Luis Prado

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.

Information Processing in the Primate Basal Ganglia during Sensory-Guided and Internally Driven Rhythmic Tapping

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.

Measuring time with different neural chronometers during a synchronization-continuation task

Temporal information processing is critical for many complex behaviors including speech and music cognition, yet its neural substrate remains elusive. We examined the neurophysiological properties of medial premotor cortex (MPC) of two Rhesus monkeys during the execution of a synchronization-continuation tapping task that includes the basic sensorimotor components of a variety of rhythmic behaviors. We show that time-keeping in the MPC is governed by separate cell populations. One group encoded the time remaining for an action, showing activity whose duration changed as a function of interval duration, reaching a peak at similar magnitudes and times with respect to the movement. The other cell group showed a response that increased in duration or magnitude as a function of the elapsed time from the last movement. Hence, the sensorimotor loops engaged during the task may depend on the cyclic interplay between different neuronal chronometers that quantify the time passed and the remaining time for an action.

Rhesus Monkeys (Macaca mulatta) Detect Rhythmic Groups in Music, but Not the Beat

It was recently shown that rhythmic entrainment, long considered a human-specific mechanism, can be demonstrated in a selected group of bird species, and, somewhat surprisingly, not in more closely related species such as nonhuman primates. This observation supports the vocal learning hypothesis that suggests rhythmic entrainment to be a by-product of the vocal learning mechanisms that are shared by several bird and mammal species, including humans, but that are only weakly developed, or missing entirely, in nonhuman primates. To test this hypothesis we measured auditory event-related potentials (ERPs) in two rhesus monkeys (Macaca mulatta), probing a well-documented component in humans, the mismatch negativity (MMN) to study rhythmic expectation. We demonstrate for the first time in rhesus monkeys that, in response to infrequent deviants in pitch that were presented in a continuous sound stream using an oddball paradigm, a comparable ERP component can be detected with negative deflections in early latencies (Experiment 1). Subsequently we tested whether rhesus monkeys can detect gaps (omissions at random positions in the sound stream; Experiment 2) and, using more complex stimuli, also the beat (omissions at the first position of a musical unit, i.e. the ‘downbeat’; Experiment 3). In contrast to what has been shown in human adults and newborns (using identical stimuli and experimental paradigm), the results suggest that rhesus monkeys are not able to detect the beat in music. These findings are in support of the hypothesis that beat induction (the cognitive mechanism that supports the perception of a regular pulse from a varying rhythm) is species-specific and absent in nonhuman primates. In addition, the findings support the auditory timing dissociation hypothesis, with rhesus monkeys being sensitive to rhythmic grouping (detecting the start of a rhythmic group), but not to the induced beat (detecting a regularity from a varying rhythm).

The Context of Temporal Processing Is Represented in the Multidimensional Relationships between Timing Tasks

In the present study we determined the performance interrelations of ten different tasks that involved the processing of temporal intervals in the subsecond range, using multidimensional analyses. Twenty human subjects executed the following explicit timing tasks: interval categorization and discrimination (perceptual tasks), and single and multiple interval tapping (production tasks). In addition, the subjects performed a continuous circle-drawing task that has been considered an implicit timing paradigm, since time is an emergent property of the produced spatial trajectory. All tasks could be also classified as single or multiple interval paradigms. Auditory or visual markers were used to define the intervals. Performance variability, a measure that reflects the temporal and non-temporal processes for each task, was used to construct a dissimilarity matrix that quantifies the distances between pairs of tasks. Hierarchical clustering and multidimensional scaling were carried out on the dissimilarity matrix, and the results showed a prominent segregation of explicit and implicit timing tasks, and a clear grouping between single and multiple interval paradigms. In contrast, other variables such as the marker modality were not as crucial to explain the performance between tasks. Thus, using this methodology we revealed a probable functional arrangement of neural systems engaged during different timing behaviors.

Temporal and spatial categorization in human and non-human primates.

It has been proposed that a functional overlap exists in the brain for temporal and spatial information processing. To test this, we designed two relative categorization tasks in which human subjects and a Rhesus monkey had to assign time intervals or distances to a “short” or “long” category according to varying prototypes. The performance of both species was analyzed using psychometric techniques that showed that they may have similar perceptual, memory, and/or decision mechanisms, specially for the estimation of time intervals. We also did a correlation analysis with human subjects’ psychometric thresholds and the results imply that indeed, temporal and spatial information categorization share neural substrates. However, not all of the tested distances and intervals correlated with each other, suggesting the existence of sub-circuits that process restricted ranges of distances and intervals. A different analysis was done on the monkey data, in which the influence of the previous categorical prototypes was measured on the task currently being performed. Again, we found a significant interaction between previous and current interval and distance categorization. Overall, the present paper points toward common or at least partially overlapped neural circuits for temporal and spatial categorization in primates.

Sensorimotor neural dynamics during isochronous tapping in the medial premotor cortex of the macaque.

We determined the response properties of neurons in the primate medial premotor cortex that were classified as sensory or motor during isochronous tapping to a visual or auditory metronome, using different target intervals and three sequential elements in the task. The cell classification was based on a warping transformation, which determined whether the cell activity was statistically aligned to sensory or motor events, finding a large proportion of cells classified as sensory or motor. Two distinctive clusters of sensory cells were observed, i.e. one cell population with short response‐onset latencies to the previous stimulus, and another that was probably predicting the occurrence of the next stimuli. These cells were called sensory‐driven and stimulus‐predicting neurons, respectively. Sensory‐driven neurons showed a clear bias towards the visual modality and were more responsive to the first stimulus, with a decrease in activity for the following sequential elements of the metronome. In contrast, stimulus‐predicting neurons were bimodal and showed similar response profiles across serial‐order elements. Motor cells showed a consecutive activity onset across discrete neural ensembles, generating a rapid succession of activation patterns between the two taps defining a produced interval. The cyclical configuration in activation profiles engaged more motor cells as the serial‐order elements progressed across the task, and the rate of cell recruitment over time decreased as a function of the target interval. Our findings support the idea that motor cells were responsible for the rhythmic progression of taps in the task, gaining more importance as the trial advanced, while, simultaneously, the sensory‐driven cells lost their functional impact.

Behavioral and Neurophysiological Aspects of Target Interception

This chapter focuses on the behavioral and neurophysiological aspects of manual interception. We review the most important elements of an interceptive action from the sensory and cognitive stage to the motor side of this behavior. We describe different spatial and temporal target parameters that can be used to control the interception movement, as well as the different strategies used by the subject to intercept a moving target. We review the neurophysiological properties of the parietofrontal system during target motion processing and during a particular experiment of target interception. Finally, we describe the neural responses associated with the temporal and spatial parameters of a moving target and the possible neurophysiological mechanisms used to integrate this information in order to trigger an interception movement.

Monkeys time their pauses of movement and not their movement-kinematics during a synchronization-continuation rhythmic task

A critical question in tapping behavior is to understand whether the temporal control is exerted on the duration and trajectory of the downward-upward hand movement or on the pause between hand movements. In the present study, we determined the duration of both the movement execution and pauses of monkeys performing a synchronization-continuation task (SCT), using the speed profile of their tapping behavior. We found a linear increase in the variance of pause-duration as a function of interval, while the variance of the motor implementation was relatively constant across intervals. In fact, 96% of the variability of the duration of a complete tapping cycle (pause + movement) was due to the variability of the pause duration. In addition, we performed a Bayesian model selection to determine the effect of interval duration (450-1,000 ms), serial-order (1-6 produced intervals), task phase (sensory cued or internally driven), and marker modality (auditory or visual) on the duration of the movement-pause and tapping movement. The results showed that the most important parameter used to successfully perform the SCT was the control of the pause duration. We also found that the kinematics of the tapping movements was concordant with a stereotyped ballistic control of the hand pressing the push-button. The present findings support the idea that monkeys used an explicit timing strategy to perform the SCT, where a dedicated timing mechanism controlled the duration of the pauses of movement, while also triggered the execution of fixed movements across each interval of the rhythmic sequence.

Linking Perception, Cognition, and Action: Psychophysical Observations and Neural Network Modelling

It has been argued that perception, decision making, and movement planning are in reality tightly interwoven brain processes. However, how they are implemented in neural circuits is still a matter of debate. We tested human subjects in a temporal categorization task in which intervals had to be categorized as short or long. Subjects communicated their decision by moving a cursor into one of two possible targets, which appeared separated by different angles from trial to trial. Even though there was a 1 second-long delay between interval presentation and decision communication, categorization difficulty affected subjects’ performance, reaction (RT) and movement time (MT). In addition, reaction and movement times were also influenced by the distance between the targets. This implies that not only perceptual, but also movement-related considerations were incorporated into the decision process. Therefore, we searched for a model that could use categorization difficulty and target separation to describe subjects’ performance, RT, and MT. We developed a network consisting of two mutually inhibiting neural populations, each tuned to one of the possible categories and composed of an accumulation and a memory node. This network sequentially acquired interval information, maintained it in working memory and was then attracted to one of two possible states, corresponding to a categorical decision. It faithfully replicated subjects’ RT and MT as a function of categorization difficulty and target distance; it also replicated performance as a function of categorization difficulty. Furthermore, this model was used to make new predictions about the effect of untested durations, target distances and delay durations. To our knowledge, this is the first biologically plausible model that has been proposed to account for decision making and communication by integrating both sensory and motor planning information.