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The Persistence of Memory: How the Brain Encodes Time in Memory

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... There are potentially significant advantages of having an oscillatory time base composed of regularly repeating patterns of oscillation that are widely observed in the cortex and striatum. One is that such regulatory activity is an important aspect of sensory processing and interval timing that allows synchronization of information-processing in different brain areas, including the types of resource allocation underlying dynamic attending and working memory (e.g., Breska & Deouell, 2017;Cravo et al., 2013;Gu et al., 2015;Haegens & Golumbic, 2018;Henry & Herrmann, 2014;Herbst & Landau, 2016;Kösem et al., 2014;Meck & Benson, 2002;Teki et al. (2017) − but see Breska & Deouell, 2016 for an example of when synchronizing to distracting rhythms is detrimental to shifting attention, and van Ede et al., 2018 for a cautionary note on whether neural oscillations contained within certain frequency ranges are best viewed as sustained rhythms or transient burst events). These synchronized oscillations allow the time base to change in a systematic fashion as a function of time, thus proving additional temporal information in the repeated subsets (phase harmonics) of the oscillating time base. ...
... The EIO-SBF model has been successful in accounting for a variety of experimental findings including the observation that the cerebellum and the striatum represent core areas for representing temporal information in working memory (Teki et al., 2016(Teki et al., , 2017. In addition, multiple studies showed the increase of neural oscillations with interval timing (Emmons et al., 2016;Gu et al., 2015;Suzuki & Tanaka 2019). ...
... Excitatory/inhibitory oscillation models of temporal processing such as the EIO-SBF model developed by Gu and colleagues (Gu et al., 2015;Teki et al., 2017) provide an alternative solution for solving the unbounded accumulator problem. Unlike the original STT model, which postulates the accumulation of pacemaker pulses, multi-frequency EIO-based neurons oscillate over time, allowing a unique phase pattern to be observed at any given time (e.g., occurrence of a salient event). ...
Article
The major tenets of beat-frequency/coincidence-detection models of reward-related timing are reviewed in light of recent behavioral and neurobiological findings. This includes the emphasis on a core timing network embedded in the motor system that is comprised of a corticothalamic-basal ganglia circuit. Therein, a central hub provides timing pulses (i.e., predictive signals) to the entire brain, including a set of distributed satellite regions in the cerebellum, cortex, amygdala, and hippocampus that are selectively engaged in timing in a manner that is more dependent upon the specific sensory, behavioral, and contextual requirements of the task. Oscillation/coincidence-detection models also emphasize the importance of a tuned ‘perception’ learning and memory system whereby target durations are detected by striatal networks of medium spiny neurons (MSNs) through the coincidental activation of different neural populations, typically utilizing patterns of oscillatory input from the cortex and thalamus or derivations thereof (e.g., population coding) as a time base. The measure of success of beat-frequency/coincidence-detection accounts, such as the Striatal Beat-Frequency model of reward-related timing (SBF), is their ability to accommodate new experimental findings while maintaining their original framework, thereby making testable experimental predictions concerning diagnosis and treatment of issues related to a variety of dopamine-dependent basal ganglia disorders, including Huntington’s and Parkinson’s disease.
... A primary feature of episodic memory is the preservation of the order of events, also known as "chronological time" [1][2][3] (Figure 1e). While mental representation of chronological time preserves the temporal order in which life events occur, it does not itself contain precise information about the timing of events, or "metric time" [3][4][5] . Indeed, although the mental representation of time clearly is a crucial element of episodic, or autobiographical memory 4,[6][7][8] electrical neural activity (ramping) associated with temporal landmarks in the anterior-lateral entorhinal cortex ("LEC"; human analogue: alEC 10,11 ) in rats. ...
... Finally, 3) Chronological timeC3 reflects accuracy of recall for both Event orderC1 and Episode orderC2 (Figure 1e). Importantly, the experimental paradigm described here affords exploration of all aspects of temporal representation within the context of episodic memories, in contrast to previous studies which limited the analyses to one, or a few, temporal measures 3,5,[12][13][14][15][22][23][24] . Table S1), while for Metric timeM2 (between all episodes) the two distributions were not significantly different ( Figure 2 lower panel, Figure S2c, Table S1). ...
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The relative contributions of metric and chronological time in the encoding of episodic memories are unknown. One hundred one healthy young adults viewed 48 unique episodes of visual events and were later tested on recall of the order of events (chronological time) and the precise timing of events (metric time). The behavioral results show that metric recall accuracy correlates with chronological accuracy for events within episodes, but does not play a role on larger time-scales across episodes. Functional magnetic resonance imaging during encoding and recall showed that metric time was represented in the posterior medial entorhinal cortex, as well as the temporal pole and the cerebellum, whereas chronological time was represented in a widespread brain network including the anterior lateral entorhinal cortex, hippocampus, parahippocampal cortex and the prefrontal cortex. We conclude that metric time has a role in episodic memory on short time-scales and is mainly subserved by medial temporal lobe structures.
... Yet, lesion research has shown that the hippocampus is not critical for processing temporal duration information: Damage to this structure, both in humans and rodents, leaves intact the ability to estimate time elapsed, at least on the order of seconds (e.g., Palombo et al., 2016;Jacobs et al., 2013; also see Palombo & Verfaellie, 2017, for a review of the literature). Our data may help to reconcile these seemingly contradictory findings by suggesting that, whereas the hippocampus codes for elapsed time (likely through connections with other cortical and subcortical structures that show similar time cell patterns; Tiganj et al., 2018;Teki, Gu, & Meck, 2017;Barnett et al., 2014;Jin, Fujii, & Graybiel, 2009), it does so in the service of supporting higher order aspects of cognition, namely, for sequential processing (Palombo & Verfaellie, 2017), or as Buzsáki and Tingley (2018) state, the hippocampus is a "sequence generator." That is, the hippocampus uses duration information (coded by time cells) to represent the temporal relationships between successive microevents that form a sequence. ...
... Other recent work, both in humans and animals (Bellmund, Deuker, & Doeller, 2019a, 2019bMontchal, Reagh, & Yassa, 2019;Thavabalasingam et al., 2019;Tsao et al., 2018;Teki et al., 2017) highlights the importance of the entorhinal cortex, particularly the lateral portion (but see Robinson et al., 2017), in coding temporal information during events. Our data cannot speak to the putative contributions of the hippocampus versus entorhinal cortex to temporal sequential processing in this study, as many of our patients have damage to both structures, although the fact that a selective impairment in the sequence condition was also present in the patients with damage restricted to the hippocampus suggests that not only entorhinal cortex but also the hippocampus is critical for processing the duration of temporal sequences. ...
Article
Recent interest in the role of the hippocampus in temporal aspects of cognition has been fueled, in part, by the observation of “time” cells in the rodent hippocampus—that is, cells that have differential firing patterns depending on how long ago an event occurred. Such cells are thought to provide an internal representation of elapsed time. Yet, the hippocampus is not needed for processing temporal duration information per se, at least on the order of seconds, as evidenced by intact duration judgments in rodents and humans with hippocampal damage. Rather, it has been proposed that the hippocampus may be essential for coding higher order aspects of temporal mnemonic processing, such as those needed to temporally organize a sequence of events that form an episode. To examine whether (1) the hippocampus uses duration information in the service of establishing temporal relations among events and (2) its role in memory for duration is unique to sequences, we tested amnesic patients with medial-temporal lobe damage (including the hippocampus). We hypothesized that medial-temporal lobe damage should impair the ability to remember sequential duration information but leave intact judgments about duration devoid of a sequential demand. We found that amnesics were impaired in making judgments about durations within a sequence but not in judging single durations. This impairment was not due to higher cognitive load associated with duration judgments about sequences. In convergence with rodent and human fMRI work, these findings shed light on how time coding in the hippocampus may contribute to temporal cognition.
... Although there is wide consensus that cerebellar structures and prefrontal-striatal-hippocampal networks play a role, different proposals suggest different divisions of labor among these. In particular, the relationship between processing and remembering of absolute durations, relative order, and the relation to a regular isochronous beat has given rise to different hypothetical models [29][30][31][32]. Although the details of these models are under debate, they provide a starting point for understanding the neural implementation of a time-based context signal, as proposed in the most recent formulations of the phonological loop [33]. ...
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The ability to accurately repeat meaningless nonwords or lists of spoken digits in correct order have been associated with vocabulary acquisition in both first and second language. Individual differences in these tasks are thought to depend on the phonological loop component of working memory. However, phonological working memory may itself depend on more elementary processes. We asked whether auditory non-verbal short-term memory (STM) for patterns in time supports immediate recall of speech-based sequences. Participants tapped temporal sequences consisting of short and long beeps and repeated nonsense sentences sounding like their native language or an unfamiliar language. As a language learning task, they also memorized familiar-word–foreign-word pairs. Word learning was directly predicted by nonsense sentence repetition accuracy. It was also predicted by temporal pattern STM. However, this association was mediated by performance on the repetition measure. We propose that STM for temporal patterns may reflect a component skill that provides the context signal necessary to encode order in phonological STM. It would be needed to support representation of the prosodic profile of language material, which allows syllables in words and words in sentences to be ordered and temporally grouped for short-term representation and long-term learning.
... Because the origins of LFPs and neural oscillations are controversial (Baranauskas et al. 2012;Buzsaki et al. 2012;Wang 2010), it is somewhat difficult to connect our LFP measurements to the SBF model's predictions for individual neurons. However, a recently proposed EIO model, which extends the SBF model to consider the population pattern of coupled oscillatory inputs to neurons -including both excitatory and inhibitory inputs -proposes that the underlying mechanism(s) supporting the neural oscillations observed in the current study are related to the timing processes engaged by the ordinal-comparison task used here (Gu et al., 2015;Teki et al., 2017). Although exact relations between individual cell firing and population activity have to be shown to prove the details of EIO model, at least the arise of theta and delta rhythm as well as the theta phase resetting with a timing onset follows the exact prediction of EIO model. ...
Article
Ordinal comparison of successively presented signal durations requires a) the encoding of the first signal duration (standard), b) maintenance of temporal information specific to the standard duration in memory, and c) timing of the second signal duration (comparison) during which a comparison is made of the first and second durations. Rats were first trained to make ordinal comparisons of signal durations within three time ranges using 0.5, 1.0, and 3.0-s standard durations. Local field potentials were then recorded from the dorsal striatum and sensorimotor cortex in order to investigate the pattern of neural oscillations during each phase of the ordinal comparison process. Increased power in delta and theta frequency ranges was observed during both the encoding and comparison stages. Active maintenance of a selected response, “shorter” or “longer” (counter-balanced across left and right levers), was represented by an increase of theta and delta oscillations in the contralateral striatum and cortex. Taken together, these data suggest that neural oscillations in the delta-theta range play an important role in the encoding and comparison processes of durations in ordinal comparisons. Special Issue on ‘Time and Memory’ dedicated to Howard Eichenbaum.
... The interaction between time perception and memory has recently gained increasing interest in cognitive neuroscience (for reviews, see Matthews & Meck; Teki et al., 2017, Van Rijn, 2016. When something in the environment happens regularly, it can be very helpful to use this regularity to not only predict what will happen, but also when it will happen. ...
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The attentional blink (AB) reflects a temporal restriction of selective attention and is generally regarded as a very robust phenomenon. However, previous studies have found large individual differences in AB performance, and under some training conditions the AB can be reduced significantly. One factor that may account for individual differences in AB magnitude is the ability to accurately time attention. In the current study, we focus on the sensitivity for temporal information on the ability to control attention. Following a visual AB task, a time estimation task was presented in either the visual or auditory modality, followed by another visual AB task. It was found that the time estimation training in both the auditory and visual modality reduced AB magnitude. Although a reduction in AB magnitude was also observed when individuals were trained on a control task (either an auditory frequency or visual line length estimation task), the effect was significantly larger following the time estimation tasks. In addition, it was found that individuals who showed most improvement on the visual time estimation task, also showed the largest reduction in AB magnitude, which was not the case for individuals who were trained on the control tasks. Finally, a negative correlation was observed between depression scores (tested by Beck Depression Inventory-Short Form (BDI-SF) scores and the improvement in the AB and time estimation tasks. Our findings demonstrate clear links between timing ability and mechanisms to control attention and emotion.
... Besides that, some researchers point out the effect of a task and its processing on remembered duration (Hicks et al., 1976;McClain, 1983;Block and Zakay, 1997;Cohn-Sheehy and Ranganath, 2017;Teki et al., 2017) and consider that, in the retrospective timing, the judgment is based on a cognitive reconstruction of the task duration (Block, 1978). Prior to these studies, Ornstein (1969) proposed the theory of storage, suggesting that a complex task requires larger cognitive demand resulting in larger "storage size" in the memory, which would lengthen the remembered duration. ...
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Objectives: In artwork appreciation situations, individuals often show altered time perception. We tested the hypothesis that Parkinson’s disease (PD) patients present movement patterns that have an impact on the time perception of artwork manipulation time. We predicted that, compared to healthy controls (non-PD), differences in the exploratory behavior of patients would evoke alteration of artwork manipulation time perception. Methods: Ten PD patients and 10 non-PD participants manipulated two reproductions of artwork with different complexity levels from the series “Bichos” by Lygia Clark. Subsequently, participants performed a verbal estimation regarding the temporal duration of their manipulations. The exploratory behavior was analyzed. Results: All participants overestimated the artwork manipulation time. However, PD patients, regardless of the artwork’s level of complexity, showed shorter manipulation time and minor time overestimation compared to the non-PD participants. PD patients touched the artworks more often, especially the more complex artworks, than the non-PD participants; in contrast, PD patients moved the artworks less often, particularly the less complex artwork. Conclusion: PD patients showed an altered perception of artwork manipulation time. This suggests that exploratory behavior influenced temporal estimation. Besides, it is likely that PD patients had presented a decreased ability to manage attention during the task, which interfered in the cognitive reconstruction of its duration. Considered altogether, these appointments indicate that, as a result of cognitive and motor deficits, PD patients showed impairment in temporal information processing. The exploratory behavior facilitated the understanding of these results and processes in terms of motor-timing operations of the basal ganglia-thalamocortical system.
... It is reasonable to view interval timing sequence as an additional modality of sequential memory and to model it by a binding network. The generalization of a striatal beat model of interval timing shows how memories for multiple time intervals are represented by neural dynamics and can also be used to explain the mechanisms of resource allocation in the working memory [144]. ...
Article
Today, based on brain imaging analyses, we can consider the brilliant metaphor about event discreteness of the conscious process by William James (1890) to be an experimental fact. Such events compose sequences: linguistic, episodic memory, motor behavior, etc., whose dynamics are robust, reproducible, and sensitively react to incoming informational signals. The human mind is able to process, understand and predict time-dependent information about the environment and about ourselves, and generate corresponding commands to control behavior. Many experiments have indicated that the mind relies on sequential dynamics to carry out these tasks. Based on brain imaging experiments, we discuss here a set of key principles and their instantiation in nonlinear differential equations to form a dynamical theory of consciousness and creativity. General hierarchical models of consciousness and creativity include coupled low-dimensional equations that govern cooperative variables for several cognitive modalities: episodic (semantic) memory, working memory, attention, emotion, perception and their sequential interaction. In the phase spaces spanned by variables of these models, the joint transient dynamics of cognitive modalities is represented by coupled heteroclinic networks which share complex metastable states. The interaction of such states is responsible for the robustness of transient neural dynamics involved in the generation of thoughts and in the programming of behavior. In the framework of the analyzed dynamical models, we discuss the interaction of cognitive processes and the generation of new information in creativity.
... Time is inherent to this construct as the serial input is only stored for a short time before memory decays. However, it is still largely unknown how the temporal structure of the serial input itself factors into working memory (Teki, Gu, & Meck, 2017). The rate (tempo) of the input changes the storage time for input items prior to the recall and the time that is available to employ recall strategies, with some indications for higher performance at relatively fast rates with fixed recall order as opposed to higher performance at slower rates with reversed recall order (Posner, 1964) but also generally higher performance at slower rates (Laughery & Pinkus, 1966). ...
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The informative value of time and temporal structure often remains neglected in cognitive assessments. However, next to information about stimulus identity we can exploit temporal ordering principles, such as regularity, periodicity, or grouping to generate predictions about the timing of future events. Such predictions may improve cognitive performance by optimising adaptation to dynamic stimuli. Here, we investigated the influence of temporal structure on verbal working memory by assessing immediate recall performance for aurally presented digit sequences (forward digit span) as a function of standard (1000 ms stimulus‐onset‐asynchronies, SOAs), short (700 ms), long (1300 ms) and mixed (700–1300 ms) stimulus timing during the presentation phase. Participant's digit spans were lower for short and mixed SOA presentation relative to standard SOAs. This confirms an impact of temporal structure on the classic “magical number seven,” suggesting that working memory performance can in part be regulated through the systematic application of temporal ordering principles.
... Interestingly, although virtually all timing models make an attempt to explain how time is measured and utilized (see Matell and Meck, 2000;Hass and Durstewitz, 2016;Matthews and Meck, 2016) few of them provide specific details for how target durations are encoded and decoded within the proposed neural circuitry (Merchant and de Lafuente, 2014). This means that the form and content of temporal memory, or whether it is written and read at a single-cell level or across a distributed network is typically left unaddressed (Meck, 1983(Meck, , 2002Teki et al., 2017;Paton and Buonomano, 2018). ...
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The majority of studies in the field of timing and time perception have generally focused on sub- and supra-second time scales, specific behavioral processes, and/or discrete neuronal circuits. In an attempt to find common elements of interval timing from a broader perspective, we review the literature and highlight the need for cell and molecular studies that can delineate the neural mechanisms underlying temporal processing. Moreover, given the recent attention to the function of microtubule proteins and their potential contributions to learning and memory consolidation/re-consolidation, we propose that these proteins play key roles in coding temporal information in cerebellar Purkinje cells (PCs) and striatal medium spiny neurons (MSNs). The presence of microtubules at relevant neuronal sites, as well as their adaptability, dynamic structure, and longevity, makes them a suitable candidate for neural plasticity at both intra- and inter-cellular levels. As a consequence, microtubules appear capable of maintaining a temporal code or engram and thereby regulate the firing patterns of PCs and MSNs known to be involved in interval timing. This proposed mechanism would control the storage of temporal information triggered by postsynaptic activation of mGluR7. This, in turn, leads to alterations in microtubule dynamics through a “read-write” memory process involving alterations in microtubule dynamics and their hexagonal lattice structures involved in the molecular basis of temporal memory.
... Por último, los estudios más recientes han localizado actividad neuronal desencadenada por el cambio de plano en el hipocampo a partir de resonancias magnéticas (Ben-Yakov y Henson, 2018) y desde el electroencefalograma han localizado el modelo de respuesta N-400, relacionado con la codificación del lenguaje y procesos de memoria hipocampo (Silva, 2018). Estos últimos hallazgos resultan de gran importancia en el debate sobre la existencia o no de un lenguaje cinematográfico ya que el hipocampo está directamente relacionado con los procesos de decodificación y codificación de nueva información (Teki, Gu y Meck, 2017) y también es responsable de la percepción temporal (Eichenbaum, 2017;Eichenbaum, 2014) y espacial (Shirvalkar, Rapp y Shapiro, 2010;Howard y Eichenbaum, 2015). La aparición del N-400 en los análisis electroencefalográficos concretamente se relaciona con la memoria semántica (Federmeier y Kutas, 2001) y con la comprensión del lenguaje hablado (Van Petten, Rubin y Parks, 2000) y escrito . ...
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Precise timing is crucial for many behaviors ranging from street crossing, conversational speech, to athletic performance. The precision of motor timing has been suggested to result from the strength of phase-amplitude coupling (PAC) between the phase of alpha oscillations (α, 8-12 Hz) and the power of beta activity (β, 14-30 Hz), herein referred to as α-β PAC. The amplitude of β oscillations has been proposed to code for temporally relevant information, and the locking of β power to the phase of α oscillations to maintain timing precision. Motor timing precision has at least two sources of variability: variability of timekeeping mechanism and variability of motor control. There is ambiguity to with of these two factors α-β PAC could be ascribed to. Whether α-β PAC indexes precision of internal timekeeping mechanisms like a stopwatch, or α-β PAC indexes motor control precision is unclear. To disentangle these two hypotheses, we tested how oscillatory coupling at different stages of time reproduction related to temporal precision. Human participants perceived, and subsequently reproduced, a time interval while magnetoencephalography was recorded. The data show a robust α-β PAC during both the encoding and the reproduction of a temporal interval, a pattern which could not be predicted for by the motor control account. Specifically, we found that timing precision resulted from the tradeoff between the strength of α-β PAC during the encoding and during the reproduction of intervals. We interpret these results as supporting evidence for the hypothesis that α-β PAC codes for precision of temporal representations in the human brain. Highlights - Encoding and reproducing temporal intervals implicate α-β PAC. - α-β PAC does not represent solely motor control. - α-β PAC maintains the precision of temporal representations.
Article
Durations are defined by a beginning and an end, and a major distinction is drawn between durations that start in the present and end in the future (‘prospective timing’) and durations that start in the past and end either in the past or the present (‘retrospective timing’). Different psychological processes are thought to be engaged in each of these cases. The former is thought to engage a clock-like mechanism that accurately tracks the continuing passage of time, whereas the latter is thought to engage a reconstructive process that utilizes both temporal and non-temporal information from the memory of past events. We propose that, from a biological perspective, these two forms of duration ‘estimation’ are supported by computational processes that are both reliant on population state dynamics but are nevertheless distinct. Prospective timing is effectively carried out in a single step where the ongoing dynamics of population activity directly serve as the computation of duration, whereas retrospective timing is carried out in two steps: the initial generation of population state dynamics through the process of event segmentation and the subsequent computation of duration utilizing the memory of those dynamics. One major form of timing is the estimation of duration. In this Review, Tsao et al. describe the neural bases for estimating ongoing durations and those for estimating durations between past events within memory.
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Many aspects of human behavior are inherently rhythmic, requiring production of rhythmic motor actions as well as synchronizing to rhythms in the environment. It is well-established that individuals with ADHD exhibit deficits in temporal estimation and timing functions, which may impact their ability to accurately produce and interact with rhythmic stimuli. In the current study we seek to understand the specific aspects of rhythmic behavior that are implicated in ADHD. We specifically ask whether they are attributed to imprecision in the internal generation of rhythms or to reduced acuity in rhythm perception. We also test key predictions of the Preferred Period Hypothesis, which suggests that both perceptual and motor rhythmic behaviors are biased towards a specific personal default tempo. To this end, we tested a several aspects of rhythmic behavior, including spontaneous motor tapping (SMT), perceptual preferences (PPT) and synchronization-continuations tapping in a broad range of rhythms, from sub-second to supra-second rates. Moreover, we evaluate the intra-subject consistency of rhythmic preferences, as a means for testing the reality and reliability of personal default-rhythms. Results indicate that individuals with ADHD are primarily challenged in producing self-generating isochronous motor rhythms, during both spontaneous and memory-paced tapping. However, they nonetheless exhibit a high degree of flexibility in synchronizing to a broad range of external rhythms. These findings suggest that auditory-motor entrainment is preserved in ADHD, and that the presence of an external pacer allows overcoming the inherent difficulty in self-generating isochronous motor rhythms. Interestingly, we find no advantage for performance near so-called default motor or perceptual rhythms, in either ADHD or control groups, as was suggested by the Preferred Period Hypothesis. Moreover, participants in both groups displayed large variability in their SMTs and PPTs across session, raising questions regarding the extent to which all individuals indeed have specific motor and perceptual preferences. Therefore, alongside the insights into the nature of rhythmic deficits in ADHD, this study also challenges some assumptions made previously regarding the prevalence and functional role of default rhythmic preferences in facilitating rhythmic behavior more broadly.
Article
Many aspects of human behavior are inherently rhythmic, requiring production of rhythmic motor actions as well as synchronizing to rhythms in the environment. It is well-established that individuals with ADHD exhibit deficits in temporal estimation and timing functions, which may impact their ability to accurately produce and interact with rhythmic stimuli. In the current study we seek to understand the specific aspects of rhythmic behavior that are implicated in ADHD. We specifically ask whether they are attributed to imprecision in the internal generation of rhythms or to reduced acuity in rhythm perception. We also test key predictions of the Preferred Period Hypothesis, which suggests that both perceptual and motor rhythmic behaviors are biased towards a specific personal ‘default’ tempo. To this end, we tested several aspects of rhythmic behavior and the correspondence between them, including spontaneous motor tempo (SMT), preferred auditory perceptual tempo (PPT) and synchronization-continuations tapping in a broad range of rhythms, from sub-second to supra-second intervals. Moreover, we evaluate the intra-subject consistency of rhythmic preferences, as a means for testing the reality and reliability of personal ‘default-rhythms’. We used a modified operational definition for assessing SMT and PPT, instructing participants to tap or calibrate the rhythms most comfortable for them to count along with, to avoid subjective interpretations of the task. Our results shed new light on the specific aspect of rhythmic deficits implicated in ADHD adults. We find that individuals with ADHD are primarily challenged in producing and maintaining isochronous self-generated motor rhythms, during both spontaneous and memory-paced tapping. However, they nonetheless exhibit good flexibility for synchronizing to a broad range of external rhythms, suggesting that auditory-motor entrainment for simple rhythms is preserved in ADHD, and that the presence of an external pacer allows overcoming their inherent difficulty in self-generating isochronous motor rhythms. In addition, both groups showed optimal memory-paced tapping for rhythms near their ‘counting-based’ SMT and PPT, which were slightly faster in the ADHD group. This is in line with the predictions of the Preferred Period Hypothesis, indicating that at least for this well-defined rhythmic behavior (i.e., counting), individuals tend to prefer similar time-scales in both motor production and perceptual evaluation.
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Humans have a near-automatic tendency to entrain their motor actions to rhythms in the environment. Entrainment is hypothesized to play an important role in processing naturalistic stimuli, such as speech and music, which have intrinsically rhythmic properties. Here we studied two facets of entraining one's rhythmic motor actions to an external stimulus: (1) synchronized finger tapping to auditory rhythmic stimuli, and (2) memory-paced reproduction of a previously heard rhythm. Using modifications of the Synchronization-Continuation tapping paradigm, we studied how these two rhythmic behaviours were affected by different stimulus and task features. We tested synchronization and memory-paced tapping for a broad range of rates, from sub-second to supra-second, both for isochronous tone-sequences and for rhythmic speech stimuli (counting from one to ten), which are more ecological yet less strictly isochronous. We also asked what role motor engagement plays in forming a stable internal representation for rhythms and guiding memory-paced tapping. Results show that individuals can flexibly synchronize their motor actions to a very broad range of rhythms. However, this flexibility does not extend to memory-paced tapping, which is accurate only in a narrower range of rates, around ~1.5Hz. This pattern suggests that intrinsic rhythmic-defaults in the auditory/motor systems influence the internal representation of rhythms, in the absence of an external pace-maker. Interestingly, memory-paced tapping for speech rhythms and simple tones shared similar 'optimal rates', although with reduced accuracy, suggesting that internal constraints on rhythmic entrainment may generalize to more ecological stimuli. Last, active synchronization led to more accurate memory-paced tapping vs. passive listening, which emphasizes the importance of action-perception interactions in forming stable entrainment to external rhythms.
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In order to analyze and detect neural activations and inhibitions in film spectators to shot changes by cut in films, we developed a methodology based on comparisons of recorded EEG signals and analyzed the event-related desynchronization/synchronization (ERD/ ERS). The aim of the research is isolating these neuronal responses from other visual and auditory features that covary with film editing. This system of comparing pairs of signals using permutation tests, the Spearman correlation, and slope analysis is implemented in an automated way through sliding windows, analyzing all the registered electrodes signals at all the frequency bands defined. Through this methodology, we are able to locate, identify, and quantify the variations in neuronal rhythms in specific cortical areas and frequency ranges with temporal precision. Our results detected that after a cut there is a synchronization in theta rhythms during the first 188 ms with left lateralization, and also a desynchroniza-tion between 250 ms and 750 ms in the delta frequency band. The cortical area where most of these neuronal responses are detected in both cases is the parietal area.
Article
Purpose Humans have a near-automatic tendency to entrain their motor actions to rhythms in the environment. Entrainment has been hypothesized to play an important role in processing naturalistic stimuli, such as speech and music, which have intrinsically rhythmic properties. Here, we studied two facets of entraining one's rhythmic motor actions to an external stimulus: (a) synchronized finger tapping to auditory rhythmic stimuli and (b) memory-paced reproduction of a previously heard rhythm. Method Using modifications of the Synchronization–Continuation tapping paradigm, we studied how these two rhythmic behaviors were affected by different stimulus and task features. We tested synchronization and memory-paced tapping for a broad range of rates, from stimulus onset asynchrony of subsecond to suprasecond, both for strictly isochronous tone sequences and for rhythmic speech stimuli (counting from 1 to 10), which are more ecological yet less isochronous. We also asked what role motor engagement plays in forming a stable internal representation for rhythms and guiding memory-paced tapping. Results and Conclusions Our results show that individuals can flexibly synchronize their motor actions to a very broad range of rhythms. However, this flexibility does not extend to memory-paced tapping, which is accurate only in a narrower range of rates, around ~1.5 Hz. This pattern suggests that intrinsic rhythmic defaults in the auditory and/or motor system influence the internal representation of rhythms, in the absence of an external pacemaker. Interestingly, memory-paced tapping for speech rhythms and simple tone sequences shared similar “optimal rates,” although with reduced accuracy, suggesting that internal constraints on rhythmic entrainment generalize to more ecological stimuli. Last, we found that actively synchronizing to tones versus passively listening to them led to more accurate memory-paced tapping performance, which emphasizes the importance of action–perception interactions in forming stable entrainment to external rhythms.
Chapter
This chapter reviews recent human and nonhuman animal studies investigating neural signatures of time estimation. Investigation of the neural correlates of time estimation as measured by electrophysiology, electroencephalography, magnetoencephalography, and functional magnetic resonance imaging (fMRI) in humans and other animals has largely been focused on the to‐be‐timed period. Climbing neural activity (e.g., ramping) originating from the supplementary motor area has been implicated as a primary neural marker that coincides with the development of subjective experience of duration. However, it has recently been questioned whether such climbing neural activity directly reflects the neural mechanism(s) underpinning the sense of time. Given that the neural signatures recorded during the to‐be‐timed period are insufficient to explain various aspects of interval timing, this has led to the consideration of processes influencing timing before and after the to‐be‐timed period. Because many of these signatures are linked with the supplementary motor area, an extended discussion of the role of this cortical structure in timing and time perception is provided. These neural correlates are interpreted in light of contemporary theories of interval timing, such as the striatal beat frequency model. Future directions for the investigation of the functional and neural mechanisms of interval timing are also discussed.
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Space and time appear to play key roles in the way that information is organized in short-term memory (STM). Some argue that they are crucial contexts within which other stored features are embedded, allowing binding of information that belongs together within STM. Here we review recent behavioral, neurophysiological and imaging studies that have sought to investigate the nature of spatial, sequential and duration representations in STM, and how these might break down in disease. Findings from these studies point to an important role of the hippocampus and other medial temporal lobe structures in aspects of STM, challenging conventional accounts of involvement of these regions in only long-term memory.
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When a sequence is held in working memory, different items are retained with differing fidelity. Here we ask whether a sequence of brief time intervals that must be remembered show recency effects, similar to those observed in verbal and visuospatial working memory. It has been suggested that prioritizing some items over others can be accounted for by a “focus of attention,” maintaining some items in a privileged state. We therefore also investigated whether such benefits are vulnerable to disruption by attention or expectation. Participants listened to sequences of one to five tones, of varying durations (200 ms to 2 s). Subsequently, the length of one of the tones in the sequence had to be reproduced by holding a key. The discrepancy between the reproduced and actual durations quantified the fidelity of memory for auditory durations. Recall precision decreased with the number of items that had to be remembered, and was better for the first and last items of sequences, in line with set-size and serial position effects seen in other modalities. To test whether attentional filtering demands might impair performance, an irrelevant variation in pitch was introduced in some blocks of trials. In those blocks, memory precision was worse for sequences that consisted of only one item, i.e., the smallest memory set-size. Thus, when irrelevant information was present, the benefit of having only one item in memory is attenuated. Finally we examined whether expectation could interfere with memory. On half the trials, the number of items in the upcoming sequence was cued. When the number of items was known in advance, performance was paradoxically worse when the sequence consisted of only one item. Thus the benefit of having only one item to remember is stronger when it is unexpectedly the only item. Our results suggest that similar mechanisms are used to hold auditory time durations in working memory, as for visual or verbal stimuli. Further, solitary items were remembered better when more items were expected, but worse when irrelevant features were present. This suggests that the “privileged” state of one item in memory is particularly volatile and susceptible to interference.
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The capacity of serially-ordered auditory-verbal short-term memory (AVSTM) is sensitive to the timing of the material to be stored, and both temporal processing and AVSTM capacity are implicated in the development of language. We developed a novel ?rehearsal-probe? task to investigate the relationship between temporal precision and the capacity to remember serial order. Participants listened to a sub-span sequence of spoken digits and silently rehearsed the items and their timing during an unfilled retention interval. After an unpredictable delay, a tone prompted report of the item being rehearsed at that moment. An initial experiment showed cyclic distributions of item responses over time, with peaks preserving serial order and broad, overlapping tails. The spread of the response distributions increased with additional memory load and correlated negatively with participants? auditory digit spans. A second study replicated the negative correlation and demonstrated its specificity to AVSTM by controlling for differences in visuo-spatial STM and nonverbal IQ. The results are consistent with the idea that a common resource underpins both the temporal precision and capacity of AVSTM. The rehearsal-probe task may provide a valuable tool for investigating links between temporal processing and AVSTM capacity in the context of speech and language abilities. PQJE_1239749_supplemental_material.docx
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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.
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This chapter reviews recent human and non-human animal studies investigating neural signatures of time estimation. Investigation of the neural correlates of time estimation as measured by electrophysiology, electroencephalography, magnetoencephalography, and functional magnetic resonance imaging in humans and other animals has largely been focused on the to-be-timed period. Climbing neural activity originating from the supplementary motor area has been implicated as a primary neural marker that coincides with the development of subjective experience of duration. However, it has recently been questioned whether such climbing neural activity directly reflects the neural mechanism(s) underpinning the sense of time. Given that the neural signatures recorded during the to-be-timed period are insufficient to explain various aspects of interval timing, this has led to the consideration of processes influencing timing before and after to-be-timed period. As many of these signatures are linked with the supplementary motor area, an extended discussion of the role of the cortical structure in timing and time perception is provided. The neural correlates are interpreted in light of contemporary models of interval timing, such as the striatal beat-frequency model. Future directions for the investigation of the functional and neural mechanisms of interval timing are also discussed.
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Perception of auditory time intervals is critical for accurate comprehension of natural sounds like speech and music. However, the neural substrates and mechanisms underlying the representation of time intervals in working memory are poorly understood. In this study, we investigate the brain bases of working memory for time intervals in rhythmic sequences using functional magnetic resonance imaging. We used a novel behavioral paradigm to investigate time-interval representation in working memory as a function of the temporal jitter and memory load of the sequences containing those time intervals. Human participants were presented with a sequence of intervals and required to reproduce the duration of a particular probed interval. We found that perceptual timing areas including the cerebellum and the striatum were more or less active as a function of increasing and decreasing jitter of the intervals held in working memory respectively whilst the activity of the inferior parietal cortex is modulated as a function of memory load. Additionally, we also analyzed structural correlations between gray and white matter density and behavior and found significant correlations in the cerebellum and the striatum, mirroring the functional results. Our data demonstrate neural substrates of working memory for time intervals and suggest that the cerebellum and the striatum represent core areas for representing temporal information in working memory.
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Organizing movements in time is a critical and highly conserved feature of mammalian behavior. Temporal control of action requires corticostriatal networks. We investigate these networks in rodents using a two-interval timing task while recording LFPs in medial frontal cortex (MFC) or dorsomedial striatum. Consistent with prior work, we found cue-triggered delta (1-4 Hz) and theta activity (4-8 Hz) primarily in rodent MFC. We observed delta activity across temporal intervals in MFC and dorsomedial striatum. Rewarded responses were associated with increased delta activity in MFC. Activity in theta bands in MFC and delta bands in the striatum was linked with the timing of responses. These data suggest both delta and theta activity in frontostriatal networks are modulated during interval timing and that activity in these bands may be involved in the temporal control of action.
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Time is a universal psychological dimension, but time perception has often been studied and discussed in relative isolation. Increasingly, researchers are searching for unifying principles and integrated models that link time perception to other domains. In this review, we survey the links between temporal cognition and other psychological processes. Specifically, we describe how subjective duration is affected by non-temporal stimulus properties (perception), the allocation of processing resources (attention), and past experience with the stimulus (memory). We show that many of these connections instantiate a ‘processing principle’, according to which perceived time is positively related to perceptual vividity and the ease of information-extraction from the stimulus. This empirical generalization generates testable predictions and provides a starting-point for the development of integrated theoretical frameworks. Our intention is that, by outlining some of the links between temporal cognition and other domains, researchers in the field of timing and time perception will be encouraged to situate their work within broader theoretical frameworks, whilst researchers from other fields will be inspired to apply their insights, techniques, and theorizing to improve our understanding of the representation and judgment of time
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Cognitive processes such as decision-making, rate calculation and planning require an accurate estimation of durations in the supra-second range—interval timing. In addition to being accurate, interval timing is scale invariant: the time-estimation errors are proportional to the estimated duration.The origin and mechanisms of this fundamental property are unknown. We discuss the computational properties of a circuit consisting of a large number of (input) neural oscillators projecting on a small number of (output) coincidence detector neurons, which allows time to be coded by the pattern of coincidental activation of its inputs. We showed analytically and checked numerically that time-scale invariance emerges from the neural noise. In particular, we found that errors or noise during storing or retrieving information regarding the memorized criterion time produce symmetric, Gaussian-like output whose width increases linearly with the criterion time. In contrast, frequency variability produces an asymmetric, long-tailed Gaussian-like output, that also obeys scale invariant property. In this architecture, time-scale invariance depends neither on the details of the input population, nor on the distribution probability of noise.
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Unlabelled: Time is central to cognition. However, the neural basis for time-dependent cognition remains poorly understood. We explore how the temporal features of neural activity in cortical circuits and their capacity for plasticity can contribute to time-dependent cognition over short time scales. This neural activity is linked to cognition that operates in the present or anticipates events or stimuli in the near future. We focus on deliberation and planning in the context of decision making as a cognitive process that integrates information across time. We progress to consider how temporal expectations of the future modulate perception. We propose that understanding the neural basis for how the brain tells time and operates in time will be necessary to develop general models of cognition. Significance statement: Time is central to cognition. However, the neural basis for time-dependent cognition remains poorly understood. We explore how the temporal features of neural activity in cortical circuits and their capacity for plasticity can contribute to time-dependent cognition over short time scales. We propose that understanding the neural basis for how the brain tells time and operates in time will be necessary to develop general models of cognition.
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Recent work shows that putamen-originating beta power oscillations serve as a carrier for temporal information during tapping tasks, with higher beta power associated with longer temporal reproductions. However, given the nature of tapping tasks, it is difficult to determine whether beta power dynamics observed in these tasks are linked to the generation or execution of motor programs or to the internal representation of time. To assess whether recent findings in animals generalize to human studies we reanalyzed existing EEG data of participants who estimated a 2.5 s time interval with self-paced onset and offset keypresses. The results showed that the trial-to-trial beta power measured after the onset predicts the produced duration, such that higher beta power indexes longer produced durations. Moreover, although beta power measured before the first key-press also influenced the estimated interval, it did so independently from post-first-keypress beta power. These results suggest that initial motor inhibition plays an important role in interval production, and that this inhibition can be interpreted as a biased starting point of the decision processes involved in time estimation. Copyright © 2015. Published by Elsevier Ltd.
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This work considers bases for working memory for non-verbal sounds. Specifically we address whether sounds are represented as integrated objects or individual features in auditory working memory and whether the representational format influences WM capacity. The experiments used sounds in which two different stimulus features, spectral passband and temporal amplitude modulation rate, could be combined to produce different auditory objects. Participants had to memorize sequences of auditory objects of variable length (1-4 items). They either maintained sequences of whole objects or sequences of individual features until recall for one of the items was tested. Memory recall was more accurate when the objects had to be maintained as a whole compared to the individual features alone. This is due to interference between features of the same object. Additionally a feature extraction cost was associated with maintenance and recall of individual features, when extracted from bound object representations. An interpretation of our findings is that, at some stage of processing, sounds might be stored as objects in WM with features bound into coherent wholes. The results have implications for feature-integration theory in the context of WM in the auditory system.
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Abstract Memory for speech sounds is a key component of models of verbal working memory (WM). But how good is verbal WM? Most investigations assess this using binary report measures to derive a fixed number of items that can be stored. However, recent findings in visual WM have challenged such 'quantized' views by employing measures of recall precision with an analogue response scale. WM for speech sounds might rely on both continuous and categorical storage mechanisms. Using a novel speech matching paradigm, we measured WM recall precision for phonemes. Vowel qualities were sampled from a formant space continuum. A probe vowel had to be adjusted to match the vowel quality of a target on a continuous, analogue response scale. Crucially, this provided an index of the variability of a memory representation around its true value, and thus allowed us to estimate how memories were distorted from the original sounds. Memory load affected the quality of speech sound recall in two ways. First, there was a gradual decline in recall precision with increasing number of items, consistent with the view that WM representations of speech sounds become noisier with an increase in the number of items held in memory, just as for vision. Based on multidimensional scaling (MDS), the level of noise appeared to be reflected in distortions of the formant space. Second, as memory load increased, there was evidence of greater clustering of participants' responses around particular vowels. A mixture model captured both continuous and categorical responses, demonstrating a shift from continuous to categorical memory with increasing WM load. This suggests that direct acoustic storage can be used for single items, but when more items must be stored, categorical representations must be used.
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Sensory cue inputs and memory-related internal brain activities govern the firing of hippocampal neurons, but which specific firing patterns are induced by either of the two processes remains unclear. We found that sensory cues guided the firing of neurons in rats on a timescale of seconds and supported the formation of spatial firing fields. Independently of the sensory inputs, the memory-related network activity coordinated the firing of neurons not only on a second-long timescale, but also on a millisecond-long timescale, and was dependent on medial septum inputs. We propose a network mechanism that might coordinate this internally generated firing. Overall, we suggest that two independent mechanisms support the formation of spatial firing fields in hippocampus, but only the internally organized system supports short-timescale sequential firing and episodic memory.
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The brain can hold information about multiple objects in working memory. It is not known, however, whether intervals of time can be stored in memory as distinct items. Here, we developed a novel paradigm to examine temporal memory where listeners were required to reproduce the duration of a single probed interval from a sequence of intervals. We demonstrate that memory performance significantly varies as a function of temporal structure (better memory in regular vs. irregular sequences), interval size (better memory for sub- vs. supra-second intervals), and memory load (poor memory for higher load). In contrast memory performance is invariant to attentional cueing. Our data represent the first systematic investigation of temporal memory in sequences that goes beyond previous work based on single intervals. The results support the emerging hypothesis that time intervals are allocated a working memory resource that varies with the amount of other temporal information in a sequence.
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The standard view of the mechanisms underlying learning is that they involve strengthening or weakening synaptic connections. Learned response timing is thought to combine such plasticity with temporally patterned inputs to the neuron. We show here that a cerebellar Purkinje cell in a ferret can learn to respond to a specific input with a temporal pattern of activity consisting of temporally specific increases and decreases in firing over hundreds of milliseconds without a temporally patterned input. Training Purkinje cells with direct stimulation of immediate afferents, the parallel fibers, and pharmacological blocking of interneurons shows that the timing mechanism is intrinsic to the cell itself. Purkinje cells can learn to respond not only with increased or decreased firing but also with an adaptively timed activity pattern.
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The medial temporal lobe (MTL) is believed to support episodic memory, vivid recollection of a specific event situated in a particular place at a particular time. There is ample neurophysiological evidence that the MTL computes location in allocentric space and more recent evidence that the MTL also codes for time. Space and time represent a similar computational challenge; both are variables that cannot be simply calculated from the immediately available sensory information. We introduce a simple mathematical framework that computes functions of both spatial location and time as special cases of a more general computation. In this framework, experience unfolding in time is encoded via a set of leaky integrators. These leaky integrators encode the Laplace transform of their input. The information contained in the transform can be recovered using an approximation to the inverse Laplace transform. In the temporal domain, the resulting representation reconstructs the temporal history. By integrating movements, the equations give rise to a representation of the path taken to arrive at the present location. By modulating the transform with information about allocentric velocity, the equations code for position of a landmark. Simulated cells show a close correspondence to neurons observed in various regions for all three cases. In the temporal domain, novel secondary analyses of hippocampal time cells verified several qualitative predictions of the model. An integrated representation of spatiotemporal context can be computed by taking conjunctions of these elemental inputs, leading to a correspondence with conjunctive neural representations observed in dorsal CA1.
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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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Working memory is widely considered to be limited in capacity, holding a fixed, small number of items, such as Miller's 'magical number' seven or Cowan's four. It has recently been proposed that working memory might better be conceptualized as a limited resource that is distributed flexibly among all items to be maintained in memory. According to this view, the quality rather than the quantity of working memory representations determines performance. Here we consider behavioral and emerging neural evidence for this proposal.
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Three questions have been prominent in the study of visual working memory limitations: (a) What is the nature of mnemonic precision (e.g., quantized or continuous)? (b) How many items are remembered? (c) To what extent do spatial binding errors account for working memory failures? Modeling studies have typically focused on comparing possible answers to a single one of these questions, even though the result of such a comparison might depend on the assumed answers to both others. Here, we consider every possible combination of previously proposed answers to the individual questions. Each model is then a point in a 3-factor model space containing a total of 32 models, of which only 6 have been tested previously. We compare all models on data from 10 delayed-estimation experiments from 6 laboratories (for a total of 164 subjects and 131,452 trials). Consistently across experiments, we find that (a) mnemonic precision is not quantized but continuous and not equal but variable across items and trials; (b) the number of remembered items is likely to be variable across trials, with a mean of 6.4 in the best model (median across subjects); (c) spatial binding errors occur but explain only a small fraction of responses (16.5% at set size 8 in the best model). We find strong evidence against all 6 documented models. Our results demonstrate the value of factorial model comparison in working memory. (PsycINFO Database Record (c) 2014 APA, all rights reserved).
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Psychologists have long distinguished between prospective and retrospective timing to highlight the difference between our sense of duration during an experience in passing and our sense of duration in hindsight. Humans and other animals use prospective timing in the seconds-to-minutes range in order to learn durations, and can organize their behaviour based upon this knowledge when they know that duration information will be important ahead of time. By contrast, when durations are estimated after the fact, thus precluding the subject from consciously attending to temporal information, duration information must be extracted from other memory representations. The accumulated evidence from prospective timing research has generally led to the hippocampus (HPC) being casted in a supporting role with prefrontal-striatal, cortical or cerebellar circuits playing the lead. Here, I review findings from the animal and human literature that have led to this conclusion and consider that the contribution of the HPC to duration memory is understated because we have little understanding about how we remember duration.
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Mammalian brains exhibit population oscillations, the structures of which vary in time and space according to behavioural state. A proposed function of these oscillations is to control the flow of signals among anatomically connected networks. However, the nature of neural coding that may support selective communication that depends on oscillations has received relatively little attention. Here, we consider the role of multiplexing, whereby multiple information streams share a common neural substrate. We suggest that multiplexing implemented through periodic modulation of firing-rate population codes enables flexible reconfiguration of effective connectivity among brain areas.
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Scalar Timing Theory (an information-processing version of Scalar Expectancy Theory) and its evolution into the neurobiologically plausible Striatal Beat-Frequency (SBF) theory of interval timing are reviewed. These pacemaker/accumulator or oscillation/coincidence detection models are then integrated with the Adaptive Control of Thought-Rational (ACT-R) cognitive architecture as dedicated timing modules that are able to make use of the memory and decision-making mechanisms contained in ACT-R. The different predictions made by the incorporation of these timing modules into ACT-R are discussed as well as the potential limitations. Novel implementations of the original SBF model that allow it to be incorporated into ACT-R in a more fundamental fashion than the earlier simulations of Scalar Timing Theory are also considered in conjunction with the proposed properties and neural correlates of the "internal clock".
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Time and space are two critical elements of episodic memory that are supported by the hippocampus. Yet, until recently, there has been much greater focus on the involvement of this structure in spatial than in temporal features of memory. Here we highlight evidence from neuropsychological studies of patients with medial temporal lobe lesions, which have provided evidence that the hippocampus is critical for multiple facets of time, even in tasks that are not typically considered episodic. These studies show that the hippocampus supports memory for first, event duration, second, temporal order, and third, temporally discontiguous experiences. Overall, these findings align with theoretical models suggesting that the hippocampus codes for the temporal context of unfolding events.
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Episodic memory involves coding of the spatial location and time of individual events. Coding of space and time is also relevant to working memory, spatial navigation, and the disambiguation of overlapping memory representations. Neurophysiological data demonstrate that neuronal activity codes the current, past and future location of an animal as well as temporal intervals within a task. Models have addressed how neural coding of space and time for memory function could arise, with both dimensions coded by the same neurons. Neural coding could depend upon network oscillatory and attractor dynamics as well as modulation of neuronal intrinsic properties. These models are relevant to the coding of space and time involving structures including the hippocampus, entorhinal cortex, retrosplenial cortex, striatum and parahippocampal gyrus, which have been implicated in both animal and human studies.
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Psychologists have long distinguished between prospective and retrospective timing to highlight the difference between our sense of duration during an experience in passing and our sense of duration in hindsight. Humans and other animals use prospective timing in the seconds-to-minutes range in order to learn durations, and can organize their behaviour based upon this knowledge when they know that duration information will be important ahead of time. By contrast, when durations are estimated after the fact, thus precluding the subject from consciously attending to temporal information, duration information must be extracted from other memory representations. The accumulated evidence from prospective timing research has generally led to the hippocampus (HPC) being casted in a supporting role with prefrontal–striatal, cortical or cerebellar circuits playing the lead. Here, I review findings from the animal and human literature that have led to this conclusion and consider that the contribution of the HPC to duration memory is understated because we have little understanding about how we remember duration.
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Hippocampal replay during sharp-wave ripple events (SWRs) is thought to drive memory consolidation in hippocampal and cortical circuits. Changes in neocortical activity can precede SWR events, but whether and how these changes influence the content of replay remains unknown. Here we show that during sleep there is a rapid cortical-hippocampal-cortical loop of information flow around the times of SWRs. We recorded neural activity in auditory cortex (AC) and hippocampus of rats as they learned a sound-guided task and during sleep. We found that patterned activation in AC precedes and predicts the subsequent content of hippocampal activity during SWRs, while hippocampal patterns during SWRs predict subsequent AC activity. Delivering sounds during sleep biased AC activity patterns, and sound-biased AC patterns predicted subsequent hippocampal activity. These findings suggest that activation of specific cortical representations during sleep influences the identity of the memories that are consolidated into long-term stores.
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The contributions of cortico-cerebellar and cortico-striatal circuits to timing and time perception has often been a point of contention. In this review we propose that the cerebellum principally functions to reduce variability, through the detection of stimulus onsets and the sub-division of longer durations, thus contributing to both sub-second and supra-second timing. This sensitivity of the cerebellum to stimulus dynamics and subsequent integration with motor control allows it to accurately measure intervals within a range of 100 – 2000 ms. For intervals in the supra-second range (e.g., > 2000 ms), we propose that cerebellar output signals from the dentate nucleus pass through thalamic connections to the striatum, where cortico-thalamic-striatal circuits supporting high-level cognitive functions take over. Moreover, the importance of intrinsic circuit dynamics as well as behavioral, neuroimaging, and lesion studies of the cerebellum and striatum are discussed in terms of a framework positing initiation, continuation, adjustment, and termination phases of temporal processing.
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Interval timing behavior and its sensitivity to both temporal context and changes in dopamine (DA) levels has recently received considerable attention. Nevertheless, the exact manner in which those interactions occur is far from clear. We examined temporal reproduction with feedback in the supra-seconds range as a function of DA levels using two well-studied timing procedures. Healthy young and aged participants were studied as well as Parkinson’s disease (PD) patients tested ON and OFF their dopaminergic medication. The findings confirm the hypothesis that the “migration effect” (e.g., “short” durations are over-produced and “long” durations are under-produced) in PD patients and the closely related Vierordt’s law effect are largely influenced by the effective level of DA and in the case of the “migration effect” by the probability of feedback as well. Using a Bayesian model seeking optimal timing under conditions of uncertainty, we were able to accurately simulate the distorted patterns of temporal reproduction in all groups of participants. As DA levels decrease across groups, optimal timing behavior shifts towards a greater reliance on a statistical representation of all of the durations reproduced within a specific temporal context rather than on the representation of a single duration being timed on any one trial. This analysis demonstrates the utility of Bayesian models of interval timing and highlights the importance of DA levels on clock speed and the associated uncertainty that contributes to temporal distortions.
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The meaning we derive from our experiences is not a simple static extraction of the elements but is largely based on the order in which those elements occur. Models propose that sequence encoding is supported by interactions between high- and low-frequency oscillations, such that elements within an experience are represented by neural cell assemblies firing at higher frequencies (gamma) and sequential order is encoded by the specific timing of firing with respect to a lower frequency oscillation (theta). During episodic sequence memory formation in humans, we provide evidence that items in different sequence positions exhibit greater gamma power along distinct phases of a theta oscillation. Furthermore, this segregation is related to successful temporal order memory. Our results provide compelling evidence that memory for order, a core component of an episodic memory, capitalizes on the ubiquitous physiological mechanism of theta-gamma phase-amplitude coupling.
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Telling time and anticipating when external events will happen is among the most important tasks the brain performs. Yet the neural mechanisms underlying timing remain elusive. One theory proposes that timing is a general and intrinsic computation of cortical circuits. We tested this hypothesis using electrical and optogenetic stimulation to determine if brain slices could “learn” temporal intervals. Presentation of intervals between 100 and 500 ms altered the temporal profile of evoked network activity in an interval and pathway-specific manner—suggesting that the network learned to anticipate an expected stimulus. Recordings performed during training revealed a progressive increase in evoked network activity, followed by subsequent refinement of temporal dynamics, which was related to a time-window-specific increase in the excitatory-inhibitory balance. These results support the hypothesis that subsecond timing is an intrinsic computation and that timing emerges from network-wide, yet pathway-specific, changes in evoked neural dynamics.
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This review outlines the basic psychological and neurobiological processes associated with age-related distortions in timing and time perception in the hundredths of milliseconds-to-minutes range. The difficulty in separating indirect effects of impairments in attention and memory from direct effects on timing mechanisms is addressed. The main premise is that normal aging is commonly associated with increased noise and temporal uncertainty as a result of impairments in attention and memory as well as the possible reduction in the accuracy and precision of a central timing mechanism supported by dopamine-glutamate interactions in cortico-striatal circuits. Pertinent to these findings, potential interventions that may reduce the likelihood of observing age-related declines in timing are discussed. Bayesian optimization models are able to account for the adaptive changes observed in time perception by assuming that older adults are more likely to base their temporal judgments on statistical inferences derived from multiple trials than on a single trial’s clock reading, which is more susceptible to distortion. We propose that the timing functions assigned to the age-sensitive fronto-striatal network can be subserved by other neural networks typically associated with finely-tuned perceptuo-motor adjustments, through de-generacy principles (different structures serving a common function).
Article
Most of the computations and tasks performed by the brain require the ability to tell time, and process and generate temporal patterns. Thus, there is a diverse set of neural mechanisms in place to allow the brain to tell time across a wide range of scales: from interaural delays on the order of microseconds to circadian rhythms and beyond. Temporal processing is most sophisticated on the scale of tens of milliseconds to a few seconds, because it is within this range that the brain must recognize and produce complex temporal patterns — such as those that characterize speech and music. Most models of timing, however, have focused primarily on simple intervals and durations, thus it is not clear whether they will generalize to complex pattern-based temporal tasks. Here, we review neurobiologically based models of timing in the subsecond range, focusing on whether they generalize to tasks that require placing consecutive intervals in the context of an overall pattern, that is, pattern timing.
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The ability to decipher where one needs to be and when it is most beneficial to be there are fundamental to the success of an organism. Humans along with other animals are able to extract duration and temporal order from external as well as internal stimuli, though lacking a dedicated sensory organ for time. A plethora of studies have focused on dorsal striatal and cerebellar networks as primary timing circuits with medium spiny neurons and Purkinje cells acting as the core temporal integrators within these circuits, respectively. However, recent findings have also made a strong case for the inclusion of the hippocampus with the discovery of hippocampal ‘time cells’. The denoted cells are pyramidal cells within the hippocampal CA1 area that exhibit increased firing rates in relation to elapsing durations, independent of the space and distance traveled. Previous behavioral work had implicated the role of the hippocampus in temporal processing, but only as of late has this work been substantiated with direct electrophysiological evidence. We describe the most recent evidence supporting the identification of ‘time cells’ in the subcortical structures of the striatum, hippocampus, and cerebellum and indicate how these different timing systems might be integrated into a common percept for time.
Article
The ability to decipher where one needs to be and when it is most beneficial to be there are fundamental to the success of an organism. Humans along with other animals are able to extract duration and temporal order from external as well as internal stimuli, though lacking a dedicated sensory organ for time. A plethora of studies have focused on dorsal striatal and cerebellar networks as primary timing circuits with medium spiny neurons and Purkinje cells acting as the core temporal integrators within these circuits, respectively. However, recent findings have also made a strong case for the inclusion of the hippocampus with the discovery of hippocampal ‘time cells’. The denoted cells are pyramidal cells within the hippocampal CA1 area that exhibit increased firing rates in relation to elapsing durations, independent of the space and distance traveled. Previous behavioral work had implicated the role of the hippocampus in temporal processing, but only as of late has this work been substantiated with direct electrophysiological evidence. We describe the most recent evidence supporting the identification of ‘time cells’ in the subcortical structures of the striatum, hippocampus, and cerebellum and indicate how these different timing systems might be integrated into a common percept for time.
Article
The spatial scale of grid cells may be provided by self-generated motion information or by external sensory information from environmental cues. To determine whether grid cell activity reflects distance traveled or elapsed time independent of external information, we recorded grid cells as animals ran in place on a treadmill. Grid cell activity was only weakly influenced by location, but most grid cells and other neurons recorded from the same electrodes strongly signaled a combination of distance and time, with some signaling only distance or time. Grid cells were more sharply tuned to time and distance than non-grid cells. Many grid cells exhibited multiple firing fields during treadmill running, parallel to the periodic firing fields observed in open fields, suggesting a common mode of information processing. These observations indicate that, in the absence of external dynamic cues, grid cells integrate self-generated distance and time information to encode a representation of experience.
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The residual fluctuations that naturally arise in experimental inquiry are analyzed in terms of their time histories. Although these fluctuations are generally relegated to a statistical purgatory known as unexplained variance, this article shows that they may harbor a long-term memory process known as 1/f noise. This type of noise has been encountered in a number of biological and physical systems and is theorized to be a signature of dynamic complexity. Its presence in psychological data appears to be associated with the most elementary aspect of cognitive process, the formation of representations.
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Immediate repetition of a stimulus reduces its apparent duration relative to a novel item. Recent work indicates that this may reflect suppressed cortical responses to repeated stimuli, arising from neural adaptation and/or the predictive coding of expected stimuli. This article summarizes recent behavioral and neurobiological studies linking perceived time to the magnitude of cortical responses, including work suggesting that variations in GABA-mediated cortical inhibition may underlie some of the individual differences in time perception. We suggest that the firing of cortical neurons can be modified using simple recurrent networks with time-dependent processes that are modulated by GABA levels. These local networks feed into a core-timing network used to integrate across stimulus inputs/modalities, thereby allowing for the coordination of multiple duration ranges and effector systems.
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The hippocampal CA2 subregion has a different anatomical connectivity pattern within the entorhino-hippocampal circuit than either the CA1 or CA3 subregion. Yet major differences in the neuronal activity patterns of CA2 compared with the other CA subregions have not been reported. We show that standard spatial and temporal firing patterns of individual hippocampal principal neurons in behaving rats, such as place fields, theta modulation, and phase precession, are also present in CA2, but that the CA2 subregion differs substantially from the other CA subregions in its population coding. CA2 ensembles do not show a persistent code for space or for differences in context. Rather, CA2 activity patterns become progressively dissimilar over time periods of hours to days. The weak coding for a particular context is consistent with recent behavioral evidence that CA2 circuits preferentially support social, emotional, and temporal rather than spatial aspects of memory. Copyright © 2015 Elsevier Inc. All rights reserved.
Article
Interval timing and working memory are critical components of cognition that are supported by neural oscillations in prefrontal-striatal-hippocampal circuits. In this review, the properties of interval timing and working memory are explored in terms of behavioral, anatomical, pharmacological, and neurophysiological findings. We then describe the various neurobiological theories that have been developed to explain these cognitive processes – largely independent of each other. Following this, a coupled excitatory-inhibitory oscillation (EIO) model of temporal processing is proposed to address the shared oscillatory properties of interval timing and working memory. Using this integrative approach, we describe a hybrid model explaining how interval timing and working memory can originate from the same oscillatory processes, but differ in terms of which dimension of the neural oscillation is utilized for the extraction of item, temporal order, and duration information. This extension of the striatal beat-frequency (SBF) model of interval timing (Matell and Meck, 2000, 2004) is based on prefrontal-striatal-hippocampal circuit dynamics and has direct relevance to the pathophysiological distortions observed in time perception and working memory in a variety of psychiatric and neurological conditions.
Article
Recent studies have revealed the existence of hippocampal neurons that fire at successive moments in temporally structured experiences. Several studies have shown that such temporal coding is not attributable to external events, specific behaviours or spatial dimensions of an experience. Instead, these cells represent the flow of time in specific memories and have therefore been dubbed 'time cells'. The firing properties of time cells parallel those of hippocampal place cells; time cells thus provide an additional dimension that is integrated with spatial mapping. The robust representation of both time and space in the hippocampus suggests a fundamental mechanism for organizing the elements of experience into coherent memories.
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Some argue that hippocampus supports declarative memory, our capacity to recall facts and events, whereas others view the hippocampus as part of a system dedicated to calculating routes through space, and these two contrasting views are pursued largely independently in current research. Here we offer a perspective on where these views can and cannot be reconciled and update a bridging framework that will improve our understanding of hippocampal function. Currently, separate lines of research focus on hippocampal function in spatial navigation or in declarative memory. Here, Eichenbaum and Cohen update their relational memory account to reconcile these approaches and offer new insights into the fundamental mechanisms of memory.
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The hippocampus is critical for human episodic memory, but its role remains controversial. One fundamental question concerns whether the hippocampus represents specific objects or assigns context-dependent representations to objects. Here, we used multivoxel pattern similarity analysis of fMRI data during retrieval of learned object sequences to systematically investigate hippocampal coding of object and temporal context information. Hippocampal activity patterns carried information about the temporal positions of objects in learned sequences, but not about objects or temporal positions in random sequences. Hippocampal activity patterns differentiated between overlapping object sequences and between temporally adjacent objects that belonged to distinct sequence contexts. Parahippocampal and perirhinal cortex showed different pattern information profiles consistent with coding of temporal position and object information, respectively. These findings are consistent with models proposing that the hippocampus represents objects within specific temporal contexts, a capability that might explain its critical role in episodic memory.
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Mice with cytotoxic lesions of the dorsal hippocampus (DH) underestimated 15 s and 45 s target durations in a bi-peak procedure as evidenced by proportional leftward shifts of the peak functions that emerged during training as a result of decreases in both 'start' and 'stop' times. In contrast, mice with lesions of the ventral hippocampus (VH) displayed rightward shifts that were immediately present and were largely limited to increases in the 'stop' time for the 45 s target duration. Moreover, the effects of the DH lesions were congruent with the scalar property of interval timing in that the 15 s and 45 s functions superimposed when plotted on a relative timescale, whereas the effects of the VH lesions violated the scalar property. Mice with DH lesions also showed enhanced reversal learning in comparison to control and VH lesioned mice. These results are compared with the timing distortions observed in mice lacking δ-opioid receptors (Oprd1(-/-)) which were similar to mice with DH lesions. Taken together, these results suggest a balance between hippocampal-striatal interactions for interval timing and demonstrate possible functional dissociations along the septotemporal axis of the hippocampus in terms of motivation, timed response thresholds and encoding in temporal memory.
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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.