Macaque monkeys and humans sample temporal regularities in the acoustic environment.

Many animal species show comparable abilities to detect basic rhythms and produce rhythmic behavior. Yet, the capacities to process complex rhythms and synchronize rhythmic behavior appear to be species-specific: vocal learning animals can, but some primates might not. This discrepancy is of high interest as there is a putative link between rhythm processing and the development of sophisticated sensorimotor behavior in humans. Do our closest ancestors show comparable endogenous dispositions to sample the acoustic environment in the absence of task instructions and training? We recorded EEG from macaque monkeys and humans while they passively listened to isochronous equitone sequences. Individual- and trial-level analyses showed that macaque monkeys' and humans' delta-band neural oscillations encoded and tracked the timing of auditory events. Further, mu- (8-15 Hz) and beta-band (12-20 Hz) oscillations revealed the superimposition of varied accentuation patterns on a subset of trials. These observations suggest convergence in the encoding and dynamic attending of temporal regularities in the acoustic environment, bridging a gap in the phylogenesis of rhythm cognition.

Mapping between sound, brain and behaviour: four-level framework for understanding rhythm processing in humans and non-human primates.

Humans perceive and spontaneously move to one or several levels of periodic pulses (a meter, for short) when listening to musical rhythm, even when the sensory input does not provide prominent periodic cues to their temporal location. Here, we review a multi-levelled framework to understanding how external rhythmic inputs are mapped onto internally represented metric pulses. This mapping is studied using an approach to quantify and directly compare representations of metric pulses in signals corresponding to sensory inputs, neural activity and behaviour (typically body movement). Based on this approach, recent empirical evidence can be drawn together into a conceptual framework that unpacks the phenomenon of meter into four levels. Each level highlights specific functional processes that critically enable and shape the mapping from sensory input to internal meter. We discuss the nature, constraints and neural substrates of these processes, starting with fundamental mechanisms investigated in macaque monkeys that enable basic forms of mapping between simple rhythmic stimuli and internally represented metric pulse. We propose that human evolution has gradually built a robust and flexible system upon these fundamental processes, allowing more complex levels of mapping to emerge in musical behaviours. This approach opens promising avenues to understand the many facets of rhythmic behaviours across individuals and species. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

Monkeys share the neurophysiological basis for encoding sound periodicities captured by the frequency-following response with humans.

The extraction and encoding of acoustical temporal regularities are fundamental for human cognitive auditory abilities such as speech or beat entrainment. Because the comparison of the neural sensitivity to temporal regularities between human and animals is fundamental to relate non-invasive measures of auditory processing to their neuronal basis, here we compared the neural representation of auditory periodicities between human and non-human primates by measuring scalp-recorded frequency-following response (FFR). We found that rhesus monkeys can resolve the spectrotemporal structure of periodic stimuli to a similar extent as humans by exhibiting a homologous FFR potential to the speech syllable /da/. The FFR in both species is robust and phase-locked to the fundamental frequency of the sound, reflecting an effective neural processing of the fast-periodic information of subsyllabic cues. Our results thus reveal a conserved neural ability to track acoustical regularities within the primate order. These findings open the possibility to study the neurophysiology of complex sound temporal processing in the macaque subcortical and cortical areas, as well as the associated experience-dependent plasticity across the auditory pathway in behaving monkeys.

The Computational and Neural Basis of Rhythmic Timing in Medial Premotor Cortex.

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 STATEMENT The 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.

Recording extracellular neural activity in the behaving monkey using a semichronic and high-density electrode system.

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 (<5 ms), narrow bin (<3 ms) peaks, indicative of monosynaptic spike transmission from pre- to postsynaptic neurons. These methods have been verified extensively in rodents. Finally, we observed that the pattern of population activity was repetitive over distinct trials of the tapping task. These results show that the semichronic technique is a viable option for the large-scale parallel recording of local circuit activity at different depths in the cortex of the macaque monkey and other large species.

ß oscillations are linked to the initiation of sensory-cued movement sequences and the internal guidance of regular tapping in the monkey.

ß oscillations in the basal ganglia have been associated with interval timing. We recorded the putaminal local field potentials (LFPs) from monkeys performing a synchronization-continuation task (SCT) and a serial reaction-time task (RTT), where the animals produced regularly and irregularly paced tapping sequences, respectively. We compared the activation profile of ß oscillations between tasks and found transient bursts of ß activity in both the RTT and SCT. During the RTT, ß power was higher at the beginning of the task, especially when LFPs were aligned to the stimuli. During the SCT, ß was higher during the internally driven continuation phase, especially for tap-aligned LFPs. Interestingly, a set of LFPs showed an initial burst of ß at the beginning of the SCT, similar to the RTT, followed by a decrease in ß oscillations during the synchronization phase, to finally rebound during the continuation phase. The rebound during the continuation phase of the SCT suggests that the corticostriatal circuit is involved in the control of internally driven motor sequences. In turn, the transient bursts of ß activity at the beginning of both tasks suggest that the basal ganglia produce a general initiation signal that engages the motor system in different sequential behaviors.

Searching for the origins of musicality across species.

In the introduction to this theme issue, Honing et al. suggest that the origins of musicality--the capacity that makes it possible for us to perceive, appreciate and produce music--can be pursued productively by searching for components of musicality in other species. Recent studies have highlighted that the behavioural relevance of stimuli to animals and the relation of experimental procedures to their natural behaviour can have a large impact on the type of results that can be obtained for a given species. Through reviewing laboratory findings on animal auditory perception and behaviour, as well as relevant findings on natural behaviour, we provide evidence that both traditional laboratory studies and studies relating to natural behaviour are needed to answer the problem of musicality. Traditional laboratory studies use synthetic stimuli that provide more control than more naturalistic studies, and are in many ways suitable to test the perceptual abilities of animals. However, naturalistic studies are essential to inform us as to what might constitute relevant stimuli and parameters to test with laboratory studies, or why we may or may not expect certain stimulus manipulations to be relevant. These two approaches are both vital in the comparative study of musicality.

Subsecond timing in primates: comparison of interval production between human subjects and rhesus monkeys.

This study describes the psychometric similarities and differences in motor timing performance between 20 human subjects and three rhesus monkeys during two timing production tasks. These tasks involved tapping on a push-button to produce the same set of intervals (range of 450 to 1,000 ms), but they differed in the number of intervals produced (single vs. multiple) and the modality of the stimuli (auditory vs. visual) used to define the time intervals. The data showed that for both primate species, variability increased as a function of the length of the produced target interval across tasks, a result in accordance with the scalar property. Interestingly, the temporal performance of rhesus monkeys was equivalent to that of human subjects during both the production of single intervals and the tapping synchronization to a metronome. Overall, however, human subjects were more accurate than monkeys and showed less timing variability. This was especially true during the self-pacing phase of the multiple interval production task, a behavior that may be related to complex temporal cognition, such as speech and music execution. In addition, the well-known human bias toward auditory as opposed to visual cues for the accurate execution of time intervals was not evident in rhesus monkeys. These findings validate the rhesus monkey as an appropriate model for the study of the neural basis of time production, but also suggest that the exquisite temporal abilities of humans, which peak in speech and music performance, are not all shared with macaques.

Learning and generalization of time production in humans: rules of transfer across modalities and interval durations.

This article investigated both the ability of naive human subjects to learn interval production, as well as the properties of learning generalization across modalities and interval durations that varied systematically from the over-trained interval. Human subjects trained on a 450-, 650-, or 850-ms single-interval production task, using auditory stimuli to define the intervals, showed a significant decrease in performance variability with intensive training. This learning generalized to the visual modality and to non-trained durations following a Gaussian transfer pattern. However, the learning carryover followed different rules, depending on the duration of the trained interval as follows: (1) the dispersion of the generalization curve increased as a function of the trained interval, (2) the generalization pattern was tilted to the right in the visual condition, and (3) the transfer magnitude for 650 ms was less prominent than for the other two intervals. These findings suggest the existence of neural circuits that are tuned to specific time lengths and that show different temporal processing properties depending on their preferred interval duration.