been demonstrated to encode beat and meter imagery ( Iversen et al., 2009;Fujioka et al., 2015), and the dynamics of induced beta oscillatory activity both in humans ( Teki, 2014) and in nonhuman primates ( Bartolo et al., 2014;Bartolo and Merchant, 2015) (see the later section on Beat processing in nonhuman species), have been shown to vary according to the temporal regularity of sound sequences. In addition to beta, gamma band oscillations also appear to encode beat and meter ( Snyder and Large, 2005;Zanto et al., 2006), and entrainment in the low-frequency delta-theta band (<8 Hz) has also been shown to correlate with years of musical training ( Doelling and Poeppel, 2015). ...
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... Based on all this evidence, it seems reasonable to consider that the mCBGT circuit is part of the beat-based timing mechanism that exhibits a global entrainment in the beta band during the production of internally timed movements in the SCT (Teki 2014). The network entrainment in the beta band during internally driven rhythmic movements reduces interference from sensory inputs, permitting the internal clock to take control of the timing behavior ). ...
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The study of non-human primates in complex behaviors such as rhythm perception and entrainment is critical to understand the neurophysiological basis of human cognition. Next to reviewing the role of beta oscillations in human beat perception, here we discuss the role of primate putaminal oscillatory activity in the control of rhythmic movements that are guided by a sensory metronome or internally gated. The analysis of the local field potentials of the behaving macaques showed that gamma-oscillations reflect local computations associated with stimulus processing of the metronome, whereas beta-activity involves the entrainment of large putaminal circuits, probably in conjunction with other elements of cortico-basal ganglia-thalamo-cortical circuit, during internally driven rhythmic tapping. Thus, this review emphasizes the need of parametric neurophysiological observations in non-human primates that display a well-controlled behavior during high-level cognitive processes.
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Full-text available
  • Sep 2017
The ability to precisely anticipate the timing of upcoming events at the time-scale of seconds is essential to predict objects' trajectories or to select relevant sensory information. What neurophysiological mechanism underlies the temporal precision in anticipating the occurrence of events? In a recent article ¹ Arnal LH, Doelling KB, Poeppel D. Delta-beta coupled oscillations underlie temporal prediction accuracy. Cereb Cortex 2015; 25:3077-85.[Crossref], [PubMed], [Web of Science ®] [Google Scholar], we demonstrated that the sensori-motor system predictively controls neural oscillations in time to optimize sensory selection. However, whether and how the same oscillatory processes can be used to keep track of elapsing time and evaluate short durations remains unclear. Here, we aim at testing the hypothesis that the brain tracks durations by converting (external, objective) elapsing time into an (internal, subjective) oscillatory phase-angle. To test this, we measured magnetoencephalographic oscillatory activity while participants performed a delayed-target detection task. In the delayed condition, we observe that trials that are perceived as longer are associated with faster delta-band oscillations. This suggests that the subjective indexing of time is reflected in the range of phase-angles covered by delta oscillations during the pre-stimulus period. This result provides new insights into how we predict and evaluate temporal structure and support models in which the active entrainment of sensori-motor oscillatory dynamics is exploited to track elapsing time.
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Information Processing in the Primate Basal Ganglia during Sensory-Guided and Internally Driven Rhythmic Tapping
Article
Full-text available
  • Mar 2014
  • J NEUROSCI
Gamma (γ) and beta (β) oscillations seem to play complementary functions in the cortico-basal ganglia-thalamo-cortical circuit (CBGT) during motor behavior. We investigated the time-varying changes of the putaminal spiking activity and the spectral power of local field potentials (LFPs) during a task where the rhythmic tapping of monkeys was guided by isochronous stimuli separated by a fixed duration (synchronization phase), followed by a period of internally timed movements (continuation phase). We found that the power of both bands and the discharge rate of cells showed an orderly change in magnitude as a function of the duration and/or the serial order of the intervals executed rhythmically. More LFPs were tuned to duration and/or serial order in the β- than the γ-band, although different values of preferred features were represented by single cells and by both bands. Importantly, in the LFPs tuned to serial order, there was a strong bias toward the continuation phase for the β-band when aligned to movements, and a bias toward the synchronization phase for the γ-band when aligned to the stimuli. Our results suggest that γ-oscillations reflect local computations associated with stimulus processing, whereas β-activity involves the entrainment of large putaminal circuits, probably in conjunction with other elements of CBGT, during internally driven rhythmic tapping.
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Are non-human primates capable of rhythmic entrainment? Evidence for the gradual audiomotor evolution hypothesis
Article
Full-text available
  • Jan 2014
We propose a decomposition of the neurocognitive mechanisms that might underlie interval-based timing and rhythmic entrainment. Next to reviewing the concepts central to the definition of rhythmic entrainment, we discuss recent studies that suggest rhythmic entrainment to be specific to humans and a selected group of bird species, but, surprisingly, is not obvious in non-human primates. On the basis of these studies we propose the gradual audiomotor evolution hypothesis that suggests that humans fully share interval-based timing with other primates, but only partially share the ability of rhythmic entrainment (or beat-based timing). This hypothesis accommodates the fact that non-human primates (i.e., macaques) performance is comparable to humans in single interval tasks (such as interval reproduction, categorization, and interception), but show differences in multiple interval tasks (such as rhythmic entrainment, synchronization, and continuation). Furthermore, it is in line with the observation that macaques can, apparently, synchronize in the visual domain, but show less sensitivity in the auditory domain. And finally, while macaques are sensitive to interval-based timing and rhythmic grouping, the absence of a strong coupling between the auditory and motor system of non-human primates might be the reason why macaques cannot rhythmically entrain in the way humans do.
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Functional and Neural Mechanisms of Interval Timing
Book
Full-text available
  • Mar 2003
Understanding temporal integration by the brain is expected to be among the premier topics to unite systems, cellular, computational, and cognitive neuroscience over the next decade. The phenomenon has been studied in humans and animals, yet until now, there has been no publication to successfully bring together the latest information gathered from this exciting area of research. For the first time, Functional and Neural Mechanisms of Interval Timing synthesizes the current knowledge of both animal behavior and human cognition as related to both technical and theoretical approaches in the study of duration discrimination. Chapters written by the foremost experts in the field integrate the fields of time quantum and psychophysics, rhythmic performance and synchronization, as well as attentional effort and cognitive strategies through the linkage of time as information in brain and behavior. This cutting-edge scientific work promotes a concerted view of timing and time perception for those on both sides of the behavior-biology divide. With Functional and Neural Mechanisms of Interval Timing neuroscientists, ethologists, and psychologists will gain the necessary background to understand the psychophysics and neurobiology of this crucial behavior.
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Properties of the Internal Clock: First- and Second-Order Principles of Subjective Time
Article
Full-text available
  • Jan 2014
  • ANNU REV PSYCHOL
Humans share with other animals an ability to measure the passage of physical time and subjectively experience a sense of time passing. Subjective time has hallmark qualities, akin to other senses, which can be accounted for by formal, psychological, and neurobiological models of the internal clock. These include first-order principles, such as changes in clock speed and how temporal memories are stored, and second-order principles, including timescale invariance, multisensory integration, rhythmical structure, and attentional time-sharing. Within these principles there are both typical individual differences-influences of emotionality, thought speed, and psychoactive drugs-and atypical differences in individuals affected with certain clinical disorders (e.g., autism, Parkinson's disease, and schizophrenia). This review summarizes recent behavioral and neurobiological findings and provides a theoretical framework for considering how changes in the properties of the internal clock impact time perception and other psychological domains. Expected final online publication date for the Annual Review of Psychology Volume 65 is January 03, 2014. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
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Interval Tuning in the Primate Medial Premotor Cortex as a General Timing Mechanism
Article
Full-text available
  • May 2013
  • J NEUROSCI
The precise quantification of time during motor performance is critical for many complex behaviors, including musical execution, speech articulation, and sports; however, its neural mechanisms are primarily unknown. We found that neurons in the medial premotor cortex (MPC) of behaving monkeys are tuned to the duration of produced intervals during rhythmic tapping tasks. Interval-tuned neurons showed similar preferred intervals across tapping behaviors that varied in the number of produced intervals and the modality used to drive temporal processing. In addition, we found that the same population of neurons is able to multiplex the ordinal structure of a sequence of rhythmic movements and a wide range of durations in the range of hundreds of milliseconds. Our results also revealed a possible gain mechanism for encoding the total number of intervals in a sequence of temporalized movements, where interval-tuned cells show a multiplicative effect of their activity for longer sequences of intervals. These data suggest that MPC is part of a core timing network that uses interval tuning as a signal to represent temporal processing in a variety of behavioral contexts where time is explicitly quantified.
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Finding and Feeling the Musical Beat: Striatal Dissociations between Detection and Prediction of Regularity
Article
Full-text available
  • Apr 2012
  • CEREB CORTEX
Perception of temporal patterns is critical for speech, movement, and music. In the auditory domain, perception of a regular pulse, or beat, within a sequence of temporal intervals is associated with basal ganglia activity. Two alternative accounts of this striatal activity are possible: "searching" for temporal regularity in early stimulus processing stages or "prediction' of the timing of future tones after the beat is found (relying on continuation of an internally generated beat). To resolve between these accounts, we used functional magnetic resonance imaging (fMRI) to investigate different stages of beat perception. Participants heard a series of beat and nonbeat (irregular) monotone sequences. For each sequence, the preceding sequence provided a temporal beat context for the following sequence. Beat sequences were preceded by nonbeat sequences, requiring the beat to be found anew ("beat finding" condition), or by beat sequences with the same beat rate ("beat continuation"), or a different rate ("beat adjustment"). Detection of regularity is highest during beat finding, whereas generation and prediction are highest during beat continuation. We found the greatest striatal activity for beat continuation, less for beat adjustment, and the least for beat finding. Thus, the basal ganglia's response profile suggests a role in beat prediction, not in beat finding.
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Internalized Timing of Isochronous Sounds Is Represented in Neuromagnetic Beta Oscillations
Article
Full-text available
  • Feb 2012
  • J NEUROSCI
Moving in synchrony with an auditory rhythm requires predictive action based on neurodynamic representation of temporal information. Although it is known that a regular auditory rhythm can facilitate rhythmic movement, the neural mechanisms underlying this phenomenon remain poorly understood. In this experiment using human magnetoencephalography, 12 young healthy adults listened passively to an isochronous auditory rhythm without producing rhythmic movement. We hypothesized that the dynamics of neuromagnetic beta-band oscillations (~20 Hz)-which are known to reflect changes in an active status of sensorimotor functions-would show modulations in both power and phase-coherence related to the rate of the auditory rhythm across both auditory and motor systems. Despite the absence of an intention to move, modulation of beta amplitude as well as changes in cortico-cortical coherence followed the tempo of sound stimulation in auditory cortices and motor-related areas including the sensorimotor cortex, inferior-frontal gyrus, supplementary motor area, and the cerebellum. The time course of beta decrease after stimulus onset was consistent regardless of the rate or regularity of the stimulus, but the time course of the following beta rebound depended on the stimulus rate only in the regular stimulus conditions such that the beta amplitude reached its maximum just before the occurrence of the next sound. Our results suggest that the time course of beta modulation provides a mechanism for maintaining predictive timing, that beta oscillations reflect functional coordination between auditory and motor systems, and that coherence in beta oscillations dynamically configure the sensorimotor networks for auditory-motor coupling.
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Properties of the internal clock: First- and second-order principles of subjective time.
Article
  • Jan 2014
Humans share with other animals an ability to measure the passage of physical time and subjectively experience a sense of time passing. Subjective time has hallmark qualities, akin to other senses, which can be accounted for by formal, psychological, and neurobiological models of the internal clock. These include first-order principles, such as changes in clock speed and how temporal memories are stored, and second-order principles, including timescale invariance, multi-sensory integration, rhythmical structure, and attentional time-sharing. Within these principles there are both typical individual differences—influences of emotionality, thought speed, and psychoactive drugs—and atypical differences in individuals affected with certain clinical disorders (e.g., autism, Parkinson’s disease, and schizophrenia). This review summarizes recent behavioral and neurobiological findings and provides a theoretical framework for considering how changes in the properties of the internal clock impact time perception and other psychological domains.
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Canonical Microcircuits for Predictive Coding
Article
  • Nov 2012
This Perspective considers the influential notion of a canonical (cortical) microcircuit in light of recent theories about neuronal processing. Specifically, we conciliate quantitative studies of microcircuitry and the functional logic of neuronal computations. We revisit the established idea that message passing among hierarchical cortical areas implements a form of Bayesian inference-paying careful attention to the implications for intrinsic connections among neuronal populations. By deriving canonical forms for these computations, one can associate specific neuronal populations with specific computational roles. This analysis discloses a remarkable correspondence between the microcircuitry of the cortical column and the connectivity implied by predictive coding. Furthermore, it provides some intuitive insights into the functional asymmetries between feedforward and feedback connections and the characteristic frequencies over which they operate.
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Trial time warping to discriminate stimulus-related from movement-related neural activity
Article
  • Nov 2012
In tasks where different sensory, cognitive, and motor events are mixed in a sequence it is difficult to determine whether neural activity is related to any behavioral parameter. Here, we consider the case in which two alternative trial-alignment schemes correspond to two different neural representations, one stimulus-related and the other movement-related, using both simulations of neural activity and real recordings in the medial premotor areas during a multiple-interval tapping task called synchronization-continuation task (SCT). To discover whether neural responses are better aligned to sensory or motor events we introduce a family of trial-alignment time-warping functions indexed by a single parameter such that when the parameter takes the value 0 the trials are aligned to the stimulus and when the parameter takes the value 1 they are aligned to the movement. We then characterize neurons by the best-fitting alignment scheme (in the sense of maximum likelihood) under the assumption that the correct alignment would produce homogeneous trials without excess trial-to-trial variation. We use Bayes factors to determine the evidence in favor of sensory or motor neural alignments. The simulations revealed that the variability in neural responses and sequential motor outputs are key parameters to obtain appropriate warping results. In addition, the analysis on the activity of 500 neurons in the medial premotor areas of monkeys executing the SCT showed that most of the neural responses (54.2%) were aligned to the tapping movements instead of the stimuli used to drive the temporal behavior.
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