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Beat induction is the cognitive ability that allow humans to listen to a regular pulse in music and move in synchrony with it. Although auditory rhythmic cues are known to induce more consistent synchronization than flashing visual metronomes, this asymmetry can be canceled out by visual moving metronomes. Here, we investigated whether the naturalness of the visual motion or its kinematics could provide a synchronization advantage over flashing metronomes. Subjects tap in sync with visual isochronous metronomes defined by vertically or horizontally accelerating and decelerating motion, either congruent or not with natural gravity, and then continue tapping with no metronome. We found that motion kinematics was the predominant factor determining rhythm synchronization, as accelerating moving metronomes in either cardinal direction produced more precise and predictive tapping than decelerating or flashing conditions. Notably, a Bayesian observer model revealed that error correction during tapping synchronization and regression towards the mean in accuracy during tapping continuation in the absence of external cues are optimal control strategies independently of the moving properties of the visual metronomes. Our results support the notion that accelerating visual metronomes convey a strong sense of beat as seen in the cueing movements of an orchestra director.

The measurement of time in the subsecond scale is critical for many sophisticated behaviors, yet its neural underpinnings are largely unknown. Recent neurophysiological experiments from our laboratory have shown that the neural activity in the medial premotor areas (MPC) of macaques can represent different aspects of temporal processing. During interval categorization, we found that preSMA encodes a subjective category limit by reaching a peak of activity at a time that divides the set of test intervals into short and long. We also observed neural signals associated with the category selected by the subjects and the reward outcomes of the perceptual decision. On the other hand, we have studied the behavioral and neurophysiological basis of rhythmic timing. First, we have shown in different tapping tasks that macaques are able to produce predictively and accurately intervals that are cued by auditory or visual metronomes or when intervals are produced internally without sensory guidance. In addition, we found that the rhythmic timing mechanism in MPC is governed by different layers of neural clocks. Next, the instantaneous activity of single cells shows ramping activity that encode the elapsed or remaining time for a tapping movement. In addition, we found MPC neurons that build neural sequences, forming dynamic patterns of activation that flexibly cover all the produced interval depending on the tapping tempo. This rhythmic neural clock resets on every interval providing an internal representation of pulse. Furthermore, the MPC cells show mixed selectivity, encoding not only elapsed time, but also the tempo of the tapping and the serial order element in the rhythmic sequence. Hence, MPC can map different task parameters, including the passage of time, using different cell populations. Finally, the projection of the time varying activity of MPC hundreds of cells into a low dimensional state space showed circular neural trajectories whose geometry represent the internal pulse and the tapping tempo. Overall, these findings support the notion that MPC is part of the core timing mechanism for both single interval and rhythmic timing, using neural clocks with different encoding principles, probably to flexibly encode and mix the timing representation with other task parameters.

Beta oscillations are involved in a variety of cognitive functions beyond their traditional sensorimotor role. Based on prior findings of content-specific beta synchronization during working memory and decision making, we hypothesized that beta activity supports the activation and reactivation of cortical representations by mediating neural ensemble formation within and between brain regions. We here found that beta activity in monkey dorsolateral prefrontal cortex (dlPFC) and in pre-supplementary motor area (preSMA) reflects the content of a stimulus in relation to the task context, regardless of its objective properties. In multiple versions of a categorization task, we changed the boundary between categories from one block of trials to the next, such that a stimulus which belonged to one of two categories during one block could belong to the other category during the next one. During a delay in which monkeys had to hold their categorical decision in mind, we found that two distinct beta-band frequencies were consistently associated with the same two relative categories, and that activity in these respective bands predicted the animals’ responses. We characterized beta at these frequencies as transient bursts with distinct temporal profiles. We further showed that dlPFC and preSMA are connected via these distinct frequency channels, with dlPFC driving the frequency separation, a result supported by Granger causality and spike-field coherence analyses. In sum, these results provide support for the role of beta in forming neural ensembles, and further show that such ensembles synchronize at different beta frequencies.

We determined the intersubject association between rhythmic entrainment abilities of human subjects during a synchronization continuation tapping task (SCT) and the macro and microstructural properties of their superficial (SWM) and deep (dWM) white matter. Diffusion-weighted images were obtained from 32 subjects who also performed the SCT with auditory or visual metronomes and five tempos ranging from 550 to 950 ms. We developed a method to determine the fiber density of U-fibers running tangentially to the cortex. Notably, the right audiomotor system showed individual differences in the density of U-fibers that were correlated with the degree of predictive entrainment across subjects. These correlations were selective for the synchronization epoch with auditory metronomes and were specific for tempos around 1.5 Hz. In addition, there was a significant association between predictive rhythmic entrainment and the density and bundle diameter of the corpus callosum (CC), forming a chronotopic map where behavioural correlations of short and long intervals were found with the anterior and posterior portions of the CC. Finally, the fiber bundle cross-section of the arcuate fasciculus, the CC, and the Superior Longitudinal Fasciculus showed a significant correlation with the mean asynchronies of the auditory SCT. These findings suggest that the structural properties of the SWM and dWM in the audiomotor system support the predictive abilities of subjects during rhythmic tapping, where the density of cortical U-fibers are linked to the preferred tapping tempo, and the bundle properties of CC define an interval selective topography that has an anterior posterior gradient.

Dopamine, and specifically the D2 system, has been implicated in timing tasks where the absolute duration of individual time intervals is encoded discretely, yet the role of D2 during beat perception and entrainment remains largely unknown. In this type of timing, a beat is perceived as the pulse that marks equally spaced points in time and, once extracted, produces the tendency in humans to entrain or synchronize their movements to it. Hence, beat-based timing is crucial for musical execution. In this study we investigated the effects of systemic injections of quinpirole (0.005–0.05 mg/kg), a D2-like agonist, on the isochronous rhythmic tapping of rhesus monkeys, a classical task for the study of beat entrainment. We compared the rhythmic timing accuracy, precision, and the asynchronies of the monkeys with or without the effects of quinpirole, as well as their reaction times in a control serial reaction time task (SRTT). The results showed a dose-dependent disruption in the scalar property of rhythmic timing due to quinpirole administration. Specifically, we found similar temporal variabilities as a function of the metronome tempo at the largest dose, instead of the increase in variability across durations that is characteristic of the timing Weber law. Notably, these effects were not due to alterations in the basic sensorimotor mechanism for tapping to a sequence of flashing stimuli, because quinpirole did not change the reaction time of the monkeys during SRTT. These findings support the notion of a key role of the D2 system in the rhythmic timing mechanism, especially in the control of temporal precision. NEW & NOTEWORTHY Perceiving and moving to the beat of music is a fundamental trait of musical cognition. We measured the effect of quinpirole, a D2-like agonist, on the precision and accuracy of rhythmic tapping to a metronome in two rhesus monkeys. Quinpirole produced a flattening of the temporal variability as a function of tempo duration, instead of the increase in variability across durations that is characteristic of the scalar property, a hallmark property of timing.

Highlights • Data sharing of primate neuroimaging offers new opportunities. • The potential of metadata to enrich primate neuroimaging is described. • Illustration of how meta-data can be shared in the BIDS format is provided., Sharing and pooling large amounts of non-human primate neuroimaging data offer new exciting opportunities to understand the primate brain. The potential of big data in non-human primate neuroimaging could however be tremendously enhanced by combining such neuroimaging data with other types of information. Here we describe metadata that have been identified as particularly valuable by the non-human primate neuroimaging community, including behavioural, genetic, physiological and phylogenetic data.

Neuroimaging non-human primates (NHPs) is a growing, yet highly specialized field of neuroscience. Resources that were primarily developed for human neuroimaging often need to be significantly adapted for use with NHPs or other animals, which has led to an abundance of custom, in-house solutions. In recent years, the global NHP neuroimaging community has made significant efforts to transform the field towards more open and collaborative practices. Here we present the PRIMatE Resource Exchange (PRIME-RE), a new collaborative online platform for NHP neuroimaging. PRIME-RE is a dynamic community-driven hub for the exchange of practical knowledge, specialized analytical tools, and open data repositories, specifically related to NHP neuroimaging. PRIME-RE caters to both researchers and developers who are either new to the field, looking to stay abreast of the latest developments, or seeking to collaboratively advance the field . Pypreclin work was supported by the Fondation pour la Recherche Medicale (FRM grant number ECO20160736100 to JT), Fondation de France, Human Brain Project (Corticity project). RT and KH are supported by ANR-19-DATA-0025-01 NeuroWebLab. RBM is supported by the Biotechnology and Biological Sciences Research Council (BBSRC) UK [BB/N019814/1]. The Wellcome Centre for Integrative Neuroimaging is supported by core funding from the Wellcome Trust [203129/Z/16/Z]. Sí

Highlights • Strengths and challenges of longitudinal non-human primate MRI are described. • Statistical power calculation of longitudinal and cross-sectional designs are provided. • The impact of template choice on grey matter estimation is demonstrated. • Recommendations for designing and analysing such studies are provided., Longitudinal non-human primate neuroimaging has the potential to greatly enhance our understanding of primate brain structure and function. Here we describe its specific strengths, compared to both cross-sectional non-human primate neuroimaging and longitudinal human neuroimaging, but also its associated challenges. We elaborate on factors guiding the use of different analytical tools, subject-specific versus age-specific templates for analyses, and issues related to statistical power.

When we intensively train a timing skill, such as learning to play the piano, we do not only produce brain changes associated with task-specific learning, but also improve the performance on other temporal behaviors that depend on these tuned neural resources. Since the neural basis of time learning and generalization are still unknown, we measured the changes in neural activity associated with the transfer of learning from perceptual to motor timing. We found that intense training in an interval discrimination task increased the acuity of time perception in a group of subjects that also showed learning transfer, expressed as a reduction in tapping variability during an internally-driven periodic motor task. However, we also found subjects with no learning and generalization effects, and a third group with no signs of learning but with practice-based decreases in temporal variability in the motor task. Notably, these heterogeneous populations of subjects shared a common increase of activity in the medial premotor areas and the putamen in the post-with respect to the pre-training session of the tapping task. These findings support the idea that the core timing network is constantly refining its ability to time behaviors in different contexts and that practice is critical for keeping the neural clock attuned and properly functioning.

Neuroimaging non-human primates (NHPs) is a growing, yet highly specialized field of neuroscience. Resources that were primarily developed for human neuroimaging often need to be significantly adapted for use with NHPs or other animals, which has led to an abundance of custom, in-house solutions. In recent years, the global NHP neuroimaging community has made significant efforts to transform the field towards more open and collaborative practices. Here we present the PRIMatE Resource Exchange (PRIME-RE), a new collaborative online platform for NHP neuroimaging. PRIME-RE is a dynamic community-driven hub for the exchange of practical knowledge, specialized analytical tools, and open data repositories, specifically related to NHP neuroimaging. PRIME-RE caters to both researchers and developers who are either new to the field, looking to stay abreast of the latest developments, or seeking to collaboratively advance the field. HighlightsO_LIPRIME-RE is a bottom-up open science platform for non-human primate neuroimaging. C_LIO_LIThe website hosts a wiki and info about analytical tools and open data repositories. C_LIO_LISpecialized tools address structural, functional & diffusion-weighted analysis. C_LIO_LIMultiple templates & atlases for several non-human primate species are highlighted. C_LIO_LICommunication channels facilitate international conversation and collaboration C_LI

Accurate extraction of the cortical brain surface is critical for cortical thickness estimation and a key element to perform multimodal imaging analysis, where different metrics are integrated and compared in a common space. While brain surface extraction has become widespread practice in human studies, several challenges unique to neuroimaging of non-human primates (NHP) have hindered its adoption for the study of macaques. Although, some of these difficulties can be addressed at the acquisition stage, several common artifacts can be minimized through image preprocessing. Likewise, there are several image analysis pipelines for human MRIs, but very few automated methods for extraction of cortical surfaces have been reported for NHPs and none have been tested on data from diverse sources. We present PREEMACS, a pipeline that standardizes the preprocessing of structural MRI images (T1- and T2-weighted) and carries out an automatic surface extraction of the macaque brain. Building upon and extending pre-existing tools, the first module performs volume orientation, image cropping, intensity non-uniformity correction, and volume averaging, before skull-stripping through a convolutional neural network. The second module performs quality control using an adaptation of MRIqc method to extract objective quality metrics that are then used to determine the likelihood of accurate brain surface estimation. The third and final module estimates the white matter (wm) and pial surfaces from the T1-weighted volume (T1w) using an NHP customized version of FreeSurfer aided by the T2-weighted volumes (T2w). To evaluate the generalizability of PREEMACS, we tested the pipeline using 57 T1w/T2w NHP volumes acquired at 11 different sites from the PRIME-DE public dataset. Results showed an accurate and robust automatic brain surface extraction from images that passed the quality control segment of our pipeline. This work offers a robust, efficient and generalizable pipeline for the automatic standardization of MRI surface analysis on NHP.

Contains fulltext : 217200.pdf (Publisher’s version ) (Closed access) Nonhuman primate neuroimaging is on the cusp of a transformation, much in the same way its human counterpart was in 2010, when the Human Connectome Project was launched to accelerate progress. Inspired by an open data-sharing initiative, the global community recently met and, in this article, breaks through obstacles to define its ambitions. 4 p.

Perceptual categorization depends on the assignment of different stimuli to specific groups based, in principle, on the notion of flexible categorical boundaries. To determine the neural basis of categorical boundaries, we record the activity of pre-SMA neurons of monkeys executing an interval categorization task in which the limit between short and long categories changes between blocks of trials within a session. A large population of cells encodes this boundary by reaching a constant peak of activity close to the corresponding subjective limit. Notably, the time at which this peak is reached changes according to the categorical boundary of the current block, predicting the monkeys’ categorical decision on a trial-by-trial basis. In addition, pre-SMA cells also represent the category selected by the monkeys and the outcome of the decision. These results suggest that the pre-SMA adaptively encodes subjective duration boundaries between short and long durations and contains crucial neural information to categorize intervals and evaluate the outcome of such perceptual decisions., Grouping stimuli into categories often depends on a subjective determination of category boundaries. Here the authors report a neuronal population in pre-supplementary motor area whose peak activity predicts the categorical decision boundary between long and short time intervals on a trial-by-trial basis.

The study of non-human primates in complex behaviors such as rhythm perception and entrainment is critical to understand the neurophysiological basis of human cognition. Next to reviewing the role of beta oscillations in human beat perception, here we discuss the role of primate putaminal oscillatory activity in the control of rhythmic movements that are guided by a sensory metronome or internally gated. The analysis of the local field potentials of the behaving macaques showed that gamma-oscillations reflect local computations associated with stimulus processing of the metronome, whereas beta-activity involves the entrainment of large putaminal circuits, probably in conjunction with other elements of cortico-basal ganglia-thalamo-cortical circuit, during internally driven rhythmic tapping. Thus, this review emphasizes the need of parametric neurophysiological observations in non-human primates that display a well-controlled behavior during high-level cognitive processes.

The neural underpinnings of rhythmic behavior, including music and dance, have been studied using the synchronization-continuation task (SCT), where subjects initially tap in synchrony with an isochronous metronome and then keep tapping at a similar rate via an internal beat mechanism. Here, we provide behavioral and neural evidence that supports a resetting drift-diffusion model (DDM) during SCT. Behaviorally, we show the model replicates the linear relation between the mean and standard-deviation of the intervals produced by monkeys in SCT. We then show that neural populations in the medial premotor cortex (MPC) contain an accurate trial-by-trial representation of elapsed-time between taps. Interestingly, the autocorrelation structure of the elapsed-time representation is consistent with a DDM. These results indicate that MPC has an orderly representation of time with features characteristic of concatenated DDMs and that this population signal can be used to orchestrate the rhythmic structure of the internally timed elements of SCT.SIGNIFICANCE STATEMENTThe present study used behavioral data, ensemble recordings from medial premotor cortex (MPC) in macaque monkeys, and computational modeling, to establish evidence in favor of a class of drift-diffusion models of rhythmic timing during a synchronization-continuation tapping task (SCT). The linear relation between the mean and standard-deviation of the intervals produced by monkeys in SCT is replicated by the model. Populations of MPC cells faithfully represent the elapsed time between taps, and there is significant trial-by-trial relation between decoded times and the timing behavior of the monkeys. Notably, the neural decoding properties, including its autocorrelation structure are consistent with a set of drift-diffusion models that are arranged sequentially and that are resetting in each SCT tap.

The proper response to an ever-changing environment depends on the ability to quantify elapsed time, memorize short intervals and forecast when an upcoming experience may occur. A recent study describes the encoding principles of these three types of time using computational modelling.

We describe a technique to semichronically record the cortical extracellular neural activity in the behaving monkey employing commercial high-density electrodes. After the design and construction of low cost microdrives that allow varying the depth of the recording locations after the implantation surgery, we recorded the extracellular unit activity from pools of neurons at different depths in the presupplementary motor cortex (pre-SMA) of a rhesus monkey trained in a tapping task. The collected data were processed to classify cells as putative pyramidal cells or interneurons on the basis of their waveform features. We also demonstrate that short time cross-correlogram occasionally yields unit pairs with high short latency (